Can macroalgae contribute to blue carbon An Australian perspective

Ross Hill1 Alecia Bellgrove2 Peter I Macreadie34 Katherina Petrou3 John Beardall5 Andy Steven6

Peter J Ralph3

1Centre for Marine Bio-Innovation and Sydney Institute of Marine Science School of Biological Earth and EnvironmentalSciences The University of New South Wales Sydney New South Wales Australia

2Centre for Integrative Ecology School of Life amp Environmental Sciences Deakin University Warrnambool VictoriaAustralia

3Plant Functional Biology and Climate Change Cluster University of Technology Sydney Broadway New South WalesAustralia

4Centre for Integrative Ecology Deakin University Burwood Victoria Australia5School of Biological Sciences Monash University Clayton Victoria Australia6Wealth from Oceans Flagship The Commonwealth Scientific and Industrial Research Organisation Dutton ParkQueensland Australia

Abstract

Macroalgal communities in Australia and around the world store vast quantities of carbon in their living

biomass but their prevalence of growing on hard substrata means that they have limited capacity to act as

long-term carbon sinks Unlike other coastal blue carbon habitats such as seagrasses saltmarshes and man-

groves they do not develop their own organic-rich sediments but may instead act as a rich carbon source

and make significant contributions in the form of detritus to sedimentary habitats by acting as a ldquocarbon

donorrdquo to ldquoreceiver sitesrdquo where organic material accumulates The potential for storage of this donated car-

bon however is dependent on the decay rate during transport and the burial efficiency at receiver sites To

better understand the potential contribution of macroalgal communities to coastal blue carbon budgets a

comprehensive literature search was conducted using key words including carbon sequestration macroalgal

distribution abundance and productivity to provide an estimation of the total amount of carbon stored in

temperate Australian macroalgae Our most conservative calculations estimate 1099 Tg C is stored in living

macroalgal biomass of temperate Australia using a coastal area covering 249697 km2 Estimates derived for

tropical and subtropical regions contributed an additional 232 Tg C By extending the search to include

global studies we provide a broader context and rationale for the study contributing to the global aspects of

the review In addition we discuss the potential role of calcium carbonate-containing macroalgae consider

the dynamic nature of macroalgal populations in the context of climate change and identify the knowledge

gaps that once addressed will enable robust quantification of macroalgae in marine biogeochemical cycling

of carbon We conclude that macroalgal communities have the potential to make ecologically meaningful

contributions toward global blue carbon sequestration as donors but given that the fate of detached macro-

algal biomass remains unclear further research is needed to quantify this contribution

Anthropogenic activities since the industrial revolution

such as the burning of fossil fuels industrialization defores-

tation and intensive agricultural practices have rapidly

raised the atmospheric concentration of greenhouse gases

(Bala 2013) The increased abundance of these heat-trapping

gases has resulted in rising global temperatures and is dis-

rupting climatic processes around the globe Carbon dioxide

(CO2) is the greatest contributor to greenhouse gas emissions

and is also responsible for causing ocean acidification

(Doney et al 2009) One third of anthropogenic CO2 emis-

sions dissolve into the oceans which slows the rise in the

atmospheric CO2 concentration but this process reduces

ocean pH (Sabine et al 2004) Over the last 250 yr the CO2

concentration has increased from 280 ppm to over 400 ppm

(Bala 2013) Although this range of concentrations is not

unusual over geological timescales the rate of CO2 increase

is faster than at any time in the last 300 million years

(Heuroonisch et al 2012) As a result the rapid increase in CO2

concentration is having severe impacts on global climate

patterns (eg extreme weather events and loss of habitable

land due to sea level rise) ocean chemistry (eg reduction

in carbonate ion availability required for calcification)Correspondence rosshillmqeduau

1

LIMNOLOGYand

OCEANOGRAPHY Limnol Oceanogr 00 2015 00ndash00VC 2015 Association for the Sciences of Limnology and Oceanography

doi 101002lno10128

biological processes (eg hypercapnia sensing of olfactory

queues) the functioning of ecosystems (eg bleaching and

death of corals) as well as human livelihoods (eg eco-

nomic loses from agricultural activities affected by drought

reduced value of ecosystem services) (Guinotte and Fabry

2008 Doney et al 2009 Hoegh-Guldberg and Bruno 2010

Hilmi et al 2013) While the rising CO2 concentration is

causing widespread problems it is having a positive effect

on the photosynthetic rate of those terrestrial plants that are

otherwise carbon-limited (Long et al 2004 Cornwall et al

2012 Koch et al 2013 Johnson et al 2014)

During the 20th century ocean temperatures rose by

0748C and pH dropped by 01 units (equivalent to a 30

increase in hydrogen ions) (IPCC 2007) Over the next cen-

tury it is predicted global temperatures may rise by a further

48C and pH decline by a further 04 pH units (under the

higher emission A1F1 scenario (IPCC 2007)) Given the

severity of these impacts mitigation of CO2 emissions is of

great importance Carbon capture and storage technologies

engineered to sequester CO2 have been developed but cur-

rently do not represent viable affordable long-term or pro-

ven solutions (Gough 2008 Markewitz et al 2012 Rubin

et al 2012)

Carbon sequestration through photosynthetic carbon fixa-

tion represents an alternative solution to removing CO2

from the atmosphere and if the organic carbon is stored

long-term within the system this represents a viable carbon

sink for mitigating CO2 emissions and climate change

(Duarte et al 2013 Singh and Ahluwalia 2013) Natural ter-

restrial and aquatic carbon sinks are known to represent a

powerful means of storing carbon with both mature (eg

ancient forests or seagrass meadows) and immature ecosys-

tems (eg forest plantations) capable of building carbon

stocks where rates of carbon gain through photosynthesis

exceed counteracting carbon losses from respiration (Grace

2004)

Recently the term ldquoblue carbonrdquo was coined referring to

carbon sinks in vegetated coastal ecosystems (Nellemann

et al 2009) Typically this term refers to the carbon seques-

tered in mangrove forests seagrass beds and salt marshes

(Mcleod et al 2011) The focus of this review however is on

macroalgal populations of coastal ecosystems and the poten-

tial role they play as marine carbon sinks As macroalgae pri-

marily grow on hard substrata it has been assumed they do

not directly contribute to carbon sequestration due to the

absence of soft sediment that accretes as a result of organic

carbon deposition (Duarte et al 2013) However the export

of macroalgal detrital material to other ecosystems such as

the continental margins (Dierssen et al 2009) suggest they

may have the potential to act as significant carbon donors to

other long-term sequestration habitats Australia has approx-

imately 60000 km2 of coastline (Geoscience Australia 2010)

from tropical to cool temperate latitudes where large stands

of macroalgae are a dominant feature of many coastal

regions Here we specifically address the contribution mac-

roalgae could play in carbon sequestration in the Australian

context a region that possesses the greatest biodiversity of

macroalgae globally and high endemism (Phillips 2001) The

findings of this review while based on data from the Austra-

lian coastline are applicable to macroalgal communities

around the world

Blue carbon definitions assumptions andrequirements

Carbon sequestration is the capture and long-term storage

of carbon dioxide from the atmosphere through biological

chemical or physical processes Carbon accumulates in bio-

logical organisms as living biomass but only a fraction of

that carbon becomes sequestered Through photosynthesis

organisms absorb and fix carbon dioxide incorporating it

into their cells for growth however more than 97 of this

fixed carbon is subsequently released back into the atmos-

phere either through plant respiration or the breakdown of

biomass by microbes (Farrelly et al 2013) Therefore while

more than 1550 Gt C is stored in the form of biomass the

loss of carbon via these two pathways results in the net

sequestration of only 5 GtC yr21 (Raven and Falkowski

1999 Sabine et al 2004 Lal 2005 Farrelly et al 2013)

The two most significant sinks for long-term carbon stor-

age (after respiration and remineralization are accounted

for) are terrestrial soils and the deep ocean with the total

stored carbon content estimated at 39300 Gt (Farrelly

et al 2013) The oceans are by far the largest carbon sinks

estimated to hold around 37000 Gt of inorganic carbon

(Raven and Falkowski 1999) with approximately 2 Gt of

additional carbon absorbed each year via physico-chemical

processes (Behrenfeld et al 2002)

As with terrestrial soils sequestered carbon in marine

sediments can remain over geological timescales in the form

of particulate organic carbon (known as blue carbon) unless

disturbed In particular disturbance that oxygenates other-

wise anoxic sediment can activate aerobic bacteria which

through aerobic metabolic pathways may convert recalci-

trant carbon back to CO2 (Hartnett et al 1998) Thus a

change in the redox state of the sediment (from anoxic to

oxic) could potentially increase the efflux of carbon from

these natural sinks

Ocean carbonate can also be stored for geological time-

scales in the form of magnesium and calcium salts (Raven

and Falkowski 1999) The oceans are by far the largest car-

bon sinks estimated to hold around 37000 Gt of inorganic

carbon (Raven and Falkowski 1999) with approximately 2 Gt

of additional carbon absorbed each year via physico-

chemical processes (Behrenfeld et al 2002)

All signatories of the Kyoto Protocol are required to

reduce CO2 emissions either by decreasing the consumption

of fossil fuels or by increasing sequestration particularly by

Hill et al Can macroalgae contribute to blue carbon

2

terrestrial carbon sinks More recently consideration of

coastal systems as carbon sinks has led to increased investi-

gation into understanding carbon cycling and storage in

coastal systems (Pendleton et al 2012) Carbon stock is

formed from a combination of autochthonous (derived from

primary producers within the habitat) and allochthonous

(derived from external sources) carbon One measure of dif-

ferentiating sinks from sources is the use of a production

respiration (P R) ratio Having a P R greater than 1 is said

to be a carbon sink removing and storing more carbon than

is released while a ratio of less than 1 is deemed a net car-

bon source However in the case of some coastal systems

that have a P R of less than 1 if significantly large amounts

of allochthonous carbon gets trapped and sequestered the

system could in fact be a net carbon sink It has already

been suggested that CO2 drawdown and assimilation by cul-

tured and wild-grown macroalgae represents a significant

sink for anthropogenic emissions (Chung et al 2011)

Chung et al (2011) argue that through the correct use of

harvested macroalgae significant contributions to carbon

sequestration and offsetting of greenhouse gas emissions

would be possible Their argument is strongly based on the

high productivity rates of macroalgae compared with higher

plants in the context of crops for biofuel production How-

ever in order for this offset to be effective the carbon fixed

through macroalgal photosynthesis (ie the harvested bio-

mass) would have to be utilised in biofuels as a replacement

of fossil fuel use to ensure a net gain in the reduction of

total emissions as no carbon is stored long-term in this sce-

nario While Chung et al (2011) demonstrates the potential

for carbon sequestration through macroalgal harvesting we

focus here on the contribution of wild macroalgal popula-

tions to carbon sequestration in the oceans

The carbon derived from the primary production of

coastal systems can be transported or donated to other eco-

systems in the form of particulate organic carbon (POC) dis-

solved organic carbon (DOC) and dissolved inorganic

carbon (DIC) Given the complexity involved in measuring

production and export processes such as the amount of car-

bon that is donated its impact on the recipient system and

ultimately its long-term fate a complete understanding of

macroalgae in the coastal marine system and the importance

in managing global carbon stocks is still lacking For macro-

algal communities to be considered significant contributors

to blue carbon they must either have the capacity to

directly store and accumulate carbon within their own habi-

tat or transport biomass to receiver habitats where carbon

can be effectively buried and the organic material prevented

from undergoing microbial remineralization

Like all major blue carbon habitats community produc-

tion (P) by macroalgae generally exceeds respiration (R) thus

making them effective short-term CO2 sinks as carbon is

sequestered into organic matter However given that macro-

algae predominantly grow on rocky substrates long-term

sequestration of this fixed carbon is considered less effective

than that of other blue carbon sources as there is less oppor-

tunity for the assimilated carbon to be accreted in anaerobic

sediments (Duarte et al 2013) Therefore understanding the

role of macroalgal stands as a donor system and the fate of

the carbon that is stored as biomass is of critical importance

In this review we aim to determine whether macroalgae

can contribute to blue carbon We consider the potential for

direct storage of carbon within macroalgal habitats as well

as the contribution macroalgae can make as a carbon donor

to receiver sites where allochthonous carbon accumulates In

our calculations of carbon storage in macroalgal commun-

ities and comparison to other terrestrial and marine carbon

sinks we specifically focus on the Australian continent

though our conclusions are equally applicable to similar eco-

systems worldwide The distribution biomass and productiv-

ity of macroalgal communities are vulnerable to change and

we consider the impact of anthropogenic factors in influenc-

ing the ability of macroalgal habitats to contribute to blue

carbon into the future

Methods

This article presents a review of the research literature on

blue carbon habitats with a focus on Australian coastal mac-

roalgal communities A literature search was conducted on

the electronic database Web of Science to identify publica-

tions on blue carbon carbon sequestration macroalgal dis-

tribution macroalgal abundance macroalgal productivity

physiological and structural properties of macroalgae and

threats to marine communities without restrictions on the

date of publication or geographic location of the study site

Australian-based studies were targeted to gather data on

the distribution abundance and productivity of macroalgal

communities to establish a comprehensive dataset on the

abundance areal extent depth range biomass biomass

turnover growth rate rate of maximum net primary produc-

tion and total carbon stored in living macroalgae in distinct

regions of the Australian coastline The total amount of car-

bon stored in temperate Australian macroalgae (Table 1) was

estimated from data of the most common assemblages This

involved (1) summing published values of total carbon

stored in mixed understorey turfs with Ecklonia radiata and

mixed fucoid assemblages and extrapolated values of mean

total carbon stored in Durvillaea potatorum (based on fwt

dwt ratio of 460 and published value of 0312 gC g21 dwt

Raven et al 1989) (2) multiplying the summed value by the

area of coastal temperate waters to 60 m depth (Whiteway

2009) (3) multiplying the product of (2) by two estimates of

the percentage of rocky reef conducive to supporting macro-

algal populations in temperate Australia based on published

data and a more conservative estimate Similar calculations

were made for tropical Australia based on the scant data

available for the Great Barrier Reef Queensland Further

Hill et al Can macroalgae contribute to blue carbon

3

Tab

le1

C

on

trib

ution

sof

macr

oalg

ae

tosh

ort

-term

carb

on

seq

uest

ration

thro

ug

hout

Aust

ralia

b

ase

don

ava

ilab

led

ata

V

alu

es

rep

rese

nt

those

as

pub

lish

ed

inth

elit

era

ture

exce

pt

wh

ere

oth

erw

ise

ind

icate

db

ysu

pers

crip

tsan

dfo

otn

ote

sto

exp

lain

the

deri

vati

on

of

extr

ap

ola

ted

valu

es

Reg

ion

Lati

tud

eSp

eci

es

Ab

un

dan

ce

co

ver

Are

al

exte

nt

km

2

Dep

th

ran

ge

m

Bio

mass

gm

22

Bio

mass

turn

over

tim

es

yr2

1

Gro

wth

rate

d

21

Gro

wth

mg

g

FW

21

d2

1

Max

net

pro

du

ctio

n

rate

gC

m2

2d

21

To

tal

C

sto

red

inlivin

g

macr

oalg

ae

Mg

Ckm

22

Refe

ren

ces

Nort

hern

GBR

11

8300 S

ndash

15

8350 S

Halim

eda

spp

mead

ow

s

20ndash40

4637

max

525

mean

Dre

wan

d

Ab

e(l

1988)

Nort

hern

GBR

14

8270 S

ndash

15

8020 S

Halim

eda

moun

ds

bio

herm

s

26

shelf

in

nort

hern

sect

ion

of

GBR

2000

(up

to

19

mth

ick)

20ndashgt

50

Mars

hall

an

d

Davi

es

(1988)

Orm

ean

d

Sala

ma

(1988)

Gre

at

Palm

Fan

tom

e

an

dBro

ok

isla

nd

sG

BR

18

8090 S

ndash

18

8410 S

Sarg

ass

um

bacc

ula

ria

2ndash3

190

(AFD

W)

440

3Sch

affelk

ean

d

Klu

mp

p(1

997)

Davi

es

Reef

GBR

18

844

Ep

ilith

icalg

al

com

mun

ity

(cru

stose

cora

llin

es)

20

39

422

daggerK

lum

pp

an

d

McK

inn

on

(1989

1992)

GBR

15

8S

19

8S

25

8S

Ep

ilith

ic

alg

al

com

mun

ity

(turf

s)

60ndash80

reef

sub

stra

te

on

GBR

5ndash20

45

max

30

mean

56

25

253

daggerK

lum

pp

an

d

McK

inn

on

(1989

1992)

Sh

ark

Bay

West

ern

Aust

ralia

26

8D

rift

alg

ae

(pre

dom

inan

tly

Laure

nci

asp

p

Vid

alia

spiralis

Dig

enia

sim

ple

x

an

dEu

cheu

ma

spec

iosu

m)

152

(dw

t-

in

Am

phib

ilos

anta

rctica

bed

)

223

(dw

t-

inPosi

donia

aust

ralis

bed

)

Ken

drick

et

al

(1990)

Moolo

ola

ba

Qld

26

8400 S

Eckl

onia

radia

ta

an

dsu

btid

al

fuco

ids

Turf

s

(multis

peci

es)

0 57

Con

nell

an

d

Irvi

ng

(2008)

Houtm

an

Ab

roh

los

Isla

nd

s

West

ern

Aust

ralia

28

8Sndash29

8SEc

klonia

radia

ta

Red

folio

se

alg

ae

Cru

stose

cora

llin

es

15

15

3

20ndash40

1ndash50

ND

1040

(dw

t)03

Hatc

her

et

al

(1987)

Sm

ale

et

al

(2010)

Balli

na

NSW

28

8520 S

Eckl

onia

radia

ta

an

dsu

btid

al

fuco

ids

Turf

s

(multis

peci

es)

84

15

Con

nell

an

d

Irvi

ng

(2008)

TA

BLE

1

Con

tin

ued

Reg

ion

Lati

tud

eSp

eci

es

Ab

un

dan

ce

co

ver

Are

al

exte

nt

km

2

Dep

th

ran

ge

m

Bio

mass

gm

22

Bio

mass

turn

over

tim

es

yr2

1

Gro

wth

rate

d

21

Gro

wth

mg

g

FW

21

d2

1

Max

net

pro

du

ctio

n

rate

gC

m2

2d

21

To

tal

C

sto

red

inlivin

g

macr

oalg

ae

Mg

Ckm

22

Refe

ren

ces

Rott

nest

Isla

nd

32

8420 S

Eckl

onia

radia

ta

Scy

toth

alia

dory

carp

aRed

folio

sealg

ae

Cru

stose

cora

llin

es

30

4 6 12

1ndash50

1ndash50

1ndash70

ND

Sm

ale

et

al

(2010)

South

ern

Aust

ralia

Coast

33

8050 S

ndash

35

8360 S

Eckl

onia

radia

ta

an

dsu

btid

al

fuco

ids

90

(WA

an

dSA

)

41

(NSW

)

20m

180

00

(ww

tndash

WA

Era

dia

ta)

6(S

A

fuco

ids)

09

(WA

Era

dia

ta)

9(W

A

Era

dia

ta)

6(S

A

fuco

ids)

635 (S

A)

Kirkm

an

(1984

1989)

Ch

esh

ire

et

al

(1996)

Con

nell

an

d

Irvi

ng

(2008)

South

ern

Aust

ralia

Coast

33

8050 S

ndash

35

8510 S

Turf

s

(multis

peci

es)

65

ndash8

(WA

an

dSA

)to

40

wh

ere

can

op

y

rest

rict

ed

(SA

)17

(NSW

)

4an

d10

mfo

r

pro

duct

ivity

measu

res

88ndash100

(AFD

W)

29ndash79

29

(SA

)32ndash36

Cop

ert

ino

et

al

(2005)

Con

nell

an

d

Irvi

ng

(2008)

South

ern

Aust

ralia

Coast

33

8050 S

ndash

35

8360 S

Cru

stose

cora

llin

e

barr

en

s

0(W

Aan

dSA

)

38

(NSW

)

Con

nell

an

d

Irvi

ng

(2008)

South

east

ern

Aust

ralia

35

8Sndash

43

8SD

urv

illaea

pota

toru

m

0ndash5

225

004

891m

ean

1080

002

34

78

max

(ww

td

wt

resp

ect

ively

)

603

sect1526Dagger

Ch

esh

ire

an

d

Halla

m(1

988)

Rave

net

al

(1989)

Vic

toria

(9

of

Vic

coast

line)

38

8110 S

ndash

38

8520 S

Dom

inan

t

macr

oalg

al

ass

em

bla

ges

(pre

dom

inate

ly

ph

aeop

hyte

s

an

drh

od

op

hyte

s)

341

377

10ndash60

Iero

dia

con

ou

et

al

(2007

2011)

Ratt

ray

et

al

(2009)

Ch

eH

asa

n

et

al

(2012)

Mon

ket

al

(2012)

Ratt

ray

et

al

(2013)

Rob

ins

Pass

ag

e

toSw

an

Isla

nd

nort

hco

ast

Tasm

an

ia

40

8420 S

ndash

41

8120 S

Durv

illaea

pota

toru

m

Mix

ed

Era

dia

ta

an

dfu

coid

s

Mix

ed

turf

s

10ndash50

60ndash100

40ndash60

0ndash5

0ndash25

15ndash30

Luci

eer

et

al

(2007b

)

Tasm

an

iandash

east

ern

coast

41

8Sndash

43

8360 S

Macr

ocy

stis

pyr

ifer

a

11

(1940)

131

1(3

45

bed

s1999)

lt1

(2010)

2m

md

21

2400

g

ww

tm

22

yr2

1

San

ders

on

(1990)

Ed

yva

ne

(2003)

Joh

nso

net

al

(2011)

TA

BLE

1

Con

tin

ued

Reg

ion

Lati

tud

eSp

eci

es

Ab

un

dan

ce

co

ver

Are

al

exte

nt

km

2

Dep

th

ran

ge

m

Bio

mass

gm

22

Bio

mass

turn

over

tim

es

yr2

1

Gro

wth

rate

d

21

Gro

wth

mg

g

FW

21

d2

1

Max

net

pro

du

ctio

n

rate

gC

m2

2d

21

To

tal

C

sto

red

inlivin

g

macr

oalg

ae

Mg

Ckm

22

Refe

ren

ces

St

Hele

ns

Poin

t

toSch

oute

n

Isla

nd

SE

Tasm

an

ia

41

8170 S

ndash

42

8S

Tota

lalg

ae

(pre

dom

inan

tly

Phyl

losp

ora

com

osa

an

d

Era

dia

ta)

70ndash100

0ndash25

Eckl

onia

4700

g

ww

tm

22

yr2

1

Phyl

losp

ora

7400

g

ww

tm

22

yr2

1

San

ders

on

(1990)

Luci

eer

et

al

(2007a)

Hig

hYello

w

Blu

ffto

Cap

e

Hauy

Georg

e

III

Rock

SE

Tasm

an

ia

43

8Sndash

43

8300 S

Ph

aeop

hyce

ae

(pre

dom

inan

tly

Era

dia

ta)

Rh

od

op

hyta

Ch

loro

ph

yta

43ndash48

46ndash10

7

20ndash40

20ndash30

to40ndash50

20ndash30

Luci

eer

et

al

(2012)

Valu

es

use

dto

est

imate

carb

on

stora

ge

ass

oci

ated

with

bio

mass

of

south

-east

ern

Aust

ralia

nsu

btid

alm

acr

oalg

ae

daggerV

alu

es

use

dto

est

imate

carb

on

stora

ge

ass

oci

ated

with

bio

mass

of

EA

Con

the

Gre

at

Barr

ier

Reef

DaggerExtr

ap

ola

ted

valu

es

from

pub

lish

ed

dat

ab

ase

don

fwt

d

wt

ratio

of

46

0g

Cg

21

dw

tan

d03

12

gC

g2

1d

wt

(Rave

net

al

1989)

sectExtr

ap

ola

ted

valu

es

from

pub

lish

ed

dat

aan

dass

um

ing

maxim

alp

hoto

syn

thetic

rate

for

12

hd

21

(Rave

net

al

1989)

details and justification for these choices are given in the

next section

Studies from around the world were used for all other pur-

poses of the review and informed the findings from the Aus-

tralian continent in terms of the potential for above- and

below-ground carbon storage across a range of habitats com-

parable to macroalgal communities which are known for

their efficacy in carbon sequestration (terrestrial forests salt-

marshes mangrove forests and seagrass beds) Total carbon

stored in Australia was calculated for each habitat from data

reported in the literature (Table 2) Minimum and maximum

values were calculated by multiplication of the carbon stor-

age capacity per unit area of each habitat type by the area

of that habitat found in Australia Studies from around the

world were also used to provide a rationale for the review

and contributed to the general discussion to provide a global

perspective on calcification decomposition and the influ-

ence of anthropogenic impacts on the blue carbon capacity

of macroalgae

Potential for macroalgae to directly store carbon

Macroalgae are known to have very high rates of primary

productivity and growth and significant biomass on coastal

margins (Mann 1973 Chung et al 2011) particularly in

temperate regions (Mann 1973 Cheshire et al 1996 Connell

and Irving 2008) Macroalgae are typically associated with

hard substrata to which they attach and grow obtaining

their nutritional needs from the surrounding water rather

than via vascular root systems penetrating the sediment As

such and unlike other aquatic macrophytes their biomass is

all ldquoabove groundrdquo with the exception of calcifying algae

that can build up significant calcium carbonate deposits in

the sediments (eg Halimeda in Table 1 and below) and sto-

loniferous taxa such as Caulerpa The capacity for noncalcify-

ing macroalgae to directly store carbon is thus largely

associated with the above ground living biomass and how

long the carbon within living biomass remains fixed before

being remineralized by bacteria

Australia has an extensive coastline with about 30 in

the temperate coastal zone dominated by large macroalgae

such as Durvillaea potatorum (found 0ndash5 m deep) Ecklonia

radiata and mixed fucoids (occurring down to 40 m depth)

including Phyllospora comosa Cystophora spp Sargassum spp

(Table 1) and Scytothalia doryocarpa in the west (Wernberg

et al 2003) However for most of the Australian coast data

on areal extent biomass and productivity of macroalgae are

very fragmented and often reported in non-standardised

units (Table 1) Moreover there are few records of standing

stock of carbon or carbon contents of particular species that

allow extrapolation from available biomass data Thus accu-

rate assessments of the total amount of carbon stored in

Table 2 Organic carbon stored both above and below ground in terrestrial forests and different marine ecosystems in Australia

Ecosystem

Carbon stored (Mg C km22) Area in

Australia

(km2)

Total C

stored in

Australia (Tg C) ReferencesAbove ground Below ground Total

Terrestrial forests 5700ndash21700 6200ndash23000 11900ndash44700 1494000 177786ndash667818 Malhi et al (1999)

Fourqurean

et al (2012)

Department of

Agriculture (2013)

Saltmarsh 67ndash922 207ndash12972 274ndash13894 13029 36ndash1810 Cacador et al (2004)

Howe et al (2009)

OzCoasts (2013)

Mangrove 9750ndash31724 5731ndash67816 16792ndash99540 3976 668ndash3958 Twilley et al (1992)

Howe et al (2009)

Fourqurean

et al (2012)

OzCoasts (2013)

Seagrass 01ndash555 01ndash83678 02ndash84233 296 (temperate

Australia)

21482 (all

of Australia)

592 3 1025ndash249

430 3 1023ndash18095

Fourqurean et al (2012)

Waycott et al (2009)

OzCoasts (2013)

Australian

temperate

macroalgae

2200 0 2200 49939ndash124849 1099ndash2747 This study

Hill et al Can macroalgae contribute to blue carbon

7

living biomass of macroalgae in Australia are at this stage

difficult to determine We estimate however that the coastal

waters of southern Australia with D potatorum in the upper

subtidal and E radiata monospecific andor mixed fucoid

dominated assemblages to 30 m that support an understorey

of turfing algae that may extend to 60 m in depth could

store in excess of 2200 Mg C km22 (Table 1) If we extrapolate

to the temperate coastal waters of Australialt60 m depth

(249697 km2 Whiteway 2009) and assume that approxi-

mately 50 (124849 km2) of coastal waters are rocky reef

(based on data compiled from Victoria Australia in Ierodiaco-

nou et al 2007 Rattray et al 2009 Ierodiaconou et al 2011

Che Hasan et al 2012 Monk et al 2012 Rattray et al 2013)

we estimate 2747 Tg C may be directly stored in living mac-

roalgal biomass in temperate Australia (Table 2) The above

studies targeted reef areas but there are large expanses of

sandy sediments in temperate Australia (eg Ninety-mile

beach Victoria) so if we take a more conservative estimate

of 20 (49939 km2) reef to 60 m we estimate 1099 Tg C

stored in living macroalgal biomass in temperate Australia

(Table 2) For tropical and subtropical Australia data are even

sparser but based on estimates of carbon storage by epilithic

algal communities the Great Barrier Reef may store 232 Tg C

in epilithic algae alone (675 g C m22 3 344400 km2 Table 1)

The capacity for carbon storage per unit area in macroalgae is

generally lower than for other blue carbon habitats and ter-

restrial forests due to the absence of below ground biomass

(Table 2) However the vast extent of temperate macroalgae

communities makes total carbon storage comparable to the

other blue carbon habitats (saltmarsh mangroves and sea-

grass beds) which have both above and below ground carbon

storage (Table 2) We of course acknowledge that there are

temporal and spatial variability in productivity biomass and

carbon content of different species (Table 1) and thus these

values are crude estimates only New data on aerial extent

biomass and carbon storage for algal species and assemblages

from around Australia will improve our estimates Compara-

ble data for other regions are needed for reliable global esti-

mates of carbon storage in macroalgal living biomass

Seasonality in alternation of generations fragmentation

and dislodgment (Thomsen et al 2004 McKenzie and Bell-

grove 2009 Krumhansl et al 2011) of macroalgae all con-

tribute to high turnover of macroalgal biomass High

productivity and growth rates of macroalgae replenish the

biomass There are however no comprehensive data on the

spatial and temporal variability in biomass of any macroalgal

species in Australia (references in Table 1) Assuming rela-

tively stable annual macroalgal standing stock productivity

growth and turnover do not affect the potential for macroal-

gae to directly store carbon in the above ground biomass

High productivity will not result in more carbon storage

unless it equates to greater total biomass However high

rates of productivity growth and turnover do become impor-

tant to carbon-storage potential of macroalgae if we consider

their possible role as carbon donors to other systems which

is a function of their decay rate en route to receiver sites the

burial efficiency of the receiver site and their structural com-

plexity (ie susceptibility to being remineralized) We

explore this role in more detail below (see ldquoMacroalgae as

carbon donorsrdquo)

Calcification in macroalgae

All macroalgal groups contain genera that form calcium

carbonate deposits and calcified algae are found in the

photic zone of all marine habitats from polar to tropical seas

(Nelson 2009) In the Phaeophyceae calcification is most

notable in Padina though a few other brown algae also cal-

cify The calcifying Chlorophyte algae are mostly tropical

and contain genera such as Acetabularia Neomeris Avrainvil-

lea and most importantly in terms of its contribution Hali-

meda Many red algae are calcifying both in tropical and

cold waters but calcification is best known in the Coralli-

nales with both geniculate and nongeniculate or crustose

forms Free-living nongeniculate corallines are known as rho-

doliths and form extensive beds which are harvested in

Europe and elsewhere (eg Brazil) In most cases the calcium

carbonate is found as the mineral aragonite either deposited

at the cell surface (eg Padina) or in intercellular spaces

(eg Halimeda) Calcium carbonate can also be deposited as

calcite which has a different crystal structure to aragonite

making it more stable and less prone to dissolution in sea-

water especially under the lowered carbonate concentrations

likely to be found with increasing ocean acidification in the

future Calcite is found in external crusts on Chaetomorpha

and within the cell walls of coralline genera such as Litho-

phyllum and Lithothamnion (Lobban and Harrison 1994)

Many calcifying algae also grow epiphytically on seagrass

leaves as well as on other marine organisms including

bivalves and molluscs Indeed seagrass photosynthesis can

promote calcification rates by other organisms such as Hali-

meda growing in seagrass beds (Semesi et al 2009)

Although many of the algae that calcify are slow growing

the calcium carbonate (aragonite and especially calcite) can

persist in the marine environment long after the living cells

have decayed Iconic calcium carbonate deposits such as the

White Cliffs of Dover are the remains of marine calcifying

microalgae deposited over geological time The rhodolith

beds in France and Brazil are harvested to the rate of

500 Gg yr21 (Briand 1991) and up to 120 Gg yr21 (Riul et al

2008) respectively for industrial processes including agricul-

ture water purification mineralization and the manufacture

of cosmetics (Grall and Hall-Spencer 2003) Carbonate depo-

sition (accumulation) in coastal waters (including coral reefs)

globally is in the order of 12 Pg CaCO3 yr21 (017 Pg C yr21)

with approximately the same accumulated in the pelagic

ocean though production rates in the open ocean are closer

to 11 Pg C yr21 (Iglesias-Rodriguez et al 2002) Decomposed

Halimeda tissues are important sediment elements in tropical

Hill et al Can macroalgae contribute to blue carbon

8

regions (Table 1) and contribute the major part of the cal-

careous sediment found in the sandy beaches of many tropi-

cal shores Halimeda bioherms alone have been estimated to

contribute 400 Tg CaCO3 yr21 to CaCO3 accumulation (Hillis

1997) Rhodolith forming species can produce in the region

of 60ndash1000 g CaCO3 m22 yr21 with CaCO3 deposits off Bra-

zilrsquos coast alone of 2 Pg (Riul et al 2008 Nelson 2009)

Importantly carbonates deposited by oceanic organisms

have not previously been included in blue carbon budgets

This is because the calcification process (Eq 1) results in the

release of 1 CO2 for every CaCO3 formed

2 HCO23 1Ca21 CaCO31CO21H2O (1)

However the CO2 produced in this way can be rapidly

utilised in photosynthesis and even if it is not (during calcifi-

cation in the dark for instance) there is still the net conver-

sion of one soluble HCO23 into one insoluble carbonate

(ie calcification still results in net drawdown of carbon in

the recalcitrant carbonate minerals aragonite or calcite)

Given the significant contribution of macroalgal calcifica-

tion to the global C budget and the persistence of CaCO3 in

sediments we would argue that calcification should be con-

sidered in any calculations of blue carbon into the future If

included this would constitute a further 034 Pg C yr21

sequestered globally

Macroalgae as carbon donors

So far we have established that most macroalgal species

have limited capacity to act as long-term carbon sinks in

their own right (Table 2) largely due to their inability to

accumulate below-ground stores of carbon relative to other

vegetated coastal habitats such as seagrasses saltmarshes

and mangroves However even though macroalgae do not

develop significant carbon deposits themselves there still

exists the possibility that they could make significant contri-

butions to global carbon sequestration by acting as ldquocarbon

donorsrdquo In this section we explore this possibility

What is a ldquocarbon donorrdquo Here we define a carbon donor

as an autotroph that ldquodonatesrdquo carbon to another ldquoreceiverrdquo

habitat that ultimately buries that carbon Therefore carbon

donors make indirect contributions to carbon sequestration

Such movement of carbon from one system to another is

referred to as ldquoleakagerdquo (or ldquospilloverrdquo) A well-recognised

example of leakage can be seen in seagrass ecosystems Sea-

grasses have a high particle-trapping capacity (Agawin and

Duarte 2002 Gruber and Kemp 2010) and due to their

occurrence at the interface between land and sea they cap-

ture large amounts of terrestrial carbon that runs off the

land following rainfall events (Kennedy et al 2010 Macrea-

die et al 2014) This externally derived carbon that leaks

into a receiver habitat is termed ldquoallochthonousrdquo carbon In

seagrasses allochthonous carbon can contribute as much as

half the total organic carbon that is sequestered in a meadow

(Kennedy et al 2010)

From a carbon accounting perspective leakage of carbon

is a complex issue Can habitats take credit for carbon that

they didnrsquot produce What happens if the carbon was

already credited to another system (double-counting) How

can the origin of carbon be determined These questions are

at the forefront of many terrestrial carbon-offset programs

(eg REDD) but have received comparatively little attention

in the aquatic fields The matter of carbon accounting of

leakage will however become increasingly important with

the rising prominence of blue carbon but is beyond the

scope of this review We recommend Murray et al (2007) for

more information on leakage

For a system to be a significant carbon donor there are

three requirements (1) high rates of biomass production (2)

effective transfer of biomass to receiver habitats and (3) the

donor carbon must undergo efficient burial of allochthonous

biomass within receiver habitats such that it evades micro-

bial attack (the latter is a function of several factors includ-

ing the intrinsic stability of the carbon physical

mechanisms of protection and environmental conditions

that dictate microbial activity) All three requirements are

necessary none are redundant or substitutable The first

requirement has already been discussed earlier in this article

and can be summarised as follows macroalgae have excep-

tionally high biomass production their global extent (2ndash68

million km2) and primary production (019ndash064 Pg C yr21)

exceeds that of all the vegetated coastal habitats (seagrass

beds saltmarshes mangroves) combined (Duarte et al

2013) In the following section we will discuss requirements

2 and 3 which concern the export and fate of this biomass

production

Export and fate of macroalgal biomass

to receiver habitats

Most macroalgal species spend their early life history

attached to benthic (hard) substrata (Leurouning 1990) but then

become dislodged or fragmented and can undergo a period

of transport in surface or bottom waters by wind and water

movement (potentially as rafts that travel significant distan-

ces) until eventually sinking disintegrating or becoming

cast upon land (Thiel 2003 Thiel and Gutow 2005 Macrea-

die et al 2011) Detachment of macroalgal tissue can arise

from natural senescence (Ang 1985) dislodgement by herbi-

vores (Kingsford 1992 Tegner et al 1995) and through

hydrodynamic forces such as waves and storms (Duggins

et al 2003) The supply quality persistence and transport

(trajectory and duration) of macroalgal rafts are all influ-

enced by climate (Macreadie et al 2011) particularly tem-

perature (Graiff et al 2013) Thus whilst there is temporal

variation in the extent of macroalgal rafts related to these

processes there is continuous export of macroalgal biomass

throughout the year whereas saltmarsh and seagrass detrital

Hill et al Can macroalgae contribute to blue carbon

9

export tends to be seasonal (Josselyn and Mathieson 1980)

Furthermore acknowledging spatial variation in the export

of macroalgal and vascular plant biomass macroalgae are

often more significant contributors to surf-zone and beach

wrack than seagrasses (Josselyn and Mathieson 1980 Gomez

et al 2013 Baring et al 2014 Ruiz-Delgado et al 2014)

From genetic and tracking studies we know that exported

macroalgal biomass can be transported long distances (Thiel

and Haye 2006 Fraser et al 2009 2010 2011 Nikula et al

2010) but there is limited information on what happens to

carbon bound within macroalgal biomass once rafts or frag-

ments sink and disintegratemdashie the point at which carbon

bound within macroalgal biomass is broken down into dis-

solved and particulate organic carbon Wada et al (2007)

suggested that macroalgae could release 20ndash40 of their pro-

ductivity as dissolved organic matter (DOM) Much of the

macroalgal DOM is likely to be microbially degraded but

estimates of the refractory component of this DOM will be

important for understanding how much could be donated to

other habitats UV is known to degrade DOM this means

that if this matter can be deposited in regions away from

light such as the deep ocean the breakdown will be further

diminished

There is some evidence to suggest that macroalgal carbon

is donated to other receiver habitats that have long-term

sequestration capacity including the deep sea (Wada et al

2008 Dierssen et al 2009) and other vegetated coastal habi-

tats such as mangrove forests seagrass beds and salt

marshes (Hyndes et al 2012 Macreadie et al 2012) In tropi-

cal estuaries and bays it is estimated that about half of the

macroalgal biomass produced is consumed by herbivores and

the other half is exported to other habitats whereas in the

temperate open coast most of the biomass is decomposed by

detritivores with a lesser amount being exported and only

small fractions being consumed or accumulated as detritus

(Hyndes et al 2013) The fate of macroalgal biomass in tem-

perate estuaries and fjords is largely unknown (Hyndes et al

2013) Most export of macroalgal biomass occurs via advec-

tion but there are also complex biotic pathways that trans-

port macroalgal biomass into receiver habitats such as via

ingestion and concomitant faecal deposition of carbon

within receiver habitats by fish which can contribute to car-

bon sequestration by fertilising receiver habitats and thereby

increasing their productivity and sequestration capacity

(Valiela 1995 Hyndes et al 2013) Breakdown of macroalgae

has been shown to be mostly mediated by microbial proc-

esses (Rieper-Kirchner 1990) however protozoans and meio-

fauna also contribute to the decomposition of macroalgal

tissues as well as enhance microbial degradation Microbial

breakdown rate is also dependent upon the sediment com-

position and oxic status of the water Sassi et al (1988)

found that macroalgal decomposition rates over 25 d under

aerobic vs anaerobic conditions were 35 and 24 respec-

tively Therefore if the macroalgal detritus can be advected

to a rapidly sedimenting region where it can be incorporated

into an anaerobic sediment this will slow the microbial

breakdown and maintain the carbon within the sediment

longer More research is needed to understand how long this

carbon actually remains within anaerobic sediment

All macroalgal carbon that enters the sedimentary carbon

pool will eventually be broken down (oxidised and reminer-

alized) by microbes and converted to inorganic forms and

potentially returned to the atmosphere The rate and effi-

ciency of this remineralization process can dictate whether

macroalgal carbon remains bound within sediments for

months or millennia Macroalgal carbon entering the sedi-

mentary pool has three possible fates (1) particulate and dis-

solved organic carbon that is recalcitrant to microbial

degradation is likely to remain stored within the sediment

for prolonged periods while labile carbon will be recycled by

heterotrophic bacteria and is either (2) assimilated into

microbial biomass or (3) respired as CO2 back to the water

column and possibly the atmosphere The proportion of

nonrespired carbon represents the amount of macroalgal car-

bon that is sequestered

It should be recognised that macroalgae lack the struc-

tural polysaccharide complexity of higher plants and conse-

quently their decomposition rates are faster (Sassi et al

1988) To better understand the degradation pathways of

macroalgal plant material within aquatic sediments

researchers have used several techniques Analyses of ele-

mental composition and stable isotope signatures are rou-

tinely used to ldquofingerprintrdquo carbon and determine its origin

although there is difficultly in separating microalgal and

macroalgal organic carbon signatures (Hardison et al 2011)

Furthermore isotopic signatures may also be variable in

space and time during the decomposition process (Fenton

and Ritz 1988) Similarly a problem with identifying sources

of organic carbon based on carbohydrate composition is that

many groups of organisms contain the same carbohydrates

(Vichkovitten and Holmer 2004) Fatty acid signatures have

proven to offer better resolution of the different plant contri-

butions to organic matter (Hardison et al 2013) although

the level of complexity using this technique is much higher

(Graeve et al 2002) Manipulative approaches using isotopic

tracer studies (Hee et al 2001 Hardison et al 2010 2011

Hyndes et al 2012) and radiolabelling (Chidthaisong et al

1999) have proved to be robust for studying the incorpora-

tion of macroalgal carbon into sediments

Reliable data on the fate of decomposed macroalgal

carbon within sediments (eg macroalgal carbon that is

ldquolostrdquo during litter bag mass loss experiments) is scarce

Hardison et al (2010) traced carbon from senescing macroal-

gae (Gracilaria spp) that were pre-labeled with the 13C stable

isotope and found that 2ndash9 of macroalgal carbon was

incorporated into the sediment This percentage of macroal-

gal carbon uptake by sediments is relatively high suggesting

efficient burial however the fate of this buried carbon was

Hill et al Can macroalgae contribute to blue carbon

10

only monitored for 2 weeks so it is not known whether this

carbon stock was sequestered long-term Other studies sug-

gest that macroalgal carbon is not sequestered long-term For

example Garcia-Robledo et al (2008) found that macroalgal

detritus (tubular and planar Ulva spp) that entered sedimen-

tary organic carbon pools vanished within days after its ini-

tial appearance indicating that carbon from such simple and

ephemeral macroalgae is not retained for durations that

would make them an important component of the long-

term carbon pool within a receiver habitat However given

the diversity in the cell walls and carbon chemistry of mac-

roalgae it is difficult to make conclusions on likely persist-

ence of sequestered macroalgae based on only a handful of

studies

Kristensen (1994) compared the decomposition rate of six

different plant materials (two macroalgae two seagrasses

and two tree leaves) using stepwise thermogravimetry and

found that macroalgae (Fucus vesiculosus and Ulva lactuca)

lost 40ndash44 of their carbon within 70 d whereas seagrasses

(Zostera marina and Ruppia maritima) lost 29ndash55 and tree

leaves (Fagus sylvatica and Rhizophora apiculata) lost only 0ndash

8 Similarly Josselyn and Mathieson (1980) found that

macroalgae (Ascophyllum nodosum and Fucus vesiculosus)

decomposed 3ndash10 times faster than a saltmarsh plant (Spar-

tina alterniflora) and seagrass (Zostera marina) Litter bag stud-

ies have reported a lack of change in sediment carbon

following decomposition of buried macroalgae suggesting

that the organic carbon bound within macroalgal structural

material (eg carbohydrates) is highly labile and rapidly

decomposed by microbes (Vichkovitten and Holmer 2004)

Despite this general pattern of high degradability of macroal-

gae compared with aquatic angiosperms (Trevathan-Tackett

et al in press) there is a high degree of diversity in the

structural complexity of macroalgae particularly in cell-wall

structure and carbon chemistry resulting in high variability

in decay rate estimates within the literature (Rice and Han-

son 1984 Twilley et al 1986 Kristensen 1990 Wada et al

2008 Trevathan-Tackett et al in press)

Nedzarek and Rakusa-Suszczewski (2004) examined the

decomposition of 10 Antarctic macroalgal species finding

they released 80 of the nutrients with the first 3 d of a 69

d decomposition experiment these rates occurred at polar

temperatures (48C) so it would be assumed that tropical

decomposition would be more rapid Similar results were

found with North Sea macroalgae where 50ndash80 of the tis-

sue biomass was lost within 14 d at 188C (Rieper-Kirchner

1990) which included the brown leathery kelp Laminaria

saccharina

Factors influencing the future carbon storage anddonor ability of macroalgae

This review presents a static view on the current state of

carbon cycling sequestration and donor capacity of macroal-

gae with an emphasis on Australian coastal systems In real-

ity the distribution biomass and productivity of these

macroalgae are vulnerable to change due to anthropogenic

activities and as such the dynamic nature of these macroal-

gal systems should be taken into consideration Factors such

as climate change (Duarte et al 2013) and urbanisation (Air-

oldi and Beck 2007 Airoldi et al 2008) can greatly alter the

distribution abundance and productivity of these systems

although the rate of change in global macroalgae population

size remains unknown

Climate change can greatly influence the survival photo-

synthetic capacity growth and competitive interactions of

macroalgae in coastal habitats (Wernberg et al 2011b)

Ocean warming on both the east and west coasts of Australia

have caused pole-ward movement of macroalgal species over

the past five decades (Wernberg et al 2011a) Potentially

hundreds of species are expected to be driven beyond the

edge of the Australian continent as warming continues driv-

ing not only local but global extinctions as 62 of macro-

algal species found in southern Australia are endemic to the

region (Phillips 2001) On the east coast of Australia there

has been a southern retreat of three habitat-forming macro-

algal species (Ecklonia radiata Phyllospora comosa and Durvil-

laea potatorum Millar 2007) and in eastern Tasmania the

once common Macrocystis pyrifera has almost completely dis-

appeared with ocean warming (Edyvane 2003 Johnson et al

2011)

In addition to rising temperatures climate change is

expected to influence macroalgal distribution and productiv-

ity through ocean acidification emergence of marine dis-

eases and shifts in the distribution of consumers In

terrestrial ecosystems there have been climate-driven

increases in global net primary production due to the easing

of critical climatic constraints such as increasing solar radia-

tion from reduced cloud cover (Nemani et al 2003) In the

oceans while increased CO2 dissolution is reducing pH and

disrupting carbonate chemistry this inorganic carbon is a

building block for photosynthesis The predicted changes in

CO2 in the atmosphere over the next 100 yr will translate to

a 25- to 3-fold increase in dissolved CO2 in seawater

although the subsequent drop in pH will cause shifts in the

equilibria between inorganic carbon forms HCO23 concentra-

tions will only rise by 10 and total Ci available for pho-

tosynthesis (HCO23 1 CO2) will thus rise bylt15 However

if CO2 availability is a constraint to the rate of photosynthe-

sis could the more abundant CO2 result in faster macroalgal

growth Most macroalgae have the capacity to use the

HCO23 ion that is dominant in seawater and given that the

HCO23 concentrations will not change much in future an

impact on photosynthesis is unlikely Furthermore most

macroalgae and seagrasses (Beer et al 2014) possess carbon

concentrating mechanisms (CCMs Giordano et al 2005)

which actively take up inorganic carbon (as HCO23 andor

CO2) and thereby accumulate CO2 at the active site of the

Hill et al Can macroalgae contribute to blue carbon

11

CO2-fixing enzyme Rubisco This effectively saturates

Rubisco for CO2 and limits any increased productivity of

macroalgae from elevated atmospheric CO2 and ocean acidi-

fication There are few exceptions mostly subtidal rhodo-

phytes to the rule that macroalgae possess CCMs so

increased CO2 per se is unlikely to increase CO2 drawdown

by coastal primary producers However there are suggestions

that higher CO2 may increase carbon allocation to seagrass

rhizomes under high light (ie in shallow water) and

thereby enhance burial rates (Jiang et al 2010)

Anthropogenic activities such as climate-change-

associated rising sea temperatures are expected to increase

the occurrence of macroalgal diseases through an increased

virulence of opportunistic pathogens as well as reduced

resistance to disease in thermally stressed hosts (Egan et al

2013) For example in the chemically defended macroalgae

Delisea pulchra bacterial bleaching of the thallus occurs in

response to elevated temperatures due to reduced antibacte-

rial chemical defences (Campbell et al 2011 Case et al

2011) Such diseases therefore have the capacity to reduce

macroalgal abundance either through increased consump-

tion (due to reduced herbivory defence) or through direct

host mortality (Goecke et al 2010)

With the delivery of warmer water further south the East

Australian Current not only contracts the range of many

macroalgal species but also extends the range of urchin con-

sumers Urchin barrens are now extensive throughout south-

eastern Australia and are continuing to expand at the detri-

ment of macroalgal populations (Johnson et al 2011) Such

altered ecological interactions with herbivores from this tro-

picalisation of high latitudes are therefore causing macroal-

gal populations to decline in Tasmania

While climate change will have detrimental effects on

macroalgal populations especially in temperate Australia

tropical regions may experience increased macroalgal abun-

dance following thermal pulses on coral-dominated reefs If

temperatures on coral reefs exceed summer averages by as

little as 1ndash28C mass coral bleaching events can occur which

can lead to coral mortality (Hoegh-Guldberg et al 2007)

Phase shifts toward macroalgal-dominated reefs can follow

especially if herbivory has been reduced by overfishing

(McManus et al 2000 Bruno et al 2009 Hughes et al

2010) However not all tropical macroalgal species will bene-

fit from climate change with species such as Chnoospora

implexa expected to decrease in abundance (Bender et al

2013)

When considering the donor capacity of macroalgae algal

rafts have the potential to deliver dislodged macroalgae to

receiver habitats that can bury the carbon and thus enhance

the carbon sink (see above) However changes in climate

will affect raft supply and persistence (Macreadie et al

2011) Increased storm intensities (IPCC 2007) will promote

substratum detachment andor fragmentation and hence

increase the abundance of algal fragments and rafts and

may also increase burial of macroalgal material (Macreadie

et al 2011) Elevated temperatures however may counter

this process by reducing raft longevity due to an increase in

herbivore metabolism and consumption (Macreadie et al

2011) In addition changes in ocean surface currents may

affect advection routes and potential endpoints of deposition

into more or less favorable receiver environments for

sequestration

Given the dynamic nature of macroalgal populations and

changes in abundance and productivity especially from

human activities the potential for carbon storage and export

may be highly variable In considering the role macroalgae

may play in climate change mitigation the factors detailed

above should be taken into account as they are likely to

greatly influence the contribution of macroalgae to blue car-

bon storage

Conclusions and research priorities

Although macroalgal communities in Australia and

around the world produce massive quantities of plant bio-

mass with high organic carbon content the presence of a

hard rocky substrate precludes the potential for long-term

storage of carbon within the macroalgal habitat In isolation

we therefore conclude that macroalgae do not contribute to

blue carbon

However a considerable proportion of macroalgal bio-

mass becomes dislodged from the benthos and is exported

beyond macroalgal habitat boundaries This donor carbon

may be received by habitats with long-term sequestration

capacity such as seagrass beds saltmarshes mangroves and

continental shelf regions Within Australia and globally

geographic differences in macroalgal biomass community

composition and productivity will influence the blue carbon

donor capacity of macroalgae with the greatest contribu-

tions likely to be in the temperate (and possibly polar)

regions In addition to a high rate of biomass production to

be a viable carbon donor macroalgae must be transferred to

a receiver habitat undergo burial and avoid microbial remi-

neralization The fate of detached macroalgal biomass is not

entirely clear and whilst limited data on the composition of

macroalgal biomass indicates that macroalgal carbon is

highly labile recent research has highlighted the potentially

significant role of refractory taxon-specific compounds (car-

bonates long-chain lipids alginates xylans and sulphated

polysaccharides) from macroalgae in contributing to long-

term blue carbon stores (Trevathan-Tackett et al in press)

We therefore conclude that macroalgae have the potential

to make ecologically meaningful contributions toward global

blue carbon sequestration as significant carbon donors but

further research is needed to quantify these contributions

Data on the degradability of macroalgal plant material is

limited to only a handful of taxa so there is considerable

need for additional testing on other taxa The capacity for

Hill et al Can macroalgae contribute to blue carbon

12

any incorporation of organic material from macroalgae into

long-term carbon stores is only possible if the material can

avoid decomposition by microbes potentially by entering a

storage habitat that is a rapidly accreting zone Research

therefore needs to focus on determining the burial rates of

macroalgal tissue at receiver sites which of these sites are

the greatest sink of macroalgal fragments understanding the

environmental conditions that maximise the burial process

and assessing whether burial is fast enough to limit micro-

bial remineralization of the organic macroalgal material

This will also need to include further research identifying

interspecies variation in carbon donor capacity due to rate of

lability and rate of transport to accreting zones In existing

blue carbon habitats methods for identifying macroalgal car-

bon in the storage zone also need to be developed to gauge

historical contributions of macroalgae into these zones

Once these unknowns are addressed the potential for mac-

roalgae to contribute to blue carbon as a carbon donor will

become less ambiguous Focusing future research on these

key areas will provide evidence as to whether macroalgae

should be included under the blue carbon umbrella

Macroalgal aquaculture and the harvesting of natural pop-

ulations are growing industries worldwide and are actions

that can greatly increase the carbon sequestration capacity

afforded by macroalgae (Chung et al 2011) Furthermore

the production of macroalgal biochar (a process involving

the pyrolysis of biomass) for addition to soil may represent

a viable long-term CO2 sink although research in this field

is in its infancy (Lehmann et al 2006 Bird et al 2011)

Given that macroalgal populations have the highest abun-

dance biomass and productivity of all coastal habitats they

not only store an immense amount of carbon in their living

biomass but they also have an outstanding potential to act

as significant carbon donors However macroalgae are vul-

nerable to a range of anthropogenic impacts so it is impor-

tant to protect these ecosystems for their climate-change-

mitigation potential as well as their ecosystem services

References

Agawin N S R and G M Duarte 2002 Evidence of direct

particle trapping by a tropical seagrass meadow Estuaries

25 1205ndash1209 doi101007BF02692217

Airoldi L D Balata and M W Beck 2008 The Gray Zone

Relationships between habitat loss and marine diversity

and their applications in conservation J Exp Mar Biol

Ecol 366 8ndash15 doi101016jjembe200807034

Airoldi L and M W Beck 2007 Loss status and trends for

coastal marine habitats of Europe Oceanogr Mar Biol

Ann Rev 45 345ndash405

Ang P O J 1985 Regeneration studies of Sargassum

siliquosum J ag and S paniculatum J Ag (Phaeophyta

Sargassaceae) Botanical Marina 28 231ndash235 doi101515

botm1985286231

Bala G 2013 Digesting 400 ppm for global mean CO2

concentration Curr Sci 104 1471ndash1472

Baring R J P G Fairweather and R E Lester 2014

Storm versus calm Variation in fauna associated with

drifting macrophytes in sandy beach surf zones J Exp

Mar Biol Ecol 461 397ndash406 doi101016jjembe2014

09011

Beer S M Bjeuroork and J Beardall 2014 Photosynthesis in

the marine environment Wiley

Behrenfeld M J E Mara~non D A Siegel and S B Hooker

2002 Photoacclimation and nutrient-based model of

light-saturated photosynthesis for quantifying oceanic pri-

mary production Mar Ecol Prog Ser 228 103ndash117 doi

103354meps228103

Bender D G Diaz-Pulido and S Dove 2013 The impact of

CO2 emission scenarios and nutrient enrichment on a

common coral reef macroalga is modified by temporal

effects J Phycol 50 203ndash215 doi101111jpy12153

Bird M I C M Wurster P H de Paula Silva A M Bass

and D de Nys 2011 Algal biocharmdashproduction and

properties Bioresour Technol 102 1886ndash1891 doi

101111j1757-1707201101109x

Briand X 1991 Seaweed harvesting in Europe p 293ndash308

In M D Guiry and G Blunden [eds] Seaweed resources

in Europe Uses and potential Wiley

Bruno J F H Sweatman W F Precht E R Selig and V

G W Schutte 2009 Assessing evidence of phase shifts

from coral to macroalgal dominance on coral reefs

Ecology 90 1478ndash1484 doi10189008-17811

Cacador I A L Coasta and C Vale 2004 Carbon storage

in Tagus salt marsh sediments Water Air Soil Pollut Focus

4 701ndash714 doi101023BWAFO000002838884544ce

Campbell A H T Harder S Nielsen S Kjelleberg and P D

Steinberg 2011 Climate change and disease Bleaching of

a chemically defended seaweed Glob Chang Biol 17

2958ndash2970 doi101111j1365-2486201102456x

Case R J S R Longford A H Campbell A Low N Tujula

P D Steinberg and S Kjelleberg 2011 Temperature

induced bacterial virulence and bleaching disease in a

chemically defended marine macroalga Environ Microbiol

13 529ndash537 doi101111j1462-2920201002356x

Che Hasan R D Ierodiaconou and J Monk 2012

Evaluation of four supervised learning methods for Benthic

habitat mapping using backscatter from multi-beam sonar

Remote Sens 4 3427ndash3443 doi103390rs4113427

Cheshire A C and N D Hallam 1988 Biomass and

density of native stands of Durvillaea potatorum (southern

bull-kelp) in south eastern Australia Mar Ecol Prog Ser

48 277ndash283 doi103354meps048277

Cheshire A C G Westphalen A Wenden L J Scriven

and B C Rowland 1996 Photosynthesis and respiration

of phaeophycean-dominated macroalgal communities in

summer and winter Aquat Bot 55 159ndash170 doi

101016S0304-3770(96)01071-6

Hill et al Can macroalgae contribute to blue carbon

13

biological processes (eg hypercapnia sensing of olfactory

queues) the functioning of ecosystems (eg bleaching and

death of corals) as well as human livelihoods (eg eco-

nomic loses from agricultural activities affected by drought

reduced value of ecosystem services) (Guinotte and Fabry

2008 Doney et al 2009 Hoegh-Guldberg and Bruno 2010

Hilmi et al 2013) While the rising CO2 concentration is

causing widespread problems it is having a positive effect

on the photosynthetic rate of those terrestrial plants that are

otherwise carbon-limited (Long et al 2004 Cornwall et al

2012 Koch et al 2013 Johnson et al 2014)

During the 20th century ocean temperatures rose by

0748C and pH dropped by 01 units (equivalent to a 30

increase in hydrogen ions) (IPCC 2007) Over the next cen-

tury it is predicted global temperatures may rise by a further

48C and pH decline by a further 04 pH units (under the

higher emission A1F1 scenario (IPCC 2007)) Given the

severity of these impacts mitigation of CO2 emissions is of

great importance Carbon capture and storage technologies

engineered to sequester CO2 have been developed but cur-

rently do not represent viable affordable long-term or pro-

ven solutions (Gough 2008 Markewitz et al 2012 Rubin

et al 2012)

Carbon sequestration through photosynthetic carbon fixa-

tion represents an alternative solution to removing CO2

from the atmosphere and if the organic carbon is stored

long-term within the system this represents a viable carbon

sink for mitigating CO2 emissions and climate change

(Duarte et al 2013 Singh and Ahluwalia 2013) Natural ter-

restrial and aquatic carbon sinks are known to represent a

powerful means of storing carbon with both mature (eg

ancient forests or seagrass meadows) and immature ecosys-

tems (eg forest plantations) capable of building carbon

stocks where rates of carbon gain through photosynthesis

exceed counteracting carbon losses from respiration (Grace

2004)

Recently the term ldquoblue carbonrdquo was coined referring to

carbon sinks in vegetated coastal ecosystems (Nellemann

et al 2009) Typically this term refers to the carbon seques-

tered in mangrove forests seagrass beds and salt marshes

(Mcleod et al 2011) The focus of this review however is on

macroalgal populations of coastal ecosystems and the poten-

tial role they play as marine carbon sinks As macroalgae pri-

marily grow on hard substrata it has been assumed they do

not directly contribute to carbon sequestration due to the

absence of soft sediment that accretes as a result of organic

carbon deposition (Duarte et al 2013) However the export

of macroalgal detrital material to other ecosystems such as

the continental margins (Dierssen et al 2009) suggest they

may have the potential to act as significant carbon donors to

other long-term sequestration habitats Australia has approx-

imately 60000 km2 of coastline (Geoscience Australia 2010)

from tropical to cool temperate latitudes where large stands

of macroalgae are a dominant feature of many coastal

regions Here we specifically address the contribution mac-

roalgae could play in carbon sequestration in the Australian

context a region that possesses the greatest biodiversity of

macroalgae globally and high endemism (Phillips 2001) The

findings of this review while based on data from the Austra-

lian coastline are applicable to macroalgal communities

around the world

Blue carbon definitions assumptions andrequirements

Carbon sequestration is the capture and long-term storage

of carbon dioxide from the atmosphere through biological

chemical or physical processes Carbon accumulates in bio-

logical organisms as living biomass but only a fraction of

that carbon becomes sequestered Through photosynthesis

organisms absorb and fix carbon dioxide incorporating it

into their cells for growth however more than 97 of this

fixed carbon is subsequently released back into the atmos-

phere either through plant respiration or the breakdown of

biomass by microbes (Farrelly et al 2013) Therefore while

more than 1550 Gt C is stored in the form of biomass the

loss of carbon via these two pathways results in the net

sequestration of only 5 GtC yr21 (Raven and Falkowski

1999 Sabine et al 2004 Lal 2005 Farrelly et al 2013)

The two most significant sinks for long-term carbon stor-

age (after respiration and remineralization are accounted

for) are terrestrial soils and the deep ocean with the total

stored carbon content estimated at 39300 Gt (Farrelly

et al 2013) The oceans are by far the largest carbon sinks

estimated to hold around 37000 Gt of inorganic carbon

(Raven and Falkowski 1999) with approximately 2 Gt of

additional carbon absorbed each year via physico-chemical

processes (Behrenfeld et al 2002)

As with terrestrial soils sequestered carbon in marine

sediments can remain over geological timescales in the form

of particulate organic carbon (known as blue carbon) unless

disturbed In particular disturbance that oxygenates other-

wise anoxic sediment can activate aerobic bacteria which

through aerobic metabolic pathways may convert recalci-

trant carbon back to CO2 (Hartnett et al 1998) Thus a

change in the redox state of the sediment (from anoxic to

oxic) could potentially increase the efflux of carbon from

these natural sinks

Ocean carbonate can also be stored for geological time-

scales in the form of magnesium and calcium salts (Raven

and Falkowski 1999) The oceans are by far the largest car-

bon sinks estimated to hold around 37000 Gt of inorganic

carbon (Raven and Falkowski 1999) with approximately 2 Gt

of additional carbon absorbed each year via physico-

chemical processes (Behrenfeld et al 2002)

All signatories of the Kyoto Protocol are required to

reduce CO2 emissions either by decreasing the consumption

of fossil fuels or by increasing sequestration particularly by

Hill et al Can macroalgae contribute to blue carbon

2

terrestrial carbon sinks More recently consideration of

coastal systems as carbon sinks has led to increased investi-

gation into understanding carbon cycling and storage in

coastal systems (Pendleton et al 2012) Carbon stock is

formed from a combination of autochthonous (derived from

primary producers within the habitat) and allochthonous

(derived from external sources) carbon One measure of dif-

ferentiating sinks from sources is the use of a production

respiration (P R) ratio Having a P R greater than 1 is said

to be a carbon sink removing and storing more carbon than

is released while a ratio of less than 1 is deemed a net car-

bon source However in the case of some coastal systems

that have a P R of less than 1 if significantly large amounts

of allochthonous carbon gets trapped and sequestered the

system could in fact be a net carbon sink It has already

been suggested that CO2 drawdown and assimilation by cul-

tured and wild-grown macroalgae represents a significant

sink for anthropogenic emissions (Chung et al 2011)

Chung et al (2011) argue that through the correct use of

harvested macroalgae significant contributions to carbon

sequestration and offsetting of greenhouse gas emissions

would be possible Their argument is strongly based on the

high productivity rates of macroalgae compared with higher

plants in the context of crops for biofuel production How-

ever in order for this offset to be effective the carbon fixed

through macroalgal photosynthesis (ie the harvested bio-

mass) would have to be utilised in biofuels as a replacement

of fossil fuel use to ensure a net gain in the reduction of

total emissions as no carbon is stored long-term in this sce-

nario While Chung et al (2011) demonstrates the potential

for carbon sequestration through macroalgal harvesting we

focus here on the contribution of wild macroalgal popula-

tions to carbon sequestration in the oceans

The carbon derived from the primary production of

coastal systems can be transported or donated to other eco-

systems in the form of particulate organic carbon (POC) dis-

solved organic carbon (DOC) and dissolved inorganic

carbon (DIC) Given the complexity involved in measuring

production and export processes such as the amount of car-

bon that is donated its impact on the recipient system and

ultimately its long-term fate a complete understanding of

macroalgae in the coastal marine system and the importance

in managing global carbon stocks is still lacking For macro-

algal communities to be considered significant contributors

to blue carbon they must either have the capacity to

directly store and accumulate carbon within their own habi-

tat or transport biomass to receiver habitats where carbon

can be effectively buried and the organic material prevented

from undergoing microbial remineralization

Like all major blue carbon habitats community produc-

tion (P) by macroalgae generally exceeds respiration (R) thus

making them effective short-term CO2 sinks as carbon is

sequestered into organic matter However given that macro-

algae predominantly grow on rocky substrates long-term

sequestration of this fixed carbon is considered less effective

than that of other blue carbon sources as there is less oppor-

tunity for the assimilated carbon to be accreted in anaerobic

sediments (Duarte et al 2013) Therefore understanding the

role of macroalgal stands as a donor system and the fate of

the carbon that is stored as biomass is of critical importance

In this review we aim to determine whether macroalgae

can contribute to blue carbon We consider the potential for

direct storage of carbon within macroalgal habitats as well

as the contribution macroalgae can make as a carbon donor

to receiver sites where allochthonous carbon accumulates In

our calculations of carbon storage in macroalgal commun-

ities and comparison to other terrestrial and marine carbon

sinks we specifically focus on the Australian continent

though our conclusions are equally applicable to similar eco-

systems worldwide The distribution biomass and productiv-

ity of macroalgal communities are vulnerable to change and

we consider the impact of anthropogenic factors in influenc-

ing the ability of macroalgal habitats to contribute to blue

carbon into the future

Methods

This article presents a review of the research literature on

blue carbon habitats with a focus on Australian coastal mac-

roalgal communities A literature search was conducted on

the electronic database Web of Science to identify publica-

tions on blue carbon carbon sequestration macroalgal dis-

tribution macroalgal abundance macroalgal productivity

physiological and structural properties of macroalgae and

threats to marine communities without restrictions on the

date of publication or geographic location of the study site

Australian-based studies were targeted to gather data on

the distribution abundance and productivity of macroalgal

communities to establish a comprehensive dataset on the

abundance areal extent depth range biomass biomass

turnover growth rate rate of maximum net primary produc-

tion and total carbon stored in living macroalgae in distinct

regions of the Australian coastline The total amount of car-

bon stored in temperate Australian macroalgae (Table 1) was

estimated from data of the most common assemblages This

involved (1) summing published values of total carbon

stored in mixed understorey turfs with Ecklonia radiata and

mixed fucoid assemblages and extrapolated values of mean

total carbon stored in Durvillaea potatorum (based on fwt

dwt ratio of 460 and published value of 0312 gC g21 dwt

Raven et al 1989) (2) multiplying the summed value by the

area of coastal temperate waters to 60 m depth (Whiteway

2009) (3) multiplying the product of (2) by two estimates of

the percentage of rocky reef conducive to supporting macro-

algal populations in temperate Australia based on published

data and a more conservative estimate Similar calculations

were made for tropical Australia based on the scant data

available for the Great Barrier Reef Queensland Further

Hill et al Can macroalgae contribute to blue carbon

3

Tab

le1

C

on

trib

ution

sof

macr

oalg

ae

tosh

ort

-term

carb

on

seq

uest

ration

thro

ug

hout

Aust

ralia

b

ase

don

ava

ilab

led

ata

V

alu

es

rep

rese

nt

those

as

pub

lish

ed

inth

elit

era

ture

exce

pt

wh

ere

oth

erw

ise

ind

icate

db

ysu

pers

crip

tsan

dfo

otn

ote

sto

exp

lain

the

deri

vati

on

of

extr

ap

ola

ted

valu

es

Reg

ion

Lati

tud

eSp

eci

es

Ab

un

dan

ce

co

ver

Are

al

exte

nt

km

2

Dep

th

ran

ge

m

Bio

mass

gm

22

Bio

mass

turn

over

tim

es

yr2

1

Gro

wth

rate

d

21

Gro

wth

mg

g

FW

21

d2

1

Max

net

pro

du

ctio

n

rate

gC

m2

2d

21

To

tal

C

sto

red

inlivin

g

macr

oalg

ae

Mg

Ckm

22

Refe

ren

ces

Nort

hern

GBR

11

8300 S

ndash

15

8350 S

Halim

eda

spp

mead

ow

s

20ndash40

4637

max

525

mean

Dre

wan

d

Ab

e(l

1988)

Nort

hern

GBR

14

8270 S

ndash

15

8020 S

Halim

eda

moun

ds

bio

herm

s

26

shelf

in

nort

hern

sect

ion

of

GBR

2000

(up

to

19

mth

ick)

20ndashgt

50

Mars

hall

an

d

Davi

es

(1988)

Orm

ean

d

Sala

ma

(1988)

Gre

at

Palm

Fan

tom

e

an

dBro

ok

isla

nd

sG

BR

18

8090 S

ndash

18

8410 S

Sarg

ass

um

bacc

ula

ria

2ndash3

190

(AFD

W)

440

3Sch

affelk

ean

d

Klu

mp

p(1

997)

Davi

es

Reef

GBR

18

844

Ep

ilith

icalg

al

com

mun

ity

(cru

stose

cora

llin

es)

20

39

422

daggerK

lum

pp

an

d

McK

inn

on

(1989

1992)

GBR

15

8S

19

8S

25

8S

Ep

ilith

ic

alg

al

com

mun

ity

(turf

s)

60ndash80

reef

sub

stra

te

on

GBR

5ndash20

45

max

30

mean

56

25

253

daggerK

lum

pp

an

d

McK

inn

on

(1989

1992)

Sh

ark

Bay

West

ern

Aust

ralia

26

8D

rift

alg

ae

(pre

dom

inan

tly

Laure

nci

asp

p

Vid

alia

spiralis

Dig

enia

sim

ple

x

an

dEu

cheu

ma

spec

iosu

m)

152

(dw

t-

in

Am

phib

ilos

anta

rctica

bed

)

223

(dw

t-

inPosi

donia

aust

ralis

bed

)

Ken

drick

et

al

(1990)

Moolo

ola

ba

Qld

26

8400 S

Eckl

onia

radia

ta

an

dsu

btid

al

fuco

ids

Turf

s

(multis

peci

es)

0 57

Con

nell

an

d

Irvi

ng

(2008)

Houtm

an

Ab

roh

los

Isla

nd

s

West

ern

Aust

ralia

28

8Sndash29

8SEc

klonia

radia

ta

Red

folio

se

alg

ae

Cru

stose

cora

llin

es

15

15

3

20ndash40

1ndash50

ND

1040

(dw

t)03

Hatc

her

et

al

(1987)

Sm

ale

et

al

(2010)

Balli

na

NSW

28

8520 S

Eckl

onia

radia

ta

an

dsu

btid

al

fuco

ids

Turf

s

(multis

peci

es)

84

15

Con

nell

an

d

Irvi

ng

(2008)

TA

BLE

1

Con

tin

ued

Reg

ion

Lati

tud

eSp

eci

es

Ab

un

dan

ce

co

ver

Are

al

exte

nt

km

2

Dep

th

ran

ge

m

Bio

mass

gm

22

Bio

mass

turn

over

tim

es

yr2

1

Gro

wth

rate

d

21

Gro

wth

mg

g

FW

21

d2

1

Max

net

pro

du

ctio

n

rate

gC

m2

2d

21

To

tal

C

sto

red

inlivin

g

macr

oalg

ae

Mg

Ckm

22

Refe

ren

ces

Rott

nest

Isla

nd

32

8420 S

Eckl

onia

radia

ta

Scy

toth

alia

dory

carp

aRed

folio

sealg

ae

Cru

stose

cora

llin

es

30

4 6 12

1ndash50

1ndash50

1ndash70

ND

Sm

ale

et

al

(2010)

South

ern

Aust

ralia

Coast

33

8050 S

ndash

35

8360 S

Eckl

onia

radia

ta

an

dsu

btid

al

fuco

ids

90

(WA

an

dSA

)

41

(NSW

)

20m

180

00

(ww

tndash

WA

Era

dia

ta)

6(S

A

fuco

ids)

09

(WA

Era

dia

ta)

9(W

A

Era

dia

ta)

6(S

A

fuco

ids)

635 (S

A)

Kirkm

an

(1984

1989)

Ch

esh

ire

et

al

(1996)

Con

nell

an

d

Irvi

ng

(2008)

South

ern

Aust

ralia

Coast

33

8050 S

ndash

35

8510 S

Turf

s

(multis

peci

es)

65

ndash8

(WA

an

dSA

)to

40

wh

ere

can

op

y

rest

rict

ed

(SA

)17

(NSW

)

4an

d10

mfo

r

pro

duct

ivity

measu

res

88ndash100

(AFD

W)

29ndash79

29

(SA

)32ndash36

Cop

ert

ino

et

al

(2005)

Con

nell

an

d

Irvi

ng

(2008)

South

ern

Aust

ralia

Coast

33

8050 S

ndash

35

8360 S

Cru

stose

cora

llin

e

barr

en

s

0(W

Aan

dSA

)

38

(NSW

)

Con

nell

an

d

Irvi

ng

(2008)

South

east

ern

Aust

ralia

35

8Sndash

43

8SD

urv

illaea

pota

toru

m

0ndash5

225

004

891m

ean

1080

002

34

78

max

(ww

td

wt

resp

ect

ively

)

603

sect1526Dagger

Ch

esh

ire

an

d

Halla

m(1

988)

Rave

net

al

(1989)

Vic

toria

(9

of

Vic

coast

line)

38

8110 S

ndash

38

8520 S

Dom

inan

t

macr

oalg

al

ass

em

bla

ges

(pre

dom

inate

ly

ph

aeop

hyte

s

an

drh

od

op

hyte

s)

341

377

10ndash60

Iero

dia

con

ou

et

al

(2007

2011)

Ratt

ray

et

al

(2009)

Ch

eH

asa

n

et

al

(2012)

Mon

ket

al

(2012)

Ratt

ray

et

al

(2013)

Rob

ins

Pass

ag

e

toSw

an

Isla

nd

nort

hco

ast

Tasm

an

ia

40

8420 S

ndash

41

8120 S

Durv

illaea

pota

toru

m

Mix

ed

Era

dia

ta

an

dfu

coid

s

Mix

ed

turf

s

10ndash50

60ndash100

40ndash60

0ndash5

0ndash25

15ndash30

Luci

eer

et

al

(2007b

)

Tasm

an

iandash

east

ern

coast

41

8Sndash

43

8360 S

Macr

ocy

stis

pyr

ifer

a

11

(1940)

131

1(3

45

bed

s1999)

lt1

(2010)

2m

md

21

2400

g

ww

tm

22

yr2

1

San

ders

on

(1990)

Ed

yva

ne

(2003)

Joh

nso

net

al

(2011)

TA

BLE

1

Con

tin

ued

Reg

ion

Lati

tud

eSp

eci

es

Ab

un

dan

ce

co

ver

Are

al

exte

nt

km

2

Dep

th

ran

ge

m

Bio

mass

gm

22

Bio

mass

turn

over

tim

es

yr2

1

Gro

wth

rate

d

21

Gro

wth

mg

g

FW

21

d2

1

Max

net

pro

du

ctio

n

rate

gC

m2

2d

21

To

tal

C

sto

red

inlivin

g

macr

oalg

ae

Mg

Ckm

22

Refe

ren

ces

St

Hele

ns

Poin

t

toSch

oute

n

Isla

nd

SE

Tasm

an

ia

41

8170 S

ndash

42

8S

Tota

lalg

ae

(pre

dom

inan

tly

Phyl

losp

ora

com

osa

an

d

Era

dia

ta)

70ndash100

0ndash25

Eckl

onia

4700

g

ww

tm

22

yr2

1

Phyl

losp

ora

7400

g

ww

tm

22

yr2

1

San

ders

on

(1990)

Luci

eer

et

al

(2007a)

Hig

hYello

w

Blu

ffto

Cap

e

Hauy

Georg

e

III

Rock

SE

Tasm

an

ia

43

8Sndash

43

8300 S

Ph

aeop

hyce

ae

(pre

dom

inan

tly

Era

dia

ta)

Rh

od

op

hyta

Ch

loro

ph

yta

43ndash48

46ndash10

7

20ndash40

20ndash30

to40ndash50

20ndash30

Luci

eer

et

al

(2012)

Valu

es

use

dto

est

imate

carb

on

stora

ge

ass

oci

ated

with

bio

mass

of

south

-east

ern

Aust

ralia

nsu

btid

alm

acr

oalg

ae

daggerV

alu

es

use

dto

est

imate

carb

on

stora

ge

ass

oci

ated

with

bio

mass

of

EA

Con

the

Gre

at

Barr

ier

Reef

DaggerExtr

ap

ola

ted

valu

es

from

pub

lish

ed

dat

ab

ase

don

fwt

d

wt

ratio

of

46

0g

Cg

21

dw

tan

d03

12

gC

g2

1d

wt

(Rave

net

al

1989)

sectExtr

ap

ola

ted

valu

es

from

pub

lish

ed

dat

aan

dass

um

ing

maxim

alp

hoto

syn

thetic

rate

for

12

hd

21

(Rave

net

al

1989)

details and justification for these choices are given in the

next section

Studies from around the world were used for all other pur-

poses of the review and informed the findings from the Aus-

tralian continent in terms of the potential for above- and

below-ground carbon storage across a range of habitats com-

parable to macroalgal communities which are known for

their efficacy in carbon sequestration (terrestrial forests salt-

marshes mangrove forests and seagrass beds) Total carbon

stored in Australia was calculated for each habitat from data

reported in the literature (Table 2) Minimum and maximum

values were calculated by multiplication of the carbon stor-

age capacity per unit area of each habitat type by the area

of that habitat found in Australia Studies from around the

world were also used to provide a rationale for the review

and contributed to the general discussion to provide a global

perspective on calcification decomposition and the influ-

ence of anthropogenic impacts on the blue carbon capacity

of macroalgae

Potential for macroalgae to directly store carbon

Macroalgae are known to have very high rates of primary

productivity and growth and significant biomass on coastal

margins (Mann 1973 Chung et al 2011) particularly in

temperate regions (Mann 1973 Cheshire et al 1996 Connell

and Irving 2008) Macroalgae are typically associated with

hard substrata to which they attach and grow obtaining

their nutritional needs from the surrounding water rather

than via vascular root systems penetrating the sediment As

such and unlike other aquatic macrophytes their biomass is

all ldquoabove groundrdquo with the exception of calcifying algae

that can build up significant calcium carbonate deposits in

the sediments (eg Halimeda in Table 1 and below) and sto-

loniferous taxa such as Caulerpa The capacity for noncalcify-

ing macroalgae to directly store carbon is thus largely

associated with the above ground living biomass and how

long the carbon within living biomass remains fixed before

being remineralized by bacteria

Australia has an extensive coastline with about 30 in

the temperate coastal zone dominated by large macroalgae

such as Durvillaea potatorum (found 0ndash5 m deep) Ecklonia

radiata and mixed fucoids (occurring down to 40 m depth)

including Phyllospora comosa Cystophora spp Sargassum spp

(Table 1) and Scytothalia doryocarpa in the west (Wernberg

et al 2003) However for most of the Australian coast data

on areal extent biomass and productivity of macroalgae are

very fragmented and often reported in non-standardised

units (Table 1) Moreover there are few records of standing

stock of carbon or carbon contents of particular species that

allow extrapolation from available biomass data Thus accu-

rate assessments of the total amount of carbon stored in

Table 2 Organic carbon stored both above and below ground in terrestrial forests and different marine ecosystems in Australia

Ecosystem

Carbon stored (Mg C km22) Area in

Australia

(km2)

Total C

stored in

Australia (Tg C) ReferencesAbove ground Below ground Total

Terrestrial forests 5700ndash21700 6200ndash23000 11900ndash44700 1494000 177786ndash667818 Malhi et al (1999)

Fourqurean

et al (2012)

Department of

Agriculture (2013)

Saltmarsh 67ndash922 207ndash12972 274ndash13894 13029 36ndash1810 Cacador et al (2004)

Howe et al (2009)

OzCoasts (2013)

Mangrove 9750ndash31724 5731ndash67816 16792ndash99540 3976 668ndash3958 Twilley et al (1992)

Howe et al (2009)

Fourqurean

et al (2012)

OzCoasts (2013)

Seagrass 01ndash555 01ndash83678 02ndash84233 296 (temperate

Australia)

21482 (all

of Australia)

592 3 1025ndash249

430 3 1023ndash18095

Fourqurean et al (2012)

Waycott et al (2009)

OzCoasts (2013)

Australian

temperate

macroalgae

2200 0 2200 49939ndash124849 1099ndash2747 This study

Hill et al Can macroalgae contribute to blue carbon

7

living biomass of macroalgae in Australia are at this stage

difficult to determine We estimate however that the coastal

waters of southern Australia with D potatorum in the upper

subtidal and E radiata monospecific andor mixed fucoid

dominated assemblages to 30 m that support an understorey

of turfing algae that may extend to 60 m in depth could

store in excess of 2200 Mg C km22 (Table 1) If we extrapolate

to the temperate coastal waters of Australialt60 m depth

(249697 km2 Whiteway 2009) and assume that approxi-

mately 50 (124849 km2) of coastal waters are rocky reef

(based on data compiled from Victoria Australia in Ierodiaco-

nou et al 2007 Rattray et al 2009 Ierodiaconou et al 2011

Che Hasan et al 2012 Monk et al 2012 Rattray et al 2013)

we estimate 2747 Tg C may be directly stored in living mac-

roalgal biomass in temperate Australia (Table 2) The above

studies targeted reef areas but there are large expanses of

sandy sediments in temperate Australia (eg Ninety-mile

beach Victoria) so if we take a more conservative estimate

of 20 (49939 km2) reef to 60 m we estimate 1099 Tg C

stored in living macroalgal biomass in temperate Australia

(Table 2) For tropical and subtropical Australia data are even

sparser but based on estimates of carbon storage by epilithic

algal communities the Great Barrier Reef may store 232 Tg C

in epilithic algae alone (675 g C m22 3 344400 km2 Table 1)

The capacity for carbon storage per unit area in macroalgae is

generally lower than for other blue carbon habitats and ter-

restrial forests due to the absence of below ground biomass

(Table 2) However the vast extent of temperate macroalgae

communities makes total carbon storage comparable to the

other blue carbon habitats (saltmarsh mangroves and sea-

grass beds) which have both above and below ground carbon

storage (Table 2) We of course acknowledge that there are

temporal and spatial variability in productivity biomass and

carbon content of different species (Table 1) and thus these

values are crude estimates only New data on aerial extent

biomass and carbon storage for algal species and assemblages

from around Australia will improve our estimates Compara-

ble data for other regions are needed for reliable global esti-

mates of carbon storage in macroalgal living biomass

Seasonality in alternation of generations fragmentation

and dislodgment (Thomsen et al 2004 McKenzie and Bell-

grove 2009 Krumhansl et al 2011) of macroalgae all con-

tribute to high turnover of macroalgal biomass High

productivity and growth rates of macroalgae replenish the

biomass There are however no comprehensive data on the

spatial and temporal variability in biomass of any macroalgal

species in Australia (references in Table 1) Assuming rela-

tively stable annual macroalgal standing stock productivity

growth and turnover do not affect the potential for macroal-

gae to directly store carbon in the above ground biomass

High productivity will not result in more carbon storage

unless it equates to greater total biomass However high

rates of productivity growth and turnover do become impor-

tant to carbon-storage potential of macroalgae if we consider

their possible role as carbon donors to other systems which

is a function of their decay rate en route to receiver sites the

burial efficiency of the receiver site and their structural com-

plexity (ie susceptibility to being remineralized) We

explore this role in more detail below (see ldquoMacroalgae as

carbon donorsrdquo)

Calcification in macroalgae

All macroalgal groups contain genera that form calcium

carbonate deposits and calcified algae are found in the

photic zone of all marine habitats from polar to tropical seas

(Nelson 2009) In the Phaeophyceae calcification is most

notable in Padina though a few other brown algae also cal-

cify The calcifying Chlorophyte algae are mostly tropical

and contain genera such as Acetabularia Neomeris Avrainvil-

lea and most importantly in terms of its contribution Hali-

meda Many red algae are calcifying both in tropical and

cold waters but calcification is best known in the Coralli-

nales with both geniculate and nongeniculate or crustose

forms Free-living nongeniculate corallines are known as rho-

doliths and form extensive beds which are harvested in

Europe and elsewhere (eg Brazil) In most cases the calcium

carbonate is found as the mineral aragonite either deposited

at the cell surface (eg Padina) or in intercellular spaces

(eg Halimeda) Calcium carbonate can also be deposited as

calcite which has a different crystal structure to aragonite

making it more stable and less prone to dissolution in sea-

water especially under the lowered carbonate concentrations

likely to be found with increasing ocean acidification in the

future Calcite is found in external crusts on Chaetomorpha

and within the cell walls of coralline genera such as Litho-

phyllum and Lithothamnion (Lobban and Harrison 1994)

Many calcifying algae also grow epiphytically on seagrass

leaves as well as on other marine organisms including

bivalves and molluscs Indeed seagrass photosynthesis can

promote calcification rates by other organisms such as Hali-

meda growing in seagrass beds (Semesi et al 2009)

Although many of the algae that calcify are slow growing

the calcium carbonate (aragonite and especially calcite) can

persist in the marine environment long after the living cells

have decayed Iconic calcium carbonate deposits such as the

White Cliffs of Dover are the remains of marine calcifying

microalgae deposited over geological time The rhodolith

beds in France and Brazil are harvested to the rate of

500 Gg yr21 (Briand 1991) and up to 120 Gg yr21 (Riul et al

2008) respectively for industrial processes including agricul-

ture water purification mineralization and the manufacture

of cosmetics (Grall and Hall-Spencer 2003) Carbonate depo-

sition (accumulation) in coastal waters (including coral reefs)

globally is in the order of 12 Pg CaCO3 yr21 (017 Pg C yr21)

with approximately the same accumulated in the pelagic

ocean though production rates in the open ocean are closer

to 11 Pg C yr21 (Iglesias-Rodriguez et al 2002) Decomposed

Halimeda tissues are important sediment elements in tropical

Hill et al Can macroalgae contribute to blue carbon

8

regions (Table 1) and contribute the major part of the cal-

careous sediment found in the sandy beaches of many tropi-

cal shores Halimeda bioherms alone have been estimated to

contribute 400 Tg CaCO3 yr21 to CaCO3 accumulation (Hillis

1997) Rhodolith forming species can produce in the region

of 60ndash1000 g CaCO3 m22 yr21 with CaCO3 deposits off Bra-

zilrsquos coast alone of 2 Pg (Riul et al 2008 Nelson 2009)

Importantly carbonates deposited by oceanic organisms

have not previously been included in blue carbon budgets

This is because the calcification process (Eq 1) results in the

release of 1 CO2 for every CaCO3 formed

2 HCO23 1Ca21 CaCO31CO21H2O (1)

However the CO2 produced in this way can be rapidly

utilised in photosynthesis and even if it is not (during calcifi-

cation in the dark for instance) there is still the net conver-

sion of one soluble HCO23 into one insoluble carbonate

(ie calcification still results in net drawdown of carbon in

the recalcitrant carbonate minerals aragonite or calcite)

Given the significant contribution of macroalgal calcifica-

tion to the global C budget and the persistence of CaCO3 in

sediments we would argue that calcification should be con-

sidered in any calculations of blue carbon into the future If

included this would constitute a further 034 Pg C yr21

sequestered globally

Macroalgae as carbon donors

So far we have established that most macroalgal species

have limited capacity to act as long-term carbon sinks in

their own right (Table 2) largely due to their inability to

accumulate below-ground stores of carbon relative to other

vegetated coastal habitats such as seagrasses saltmarshes

and mangroves However even though macroalgae do not

develop significant carbon deposits themselves there still

exists the possibility that they could make significant contri-

butions to global carbon sequestration by acting as ldquocarbon

donorsrdquo In this section we explore this possibility

What is a ldquocarbon donorrdquo Here we define a carbon donor

as an autotroph that ldquodonatesrdquo carbon to another ldquoreceiverrdquo

habitat that ultimately buries that carbon Therefore carbon

donors make indirect contributions to carbon sequestration

Such movement of carbon from one system to another is

referred to as ldquoleakagerdquo (or ldquospilloverrdquo) A well-recognised

example of leakage can be seen in seagrass ecosystems Sea-

grasses have a high particle-trapping capacity (Agawin and

Duarte 2002 Gruber and Kemp 2010) and due to their

occurrence at the interface between land and sea they cap-

ture large amounts of terrestrial carbon that runs off the

land following rainfall events (Kennedy et al 2010 Macrea-

die et al 2014) This externally derived carbon that leaks

into a receiver habitat is termed ldquoallochthonousrdquo carbon In

seagrasses allochthonous carbon can contribute as much as

half the total organic carbon that is sequestered in a meadow

(Kennedy et al 2010)

From a carbon accounting perspective leakage of carbon

is a complex issue Can habitats take credit for carbon that

they didnrsquot produce What happens if the carbon was

already credited to another system (double-counting) How

can the origin of carbon be determined These questions are

at the forefront of many terrestrial carbon-offset programs

(eg REDD) but have received comparatively little attention

in the aquatic fields The matter of carbon accounting of

leakage will however become increasingly important with

the rising prominence of blue carbon but is beyond the

scope of this review We recommend Murray et al (2007) for

more information on leakage

For a system to be a significant carbon donor there are

three requirements (1) high rates of biomass production (2)

effective transfer of biomass to receiver habitats and (3) the

donor carbon must undergo efficient burial of allochthonous

biomass within receiver habitats such that it evades micro-

bial attack (the latter is a function of several factors includ-

ing the intrinsic stability of the carbon physical

mechanisms of protection and environmental conditions

that dictate microbial activity) All three requirements are

necessary none are redundant or substitutable The first

requirement has already been discussed earlier in this article

and can be summarised as follows macroalgae have excep-

tionally high biomass production their global extent (2ndash68

million km2) and primary production (019ndash064 Pg C yr21)

exceeds that of all the vegetated coastal habitats (seagrass

beds saltmarshes mangroves) combined (Duarte et al

2013) In the following section we will discuss requirements

2 and 3 which concern the export and fate of this biomass

production

Export and fate of macroalgal biomass

to receiver habitats

Most macroalgal species spend their early life history

attached to benthic (hard) substrata (Leurouning 1990) but then

become dislodged or fragmented and can undergo a period

of transport in surface or bottom waters by wind and water

movement (potentially as rafts that travel significant distan-

ces) until eventually sinking disintegrating or becoming

cast upon land (Thiel 2003 Thiel and Gutow 2005 Macrea-

die et al 2011) Detachment of macroalgal tissue can arise

from natural senescence (Ang 1985) dislodgement by herbi-

vores (Kingsford 1992 Tegner et al 1995) and through

hydrodynamic forces such as waves and storms (Duggins

et al 2003) The supply quality persistence and transport

(trajectory and duration) of macroalgal rafts are all influ-

enced by climate (Macreadie et al 2011) particularly tem-

perature (Graiff et al 2013) Thus whilst there is temporal

variation in the extent of macroalgal rafts related to these

processes there is continuous export of macroalgal biomass

throughout the year whereas saltmarsh and seagrass detrital

Hill et al Can macroalgae contribute to blue carbon

9

export tends to be seasonal (Josselyn and Mathieson 1980)

Furthermore acknowledging spatial variation in the export

of macroalgal and vascular plant biomass macroalgae are

often more significant contributors to surf-zone and beach

wrack than seagrasses (Josselyn and Mathieson 1980 Gomez

et al 2013 Baring et al 2014 Ruiz-Delgado et al 2014)

From genetic and tracking studies we know that exported

macroalgal biomass can be transported long distances (Thiel

and Haye 2006 Fraser et al 2009 2010 2011 Nikula et al

2010) but there is limited information on what happens to

carbon bound within macroalgal biomass once rafts or frag-

ments sink and disintegratemdashie the point at which carbon

bound within macroalgal biomass is broken down into dis-

solved and particulate organic carbon Wada et al (2007)

suggested that macroalgae could release 20ndash40 of their pro-

ductivity as dissolved organic matter (DOM) Much of the

macroalgal DOM is likely to be microbially degraded but

estimates of the refractory component of this DOM will be

important for understanding how much could be donated to

other habitats UV is known to degrade DOM this means

that if this matter can be deposited in regions away from

light such as the deep ocean the breakdown will be further

diminished

There is some evidence to suggest that macroalgal carbon

is donated to other receiver habitats that have long-term

sequestration capacity including the deep sea (Wada et al

2008 Dierssen et al 2009) and other vegetated coastal habi-

tats such as mangrove forests seagrass beds and salt

marshes (Hyndes et al 2012 Macreadie et al 2012) In tropi-

cal estuaries and bays it is estimated that about half of the

macroalgal biomass produced is consumed by herbivores and

the other half is exported to other habitats whereas in the

temperate open coast most of the biomass is decomposed by

detritivores with a lesser amount being exported and only

small fractions being consumed or accumulated as detritus

(Hyndes et al 2013) The fate of macroalgal biomass in tem-

perate estuaries and fjords is largely unknown (Hyndes et al

2013) Most export of macroalgal biomass occurs via advec-

tion but there are also complex biotic pathways that trans-

port macroalgal biomass into receiver habitats such as via

ingestion and concomitant faecal deposition of carbon

within receiver habitats by fish which can contribute to car-

bon sequestration by fertilising receiver habitats and thereby

increasing their productivity and sequestration capacity

(Valiela 1995 Hyndes et al 2013) Breakdown of macroalgae

has been shown to be mostly mediated by microbial proc-

esses (Rieper-Kirchner 1990) however protozoans and meio-

fauna also contribute to the decomposition of macroalgal

tissues as well as enhance microbial degradation Microbial

breakdown rate is also dependent upon the sediment com-

position and oxic status of the water Sassi et al (1988)

found that macroalgal decomposition rates over 25 d under

aerobic vs anaerobic conditions were 35 and 24 respec-

tively Therefore if the macroalgal detritus can be advected

to a rapidly sedimenting region where it can be incorporated

into an anaerobic sediment this will slow the microbial

breakdown and maintain the carbon within the sediment

longer More research is needed to understand how long this

carbon actually remains within anaerobic sediment

All macroalgal carbon that enters the sedimentary carbon

pool will eventually be broken down (oxidised and reminer-

alized) by microbes and converted to inorganic forms and

potentially returned to the atmosphere The rate and effi-

ciency of this remineralization process can dictate whether

macroalgal carbon remains bound within sediments for

months or millennia Macroalgal carbon entering the sedi-

mentary pool has three possible fates (1) particulate and dis-

solved organic carbon that is recalcitrant to microbial

degradation is likely to remain stored within the sediment

for prolonged periods while labile carbon will be recycled by

heterotrophic bacteria and is either (2) assimilated into

microbial biomass or (3) respired as CO2 back to the water

column and possibly the atmosphere The proportion of

nonrespired carbon represents the amount of macroalgal car-

bon that is sequestered

It should be recognised that macroalgae lack the struc-

tural polysaccharide complexity of higher plants and conse-

quently their decomposition rates are faster (Sassi et al

1988) To better understand the degradation pathways of

macroalgal plant material within aquatic sediments

researchers have used several techniques Analyses of ele-

mental composition and stable isotope signatures are rou-

tinely used to ldquofingerprintrdquo carbon and determine its origin

although there is difficultly in separating microalgal and

macroalgal organic carbon signatures (Hardison et al 2011)

Furthermore isotopic signatures may also be variable in

space and time during the decomposition process (Fenton

and Ritz 1988) Similarly a problem with identifying sources

of organic carbon based on carbohydrate composition is that

many groups of organisms contain the same carbohydrates

(Vichkovitten and Holmer 2004) Fatty acid signatures have

proven to offer better resolution of the different plant contri-

butions to organic matter (Hardison et al 2013) although

the level of complexity using this technique is much higher

(Graeve et al 2002) Manipulative approaches using isotopic

tracer studies (Hee et al 2001 Hardison et al 2010 2011

Hyndes et al 2012) and radiolabelling (Chidthaisong et al

1999) have proved to be robust for studying the incorpora-

tion of macroalgal carbon into sediments

Reliable data on the fate of decomposed macroalgal

carbon within sediments (eg macroalgal carbon that is

ldquolostrdquo during litter bag mass loss experiments) is scarce

Hardison et al (2010) traced carbon from senescing macroal-

gae (Gracilaria spp) that were pre-labeled with the 13C stable

isotope and found that 2ndash9 of macroalgal carbon was

incorporated into the sediment This percentage of macroal-

gal carbon uptake by sediments is relatively high suggesting

efficient burial however the fate of this buried carbon was

Hill et al Can macroalgae contribute to blue carbon

10

only monitored for 2 weeks so it is not known whether this

carbon stock was sequestered long-term Other studies sug-

gest that macroalgal carbon is not sequestered long-term For

example Garcia-Robledo et al (2008) found that macroalgal

detritus (tubular and planar Ulva spp) that entered sedimen-

tary organic carbon pools vanished within days after its ini-

tial appearance indicating that carbon from such simple and

ephemeral macroalgae is not retained for durations that

would make them an important component of the long-

term carbon pool within a receiver habitat However given

the diversity in the cell walls and carbon chemistry of mac-

roalgae it is difficult to make conclusions on likely persist-

ence of sequestered macroalgae based on only a handful of

studies

Kristensen (1994) compared the decomposition rate of six

different plant materials (two macroalgae two seagrasses

and two tree leaves) using stepwise thermogravimetry and

found that macroalgae (Fucus vesiculosus and Ulva lactuca)

lost 40ndash44 of their carbon within 70 d whereas seagrasses

(Zostera marina and Ruppia maritima) lost 29ndash55 and tree

leaves (Fagus sylvatica and Rhizophora apiculata) lost only 0ndash

8 Similarly Josselyn and Mathieson (1980) found that

macroalgae (Ascophyllum nodosum and Fucus vesiculosus)

decomposed 3ndash10 times faster than a saltmarsh plant (Spar-

tina alterniflora) and seagrass (Zostera marina) Litter bag stud-

ies have reported a lack of change in sediment carbon

following decomposition of buried macroalgae suggesting

that the organic carbon bound within macroalgal structural

material (eg carbohydrates) is highly labile and rapidly

decomposed by microbes (Vichkovitten and Holmer 2004)

Despite this general pattern of high degradability of macroal-

gae compared with aquatic angiosperms (Trevathan-Tackett

et al in press) there is a high degree of diversity in the

structural complexity of macroalgae particularly in cell-wall

structure and carbon chemistry resulting in high variability

in decay rate estimates within the literature (Rice and Han-

son 1984 Twilley et al 1986 Kristensen 1990 Wada et al

2008 Trevathan-Tackett et al in press)

Nedzarek and Rakusa-Suszczewski (2004) examined the

decomposition of 10 Antarctic macroalgal species finding

they released 80 of the nutrients with the first 3 d of a 69

d decomposition experiment these rates occurred at polar

temperatures (48C) so it would be assumed that tropical

decomposition would be more rapid Similar results were

found with North Sea macroalgae where 50ndash80 of the tis-

sue biomass was lost within 14 d at 188C (Rieper-Kirchner

1990) which included the brown leathery kelp Laminaria

saccharina

Factors influencing the future carbon storage anddonor ability of macroalgae

This review presents a static view on the current state of

carbon cycling sequestration and donor capacity of macroal-

gae with an emphasis on Australian coastal systems In real-

ity the distribution biomass and productivity of these

macroalgae are vulnerable to change due to anthropogenic

activities and as such the dynamic nature of these macroal-

gal systems should be taken into consideration Factors such

as climate change (Duarte et al 2013) and urbanisation (Air-

oldi and Beck 2007 Airoldi et al 2008) can greatly alter the

distribution abundance and productivity of these systems

although the rate of change in global macroalgae population

size remains unknown

Climate change can greatly influence the survival photo-

synthetic capacity growth and competitive interactions of

macroalgae in coastal habitats (Wernberg et al 2011b)

Ocean warming on both the east and west coasts of Australia

have caused pole-ward movement of macroalgal species over

the past five decades (Wernberg et al 2011a) Potentially

hundreds of species are expected to be driven beyond the

edge of the Australian continent as warming continues driv-

ing not only local but global extinctions as 62 of macro-

algal species found in southern Australia are endemic to the

region (Phillips 2001) On the east coast of Australia there

has been a southern retreat of three habitat-forming macro-

algal species (Ecklonia radiata Phyllospora comosa and Durvil-

laea potatorum Millar 2007) and in eastern Tasmania the

once common Macrocystis pyrifera has almost completely dis-

appeared with ocean warming (Edyvane 2003 Johnson et al

2011)

In addition to rising temperatures climate change is

expected to influence macroalgal distribution and productiv-

ity through ocean acidification emergence of marine dis-

eases and shifts in the distribution of consumers In

terrestrial ecosystems there have been climate-driven

increases in global net primary production due to the easing

of critical climatic constraints such as increasing solar radia-

tion from reduced cloud cover (Nemani et al 2003) In the

oceans while increased CO2 dissolution is reducing pH and

disrupting carbonate chemistry this inorganic carbon is a

building block for photosynthesis The predicted changes in

CO2 in the atmosphere over the next 100 yr will translate to

a 25- to 3-fold increase in dissolved CO2 in seawater

although the subsequent drop in pH will cause shifts in the

equilibria between inorganic carbon forms HCO23 concentra-

tions will only rise by 10 and total Ci available for pho-

tosynthesis (HCO23 1 CO2) will thus rise bylt15 However

if CO2 availability is a constraint to the rate of photosynthe-

sis could the more abundant CO2 result in faster macroalgal

growth Most macroalgae have the capacity to use the

HCO23 ion that is dominant in seawater and given that the

HCO23 concentrations will not change much in future an

impact on photosynthesis is unlikely Furthermore most

macroalgae and seagrasses (Beer et al 2014) possess carbon

concentrating mechanisms (CCMs Giordano et al 2005)

which actively take up inorganic carbon (as HCO23 andor

CO2) and thereby accumulate CO2 at the active site of the

Hill et al Can macroalgae contribute to blue carbon

11

CO2-fixing enzyme Rubisco This effectively saturates

Rubisco for CO2 and limits any increased productivity of

macroalgae from elevated atmospheric CO2 and ocean acidi-

fication There are few exceptions mostly subtidal rhodo-

phytes to the rule that macroalgae possess CCMs so

increased CO2 per se is unlikely to increase CO2 drawdown

by coastal primary producers However there are suggestions

that higher CO2 may increase carbon allocation to seagrass

rhizomes under high light (ie in shallow water) and

thereby enhance burial rates (Jiang et al 2010)

Anthropogenic activities such as climate-change-

associated rising sea temperatures are expected to increase

the occurrence of macroalgal diseases through an increased

virulence of opportunistic pathogens as well as reduced

resistance to disease in thermally stressed hosts (Egan et al

2013) For example in the chemically defended macroalgae

Delisea pulchra bacterial bleaching of the thallus occurs in

response to elevated temperatures due to reduced antibacte-

rial chemical defences (Campbell et al 2011 Case et al

2011) Such diseases therefore have the capacity to reduce

macroalgal abundance either through increased consump-

tion (due to reduced herbivory defence) or through direct

host mortality (Goecke et al 2010)

With the delivery of warmer water further south the East

Australian Current not only contracts the range of many

macroalgal species but also extends the range of urchin con-

sumers Urchin barrens are now extensive throughout south-

eastern Australia and are continuing to expand at the detri-

ment of macroalgal populations (Johnson et al 2011) Such

altered ecological interactions with herbivores from this tro-

picalisation of high latitudes are therefore causing macroal-

gal populations to decline in Tasmania

While climate change will have detrimental effects on

macroalgal populations especially in temperate Australia

tropical regions may experience increased macroalgal abun-

dance following thermal pulses on coral-dominated reefs If

temperatures on coral reefs exceed summer averages by as

little as 1ndash28C mass coral bleaching events can occur which

can lead to coral mortality (Hoegh-Guldberg et al 2007)

Phase shifts toward macroalgal-dominated reefs can follow

especially if herbivory has been reduced by overfishing

(McManus et al 2000 Bruno et al 2009 Hughes et al

2010) However not all tropical macroalgal species will bene-

fit from climate change with species such as Chnoospora

implexa expected to decrease in abundance (Bender et al

2013)

When considering the donor capacity of macroalgae algal

rafts have the potential to deliver dislodged macroalgae to

receiver habitats that can bury the carbon and thus enhance

the carbon sink (see above) However changes in climate

will affect raft supply and persistence (Macreadie et al

2011) Increased storm intensities (IPCC 2007) will promote

substratum detachment andor fragmentation and hence

increase the abundance of algal fragments and rafts and

may also increase burial of macroalgal material (Macreadie

et al 2011) Elevated temperatures however may counter

this process by reducing raft longevity due to an increase in

herbivore metabolism and consumption (Macreadie et al

2011) In addition changes in ocean surface currents may

affect advection routes and potential endpoints of deposition

into more or less favorable receiver environments for

sequestration

Given the dynamic nature of macroalgal populations and

changes in abundance and productivity especially from

human activities the potential for carbon storage and export

may be highly variable In considering the role macroalgae

may play in climate change mitigation the factors detailed

above should be taken into account as they are likely to

greatly influence the contribution of macroalgae to blue car-

bon storage

Conclusions and research priorities

Although macroalgal communities in Australia and

around the world produce massive quantities of plant bio-

mass with high organic carbon content the presence of a

hard rocky substrate precludes the potential for long-term

storage of carbon within the macroalgal habitat In isolation

we therefore conclude that macroalgae do not contribute to

blue carbon

However a considerable proportion of macroalgal bio-

mass becomes dislodged from the benthos and is exported

beyond macroalgal habitat boundaries This donor carbon

may be received by habitats with long-term sequestration

capacity such as seagrass beds saltmarshes mangroves and

continental shelf regions Within Australia and globally

geographic differences in macroalgal biomass community

composition and productivity will influence the blue carbon

donor capacity of macroalgae with the greatest contribu-

tions likely to be in the temperate (and possibly polar)

regions In addition to a high rate of biomass production to

be a viable carbon donor macroalgae must be transferred to

a receiver habitat undergo burial and avoid microbial remi-

neralization The fate of detached macroalgal biomass is not

entirely clear and whilst limited data on the composition of

macroalgal biomass indicates that macroalgal carbon is

highly labile recent research has highlighted the potentially

significant role of refractory taxon-specific compounds (car-

bonates long-chain lipids alginates xylans and sulphated

polysaccharides) from macroalgae in contributing to long-

term blue carbon stores (Trevathan-Tackett et al in press)

We therefore conclude that macroalgae have the potential

to make ecologically meaningful contributions toward global

blue carbon sequestration as significant carbon donors but

further research is needed to quantify these contributions

Data on the degradability of macroalgal plant material is

limited to only a handful of taxa so there is considerable

need for additional testing on other taxa The capacity for

Hill et al Can macroalgae contribute to blue carbon

12

any incorporation of organic material from macroalgae into

long-term carbon stores is only possible if the material can

avoid decomposition by microbes potentially by entering a

storage habitat that is a rapidly accreting zone Research

therefore needs to focus on determining the burial rates of

macroalgal tissue at receiver sites which of these sites are

the greatest sink of macroalgal fragments understanding the

environmental conditions that maximise the burial process

and assessing whether burial is fast enough to limit micro-

bial remineralization of the organic macroalgal material

This will also need to include further research identifying

interspecies variation in carbon donor capacity due to rate of

lability and rate of transport to accreting zones In existing

blue carbon habitats methods for identifying macroalgal car-

bon in the storage zone also need to be developed to gauge

historical contributions of macroalgae into these zones

Once these unknowns are addressed the potential for mac-

roalgae to contribute to blue carbon as a carbon donor will

become less ambiguous Focusing future research on these

key areas will provide evidence as to whether macroalgae

should be included under the blue carbon umbrella

Macroalgal aquaculture and the harvesting of natural pop-

ulations are growing industries worldwide and are actions

that can greatly increase the carbon sequestration capacity

afforded by macroalgae (Chung et al 2011) Furthermore

the production of macroalgal biochar (a process involving

the pyrolysis of biomass) for addition to soil may represent

a viable long-term CO2 sink although research in this field

is in its infancy (Lehmann et al 2006 Bird et al 2011)

Given that macroalgal populations have the highest abun-

dance biomass and productivity of all coastal habitats they

not only store an immense amount of carbon in their living

biomass but they also have an outstanding potential to act

as significant carbon donors However macroalgae are vul-

nerable to a range of anthropogenic impacts so it is impor-

tant to protect these ecosystems for their climate-change-

mitigation potential as well as their ecosystem services

References

Agawin N S R and G M Duarte 2002 Evidence of direct

particle trapping by a tropical seagrass meadow Estuaries

25 1205ndash1209 doi101007BF02692217

Airoldi L D Balata and M W Beck 2008 The Gray Zone

Relationships between habitat loss and marine diversity

and their applications in conservation J Exp Mar Biol

Ecol 366 8ndash15 doi101016jjembe200807034

Airoldi L and M W Beck 2007 Loss status and trends for

coastal marine habitats of Europe Oceanogr Mar Biol

Ann Rev 45 345ndash405

Ang P O J 1985 Regeneration studies of Sargassum

siliquosum J ag and S paniculatum J Ag (Phaeophyta

Sargassaceae) Botanical Marina 28 231ndash235 doi101515

botm1985286231

Bala G 2013 Digesting 400 ppm for global mean CO2

concentration Curr Sci 104 1471ndash1472

Baring R J P G Fairweather and R E Lester 2014

Storm versus calm Variation in fauna associated with

drifting macrophytes in sandy beach surf zones J Exp

Mar Biol Ecol 461 397ndash406 doi101016jjembe2014

09011

Beer S M Bjeuroork and J Beardall 2014 Photosynthesis in

the marine environment Wiley

Behrenfeld M J E Mara~non D A Siegel and S B Hooker

2002 Photoacclimation and nutrient-based model of

light-saturated photosynthesis for quantifying oceanic pri-

mary production Mar Ecol Prog Ser 228 103ndash117 doi

103354meps228103

Bender D G Diaz-Pulido and S Dove 2013 The impact of

CO2 emission scenarios and nutrient enrichment on a

common coral reef macroalga is modified by temporal

effects J Phycol 50 203ndash215 doi101111jpy12153

Bird M I C M Wurster P H de Paula Silva A M Bass

and D de Nys 2011 Algal biocharmdashproduction and

properties Bioresour Technol 102 1886ndash1891 doi

101111j1757-1707201101109x

Briand X 1991 Seaweed harvesting in Europe p 293ndash308

In M D Guiry and G Blunden [eds] Seaweed resources

in Europe Uses and potential Wiley

Bruno J F H Sweatman W F Precht E R Selig and V

G W Schutte 2009 Assessing evidence of phase shifts

from coral to macroalgal dominance on coral reefs

Ecology 90 1478ndash1484 doi10189008-17811

Cacador I A L Coasta and C Vale 2004 Carbon storage

in Tagus salt marsh sediments Water Air Soil Pollut Focus

4 701ndash714 doi101023BWAFO000002838884544ce

Campbell A H T Harder S Nielsen S Kjelleberg and P D

Steinberg 2011 Climate change and disease Bleaching of

a chemically defended seaweed Glob Chang Biol 17

2958ndash2970 doi101111j1365-2486201102456x

Case R J S R Longford A H Campbell A Low N Tujula

P D Steinberg and S Kjelleberg 2011 Temperature

induced bacterial virulence and bleaching disease in a

chemically defended marine macroalga Environ Microbiol

13 529ndash537 doi101111j1462-2920201002356x

Che Hasan R D Ierodiaconou and J Monk 2012

Evaluation of four supervised learning methods for Benthic

habitat mapping using backscatter from multi-beam sonar

Remote Sens 4 3427ndash3443 doi103390rs4113427

Cheshire A C and N D Hallam 1988 Biomass and

density of native stands of Durvillaea potatorum (southern

bull-kelp) in south eastern Australia Mar Ecol Prog Ser

48 277ndash283 doi103354meps048277

Cheshire A C G Westphalen A Wenden L J Scriven

and B C Rowland 1996 Photosynthesis and respiration

of phaeophycean-dominated macroalgal communities in

summer and winter Aquat Bot 55 159ndash170 doi

101016S0304-3770(96)01071-6

Hill et al Can macroalgae contribute to blue carbon

13

terrestrial carbon sinks More recently consideration of

coastal systems as carbon sinks has led to increased investi-

gation into understanding carbon cycling and storage in

coastal systems (Pendleton et al 2012) Carbon stock is

formed from a combination of autochthonous (derived from

primary producers within the habitat) and allochthonous

(derived from external sources) carbon One measure of dif-

ferentiating sinks from sources is the use of a production

respiration (P R) ratio Having a P R greater than 1 is said

to be a carbon sink removing and storing more carbon than

is released while a ratio of less than 1 is deemed a net car-

bon source However in the case of some coastal systems

that have a P R of less than 1 if significantly large amounts

of allochthonous carbon gets trapped and sequestered the

system could in fact be a net carbon sink It has already

been suggested that CO2 drawdown and assimilation by cul-

tured and wild-grown macroalgae represents a significant

sink for anthropogenic emissions (Chung et al 2011)

Chung et al (2011) argue that through the correct use of

harvested macroalgae significant contributions to carbon

sequestration and offsetting of greenhouse gas emissions

would be possible Their argument is strongly based on the

high productivity rates of macroalgae compared with higher

plants in the context of crops for biofuel production How-

ever in order for this offset to be effective the carbon fixed

through macroalgal photosynthesis (ie the harvested bio-

mass) would have to be utilised in biofuels as a replacement

of fossil fuel use to ensure a net gain in the reduction of

total emissions as no carbon is stored long-term in this sce-

nario While Chung et al (2011) demonstrates the potential

for carbon sequestration through macroalgal harvesting we

focus here on the contribution of wild macroalgal popula-

tions to carbon sequestration in the oceans

The carbon derived from the primary production of

coastal systems can be transported or donated to other eco-

systems in the form of particulate organic carbon (POC) dis-

solved organic carbon (DOC) and dissolved inorganic

carbon (DIC) Given the complexity involved in measuring

production and export processes such as the amount of car-

bon that is donated its impact on the recipient system and

ultimately its long-term fate a complete understanding of

macroalgae in the coastal marine system and the importance

in managing global carbon stocks is still lacking For macro-

algal communities to be considered significant contributors

to blue carbon they must either have the capacity to

directly store and accumulate carbon within their own habi-

tat or transport biomass to receiver habitats where carbon

can be effectively buried and the organic material prevented

from undergoing microbial remineralization

Like all major blue carbon habitats community produc-

tion (P) by macroalgae generally exceeds respiration (R) thus

making them effective short-term CO2 sinks as carbon is

sequestered into organic matter However given that macro-

algae predominantly grow on rocky substrates long-term

sequestration of this fixed carbon is considered less effective

than that of other blue carbon sources as there is less oppor-

tunity for the assimilated carbon to be accreted in anaerobic

sediments (Duarte et al 2013) Therefore understanding the

role of macroalgal stands as a donor system and the fate of

the carbon that is stored as biomass is of critical importance

In this review we aim to determine whether macroalgae

can contribute to blue carbon We consider the potential for

direct storage of carbon within macroalgal habitats as well

as the contribution macroalgae can make as a carbon donor

to receiver sites where allochthonous carbon accumulates In

our calculations of carbon storage in macroalgal commun-

ities and comparison to other terrestrial and marine carbon

sinks we specifically focus on the Australian continent

though our conclusions are equally applicable to similar eco-

systems worldwide The distribution biomass and productiv-

ity of macroalgal communities are vulnerable to change and

we consider the impact of anthropogenic factors in influenc-

ing the ability of macroalgal habitats to contribute to blue

carbon into the future

Methods

This article presents a review of the research literature on

blue carbon habitats with a focus on Australian coastal mac-

roalgal communities A literature search was conducted on

the electronic database Web of Science to identify publica-

tions on blue carbon carbon sequestration macroalgal dis-

tribution macroalgal abundance macroalgal productivity

physiological and structural properties of macroalgae and

threats to marine communities without restrictions on the

date of publication or geographic location of the study site

Australian-based studies were targeted to gather data on

the distribution abundance and productivity of macroalgal

communities to establish a comprehensive dataset on the

abundance areal extent depth range biomass biomass

turnover growth rate rate of maximum net primary produc-

tion and total carbon stored in living macroalgae in distinct

regions of the Australian coastline The total amount of car-

bon stored in temperate Australian macroalgae (Table 1) was

estimated from data of the most common assemblages This

involved (1) summing published values of total carbon

stored in mixed understorey turfs with Ecklonia radiata and

mixed fucoid assemblages and extrapolated values of mean

total carbon stored in Durvillaea potatorum (based on fwt

dwt ratio of 460 and published value of 0312 gC g21 dwt

Raven et al 1989) (2) multiplying the summed value by the

area of coastal temperate waters to 60 m depth (Whiteway

2009) (3) multiplying the product of (2) by two estimates of

the percentage of rocky reef conducive to supporting macro-

algal populations in temperate Australia based on published

data and a more conservative estimate Similar calculations

were made for tropical Australia based on the scant data

available for the Great Barrier Reef Queensland Further

Hill et al Can macroalgae contribute to blue carbon

3

Tab

le1

C

on

trib

ution

sof

macr

oalg

ae

tosh

ort

-term

carb

on

seq

uest

ration

thro

ug

hout

Aust

ralia

b

ase

don

ava

ilab

led

ata

V

alu

es

rep

rese

nt

those

as

pub

lish

ed

inth

elit

era

ture

exce

pt

wh

ere

oth

erw

ise

ind

icate

db

ysu

pers

crip

tsan

dfo

otn

ote

sto

exp

lain

the

deri

vati

on

of

extr

ap

ola

ted

valu

es

Reg

ion

Lati

tud

eSp

eci

es

Ab

un

dan

ce

co

ver

Are

al

exte

nt

km

2

Dep

th

ran

ge

m

Bio

mass

gm

22

Bio

mass

turn

over

tim

es

yr2

1

Gro

wth

rate

d

21

Gro

wth

mg

g

FW

21

d2

1

Max

net

pro

du

ctio

n

rate

gC

m2

2d

21

To

tal

C

sto

red

inlivin

g

macr

oalg

ae

Mg

Ckm

22

Refe

ren

ces

Nort

hern

GBR

11

8300 S

ndash

15

8350 S

Halim

eda

spp

mead

ow

s

20ndash40

4637

max

525

mean

Dre

wan

d

Ab

e(l

1988)

Nort

hern

GBR

14

8270 S

ndash

15

8020 S

Halim

eda

moun

ds

bio

herm

s

26

shelf

in

nort

hern

sect

ion

of

GBR

2000

(up

to

19

mth

ick)

20ndashgt

50

Mars

hall

an

d

Davi

es

(1988)

Orm

ean

d

Sala

ma

(1988)

Gre

at

Palm

Fan

tom

e

an

dBro

ok

isla

nd

sG

BR

18

8090 S

ndash

18

8410 S

Sarg

ass

um

bacc

ula

ria

2ndash3

190

(AFD

W)

440

3Sch

affelk

ean

d

Klu

mp

p(1

997)

Davi

es

Reef

GBR

18

844

Ep

ilith

icalg

al

com

mun

ity

(cru

stose

cora

llin

es)

20

39

422

daggerK

lum

pp

an

d

McK

inn

on

(1989

1992)

GBR

15

8S

19

8S

25

8S

Ep

ilith

ic

alg

al

com

mun

ity

(turf

s)

60ndash80

reef

sub

stra

te

on

GBR

5ndash20

45

max

30

mean

56

25

253

daggerK

lum

pp

an

d

McK

inn

on

(1989

1992)

Sh

ark

Bay

West

ern

Aust

ralia

26

8D

rift

alg

ae

(pre

dom

inan

tly

Laure

nci

asp

p

Vid

alia

spiralis

Dig

enia

sim

ple

x

an

dEu

cheu

ma

spec

iosu

m)

152

(dw

t-

in

Am

phib

ilos

anta

rctica

bed

)

223

(dw

t-

inPosi

donia

aust

ralis

bed

)

Ken

drick

et

al

(1990)

Moolo

ola

ba

Qld

26

8400 S

Eckl

onia

radia

ta

an

dsu

btid

al

fuco

ids

Turf

s

(multis

peci

es)

0 57

Con

nell

an

d

Irvi

ng

(2008)

Houtm

an

Ab

roh

los

Isla

nd

s

West

ern

Aust

ralia

28

8Sndash29

8SEc

klonia

radia

ta

Red

folio

se

alg

ae

Cru

stose

cora

llin

es

15

15

3

20ndash40

1ndash50

ND

1040

(dw

t)03

Hatc

her

et

al

(1987)

Sm

ale

et

al

(2010)

Balli

na

NSW

28

8520 S

Eckl

onia

radia

ta

an

dsu

btid

al

fuco

ids

Turf

s

(multis

peci

es)

84

15

Con

nell

an

d

Irvi

ng

(2008)

TA

BLE

1

Con

tin

ued

Reg

ion

Lati

tud

eSp

eci

es

Ab

un

dan

ce

co

ver

Are

al

exte

nt

km

2

Dep

th

ran

ge

m

Bio

mass

gm

22

Bio

mass

turn

over

tim

es

yr2

1

Gro

wth

rate

d

21

Gro

wth

mg

g

FW

21

d2

1

Max

net

pro

du

ctio

n

rate

gC

m2

2d

21

To

tal

C

sto

red

inlivin

g

macr

oalg

ae

Mg

Ckm

22

Refe

ren

ces

Rott

nest

Isla

nd

32

8420 S

Eckl

onia

radia

ta

Scy

toth

alia

dory

carp

aRed

folio

sealg

ae

Cru

stose

cora

llin

es

30

4 6 12

1ndash50

1ndash50

1ndash70

ND

Sm

ale

et

al

(2010)

South

ern

Aust

ralia

Coast

33

8050 S

ndash

35

8360 S

Eckl

onia

radia

ta

an

dsu

btid

al

fuco

ids

90

(WA

an

dSA

)

41

(NSW

)

20m

180

00

(ww

tndash

WA

Era

dia

ta)

6(S

A

fuco

ids)

09

(WA

Era

dia

ta)

9(W

A

Era

dia

ta)

6(S

A

fuco

ids)

635 (S

A)

Kirkm

an

(1984

1989)

Ch

esh

ire

et

al

(1996)

Con

nell

an

d

Irvi

ng

(2008)

South

ern

Aust

ralia

Coast

33

8050 S

ndash

35

8510 S

Turf

s

(multis

peci

es)

65

ndash8

(WA

an

dSA

)to

40

wh

ere

can

op

y

rest

rict

ed

(SA

)17

(NSW

)

4an

d10

mfo

r

pro

duct

ivity

measu

res

88ndash100

(AFD

W)

29ndash79

29

(SA

)32ndash36

Cop

ert

ino

et

al

(2005)

Con

nell

an

d

Irvi

ng

(2008)

South

ern

Aust

ralia

Coast

33

8050 S

ndash

35

8360 S

Cru

stose

cora

llin

e

barr

en

s

0(W

Aan

dSA

)

38

(NSW

)

Con

nell

an

d

Irvi

ng

(2008)

South

east

ern

Aust

ralia

35

8Sndash

43

8SD

urv

illaea

pota

toru

m

0ndash5

225

004

891m

ean

1080

002

34

78

max

(ww

td

wt

resp

ect

ively

)

603

sect1526Dagger

Ch

esh

ire

an

d

Halla

m(1

988)

Rave

net

al

(1989)

Vic

toria

(9

of

Vic

coast

line)

38

8110 S

ndash

38

8520 S

Dom

inan

t

macr

oalg

al

ass

em

bla

ges

(pre

dom

inate

ly

ph

aeop

hyte

s

an

drh

od

op

hyte

s)

341

377

10ndash60

Iero

dia

con

ou

et

al

(2007

2011)

Ratt

ray

et

al

(2009)

Ch

eH

asa

n

et

al

(2012)

Mon

ket

al

(2012)

Ratt

ray

et

al

(2013)

Rob

ins

Pass

ag

e

toSw

an

Isla

nd

nort

hco

ast

Tasm

an

ia

40

8420 S

ndash

41

8120 S

Durv

illaea

pota

toru

m

Mix

ed

Era

dia

ta

an

dfu

coid

s

Mix

ed

turf

s

10ndash50

60ndash100

40ndash60

0ndash5

0ndash25

15ndash30

Luci

eer

et

al

(2007b

)

Tasm

an

iandash

east

ern

coast

41

8Sndash

43

8360 S

Macr

ocy

stis

pyr

ifer

a

11

(1940)

131

1(3

45

bed

s1999)

lt1

(2010)

2m

md

21

2400

g

ww

tm

22

yr2

1

San

ders

on

(1990)

Ed

yva

ne

(2003)

Joh

nso

net

al

(2011)

TA

BLE

1

Con

tin

ued

Reg

ion

Lati

tud

eSp

eci

es

Ab

un

dan

ce

co

ver

Are

al

exte

nt

km

2

Dep

th

ran

ge

m

Bio

mass

gm

22

Bio

mass

turn

over

tim

es

yr2

1

Gro

wth

rate

d

21

Gro

wth

mg

g

FW

21

d2

1

Max

net

pro

du

ctio

n

rate

gC

m2

2d

21

To

tal

C

sto

red

inlivin

g

macr

oalg

ae

Mg

Ckm

22

Refe

ren

ces

St

Hele

ns

Poin

t

toSch

oute

n

Isla

nd

SE

Tasm

an

ia

41

8170 S

ndash

42

8S

Tota

lalg

ae

(pre

dom

inan

tly

Phyl

losp

ora

com

osa

an

d

Era

dia

ta)

70ndash100

0ndash25

Eckl

onia

4700

g

ww

tm

22

yr2

1

Phyl

losp

ora

7400

g

ww

tm

22

yr2

1

San

ders

on

(1990)

Luci

eer

et

al

(2007a)

Hig

hYello

w

Blu

ffto

Cap

e

Hauy

Georg

e

III

Rock

SE

Tasm

an

ia

43

8Sndash

43

8300 S

Ph

aeop

hyce

ae

(pre

dom

inan

tly

Era

dia

ta)

Rh

od

op

hyta

Ch

loro

ph

yta

43ndash48

46ndash10

7

20ndash40

20ndash30

to40ndash50

20ndash30

Luci

eer

et

al

(2012)

Valu

es

use

dto

est

imate

carb

on

stora

ge

ass

oci

ated

with

bio

mass

of

south

-east

ern

Aust

ralia

nsu

btid

alm

acr

oalg

ae

daggerV

alu

es

use

dto

est

imate

carb

on

stora

ge

ass

oci

ated

with

bio

mass

of

EA

Con

the

Gre

at

Barr

ier

Reef

DaggerExtr

ap

ola

ted

valu

es

from

pub

lish

ed

dat

ab

ase

don

fwt

d

wt

ratio

of

46

0g

Cg

21

dw

tan

d03

12

gC

g2

1d

wt

(Rave

net

al

1989)

sectExtr

ap

ola

ted

valu

es

from

pub

lish

ed

dat

aan

dass

um

ing

maxim

alp

hoto

syn

thetic

rate

for

12

hd

21

(Rave

net

al

1989)

details and justification for these choices are given in the

next section

Studies from around the world were used for all other pur-

poses of the review and informed the findings from the Aus-

tralian continent in terms of the potential for above- and

below-ground carbon storage across a range of habitats com-

parable to macroalgal communities which are known for

their efficacy in carbon sequestration (terrestrial forests salt-

marshes mangrove forests and seagrass beds) Total carbon

stored in Australia was calculated for each habitat from data

reported in the literature (Table 2) Minimum and maximum

values were calculated by multiplication of the carbon stor-

age capacity per unit area of each habitat type by the area

of that habitat found in Australia Studies from around the

world were also used to provide a rationale for the review

and contributed to the general discussion to provide a global

perspective on calcification decomposition and the influ-

ence of anthropogenic impacts on the blue carbon capacity

of macroalgae

Potential for macroalgae to directly store carbon

Macroalgae are known to have very high rates of primary

productivity and growth and significant biomass on coastal

margins (Mann 1973 Chung et al 2011) particularly in

temperate regions (Mann 1973 Cheshire et al 1996 Connell

and Irving 2008) Macroalgae are typically associated with

hard substrata to which they attach and grow obtaining

their nutritional needs from the surrounding water rather

than via vascular root systems penetrating the sediment As

such and unlike other aquatic macrophytes their biomass is

all ldquoabove groundrdquo with the exception of calcifying algae

that can build up significant calcium carbonate deposits in

the sediments (eg Halimeda in Table 1 and below) and sto-

loniferous taxa such as Caulerpa The capacity for noncalcify-

ing macroalgae to directly store carbon is thus largely

associated with the above ground living biomass and how

long the carbon within living biomass remains fixed before

being remineralized by bacteria

Australia has an extensive coastline with about 30 in

the temperate coastal zone dominated by large macroalgae

such as Durvillaea potatorum (found 0ndash5 m deep) Ecklonia

radiata and mixed fucoids (occurring down to 40 m depth)

including Phyllospora comosa Cystophora spp Sargassum spp

(Table 1) and Scytothalia doryocarpa in the west (Wernberg

et al 2003) However for most of the Australian coast data

on areal extent biomass and productivity of macroalgae are

very fragmented and often reported in non-standardised

units (Table 1) Moreover there are few records of standing

stock of carbon or carbon contents of particular species that

allow extrapolation from available biomass data Thus accu-

rate assessments of the total amount of carbon stored in

Table 2 Organic carbon stored both above and below ground in terrestrial forests and different marine ecosystems in Australia

Ecosystem

Carbon stored (Mg C km22) Area in

Australia

(km2)

Total C

stored in

Australia (Tg C) ReferencesAbove ground Below ground Total

Terrestrial forests 5700ndash21700 6200ndash23000 11900ndash44700 1494000 177786ndash667818 Malhi et al (1999)

Fourqurean

et al (2012)

Department of

Agriculture (2013)

Saltmarsh 67ndash922 207ndash12972 274ndash13894 13029 36ndash1810 Cacador et al (2004)

Howe et al (2009)

OzCoasts (2013)

Mangrove 9750ndash31724 5731ndash67816 16792ndash99540 3976 668ndash3958 Twilley et al (1992)

Howe et al (2009)

Fourqurean

et al (2012)

OzCoasts (2013)

Seagrass 01ndash555 01ndash83678 02ndash84233 296 (temperate

Australia)

21482 (all

of Australia)

592 3 1025ndash249

430 3 1023ndash18095

Fourqurean et al (2012)

Waycott et al (2009)

OzCoasts (2013)

Australian

temperate

macroalgae

2200 0 2200 49939ndash124849 1099ndash2747 This study

Hill et al Can macroalgae contribute to blue carbon

7

living biomass of macroalgae in Australia are at this stage

difficult to determine We estimate however that the coastal

waters of southern Australia with D potatorum in the upper

subtidal and E radiata monospecific andor mixed fucoid

dominated assemblages to 30 m that support an understorey

of turfing algae that may extend to 60 m in depth could

store in excess of 2200 Mg C km22 (Table 1) If we extrapolate

to the temperate coastal waters of Australialt60 m depth

(249697 km2 Whiteway 2009) and assume that approxi-

mately 50 (124849 km2) of coastal waters are rocky reef

(based on data compiled from Victoria Australia in Ierodiaco-

nou et al 2007 Rattray et al 2009 Ierodiaconou et al 2011

Che Hasan et al 2012 Monk et al 2012 Rattray et al 2013)

we estimate 2747 Tg C may be directly stored in living mac-

roalgal biomass in temperate Australia (Table 2) The above

studies targeted reef areas but there are large expanses of

sandy sediments in temperate Australia (eg Ninety-mile

beach Victoria) so if we take a more conservative estimate

of 20 (49939 km2) reef to 60 m we estimate 1099 Tg C

stored in living macroalgal biomass in temperate Australia

(Table 2) For tropical and subtropical Australia data are even

sparser but based on estimates of carbon storage by epilithic

algal communities the Great Barrier Reef may store 232 Tg C

in epilithic algae alone (675 g C m22 3 344400 km2 Table 1)

The capacity for carbon storage per unit area in macroalgae is

generally lower than for other blue carbon habitats and ter-

restrial forests due to the absence of below ground biomass

(Table 2) However the vast extent of temperate macroalgae

communities makes total carbon storage comparable to the

other blue carbon habitats (saltmarsh mangroves and sea-

grass beds) which have both above and below ground carbon

storage (Table 2) We of course acknowledge that there are

temporal and spatial variability in productivity biomass and

carbon content of different species (Table 1) and thus these

values are crude estimates only New data on aerial extent

biomass and carbon storage for algal species and assemblages

from around Australia will improve our estimates Compara-

ble data for other regions are needed for reliable global esti-

mates of carbon storage in macroalgal living biomass

Seasonality in alternation of generations fragmentation

and dislodgment (Thomsen et al 2004 McKenzie and Bell-

grove 2009 Krumhansl et al 2011) of macroalgae all con-

tribute to high turnover of macroalgal biomass High

productivity and growth rates of macroalgae replenish the

biomass There are however no comprehensive data on the

spatial and temporal variability in biomass of any macroalgal

species in Australia (references in Table 1) Assuming rela-

tively stable annual macroalgal standing stock productivity

growth and turnover do not affect the potential for macroal-

gae to directly store carbon in the above ground biomass

High productivity will not result in more carbon storage

unless it equates to greater total biomass However high

rates of productivity growth and turnover do become impor-

tant to carbon-storage potential of macroalgae if we consider

their possible role as carbon donors to other systems which

is a function of their decay rate en route to receiver sites the

burial efficiency of the receiver site and their structural com-

plexity (ie susceptibility to being remineralized) We

explore this role in more detail below (see ldquoMacroalgae as

carbon donorsrdquo)

Calcification in macroalgae

All macroalgal groups contain genera that form calcium

carbonate deposits and calcified algae are found in the

photic zone of all marine habitats from polar to tropical seas

(Nelson 2009) In the Phaeophyceae calcification is most

notable in Padina though a few other brown algae also cal-

cify The calcifying Chlorophyte algae are mostly tropical

and contain genera such as Acetabularia Neomeris Avrainvil-

lea and most importantly in terms of its contribution Hali-

meda Many red algae are calcifying both in tropical and

cold waters but calcification is best known in the Coralli-

nales with both geniculate and nongeniculate or crustose

forms Free-living nongeniculate corallines are known as rho-

doliths and form extensive beds which are harvested in

Europe and elsewhere (eg Brazil) In most cases the calcium

carbonate is found as the mineral aragonite either deposited

at the cell surface (eg Padina) or in intercellular spaces

(eg Halimeda) Calcium carbonate can also be deposited as

calcite which has a different crystal structure to aragonite

making it more stable and less prone to dissolution in sea-

water especially under the lowered carbonate concentrations

likely to be found with increasing ocean acidification in the

future Calcite is found in external crusts on Chaetomorpha

and within the cell walls of coralline genera such as Litho-

phyllum and Lithothamnion (Lobban and Harrison 1994)

Many calcifying algae also grow epiphytically on seagrass

leaves as well as on other marine organisms including

bivalves and molluscs Indeed seagrass photosynthesis can

promote calcification rates by other organisms such as Hali-

meda growing in seagrass beds (Semesi et al 2009)

Although many of the algae that calcify are slow growing

the calcium carbonate (aragonite and especially calcite) can

persist in the marine environment long after the living cells

have decayed Iconic calcium carbonate deposits such as the

White Cliffs of Dover are the remains of marine calcifying

microalgae deposited over geological time The rhodolith

beds in France and Brazil are harvested to the rate of

500 Gg yr21 (Briand 1991) and up to 120 Gg yr21 (Riul et al

2008) respectively for industrial processes including agricul-

ture water purification mineralization and the manufacture

of cosmetics (Grall and Hall-Spencer 2003) Carbonate depo-

sition (accumulation) in coastal waters (including coral reefs)

globally is in the order of 12 Pg CaCO3 yr21 (017 Pg C yr21)

with approximately the same accumulated in the pelagic

ocean though production rates in the open ocean are closer

to 11 Pg C yr21 (Iglesias-Rodriguez et al 2002) Decomposed

Halimeda tissues are important sediment elements in tropical

Hill et al Can macroalgae contribute to blue carbon

8

regions (Table 1) and contribute the major part of the cal-

careous sediment found in the sandy beaches of many tropi-

cal shores Halimeda bioherms alone have been estimated to

contribute 400 Tg CaCO3 yr21 to CaCO3 accumulation (Hillis

1997) Rhodolith forming species can produce in the region

of 60ndash1000 g CaCO3 m22 yr21 with CaCO3 deposits off Bra-

zilrsquos coast alone of 2 Pg (Riul et al 2008 Nelson 2009)

Importantly carbonates deposited by oceanic organisms

have not previously been included in blue carbon budgets

This is because the calcification process (Eq 1) results in the

release of 1 CO2 for every CaCO3 formed

2 HCO23 1Ca21 CaCO31CO21H2O (1)

However the CO2 produced in this way can be rapidly

utilised in photosynthesis and even if it is not (during calcifi-

cation in the dark for instance) there is still the net conver-

sion of one soluble HCO23 into one insoluble carbonate

(ie calcification still results in net drawdown of carbon in

the recalcitrant carbonate minerals aragonite or calcite)

Given the significant contribution of macroalgal calcifica-

tion to the global C budget and the persistence of CaCO3 in

sediments we would argue that calcification should be con-

sidered in any calculations of blue carbon into the future If

included this would constitute a further 034 Pg C yr21

sequestered globally

Macroalgae as carbon donors

So far we have established that most macroalgal species

have limited capacity to act as long-term carbon sinks in

their own right (Table 2) largely due to their inability to

accumulate below-ground stores of carbon relative to other

vegetated coastal habitats such as seagrasses saltmarshes

and mangroves However even though macroalgae do not

develop significant carbon deposits themselves there still

exists the possibility that they could make significant contri-

butions to global carbon sequestration by acting as ldquocarbon

donorsrdquo In this section we explore this possibility

What is a ldquocarbon donorrdquo Here we define a carbon donor

as an autotroph that ldquodonatesrdquo carbon to another ldquoreceiverrdquo

habitat that ultimately buries that carbon Therefore carbon

donors make indirect contributions to carbon sequestration

Such movement of carbon from one system to another is

referred to as ldquoleakagerdquo (or ldquospilloverrdquo) A well-recognised

example of leakage can be seen in seagrass ecosystems Sea-

grasses have a high particle-trapping capacity (Agawin and

Duarte 2002 Gruber and Kemp 2010) and due to their

occurrence at the interface between land and sea they cap-

ture large amounts of terrestrial carbon that runs off the

land following rainfall events (Kennedy et al 2010 Macrea-

die et al 2014) This externally derived carbon that leaks

into a receiver habitat is termed ldquoallochthonousrdquo carbon In

seagrasses allochthonous carbon can contribute as much as

half the total organic carbon that is sequestered in a meadow

(Kennedy et al 2010)

From a carbon accounting perspective leakage of carbon

is a complex issue Can habitats take credit for carbon that

they didnrsquot produce What happens if the carbon was

already credited to another system (double-counting) How

can the origin of carbon be determined These questions are

at the forefront of many terrestrial carbon-offset programs

(eg REDD) but have received comparatively little attention

in the aquatic fields The matter of carbon accounting of

leakage will however become increasingly important with

the rising prominence of blue carbon but is beyond the

scope of this review We recommend Murray et al (2007) for

more information on leakage

For a system to be a significant carbon donor there are

three requirements (1) high rates of biomass production (2)

effective transfer of biomass to receiver habitats and (3) the

donor carbon must undergo efficient burial of allochthonous

biomass within receiver habitats such that it evades micro-

bial attack (the latter is a function of several factors includ-

ing the intrinsic stability of the carbon physical

mechanisms of protection and environmental conditions

that dictate microbial activity) All three requirements are

necessary none are redundant or substitutable The first

requirement has already been discussed earlier in this article

and can be summarised as follows macroalgae have excep-

tionally high biomass production their global extent (2ndash68

million km2) and primary production (019ndash064 Pg C yr21)

exceeds that of all the vegetated coastal habitats (seagrass

beds saltmarshes mangroves) combined (Duarte et al

2013) In the following section we will discuss requirements

2 and 3 which concern the export and fate of this biomass

production

Export and fate of macroalgal biomass

to receiver habitats

Most macroalgal species spend their early life history

attached to benthic (hard) substrata (Leurouning 1990) but then

become dislodged or fragmented and can undergo a period

of transport in surface or bottom waters by wind and water

movement (potentially as rafts that travel significant distan-

ces) until eventually sinking disintegrating or becoming

cast upon land (Thiel 2003 Thiel and Gutow 2005 Macrea-

die et al 2011) Detachment of macroalgal tissue can arise

from natural senescence (Ang 1985) dislodgement by herbi-

vores (Kingsford 1992 Tegner et al 1995) and through

hydrodynamic forces such as waves and storms (Duggins

et al 2003) The supply quality persistence and transport

(trajectory and duration) of macroalgal rafts are all influ-

enced by climate (Macreadie et al 2011) particularly tem-

perature (Graiff et al 2013) Thus whilst there is temporal

variation in the extent of macroalgal rafts related to these

processes there is continuous export of macroalgal biomass

throughout the year whereas saltmarsh and seagrass detrital

Hill et al Can macroalgae contribute to blue carbon

9

export tends to be seasonal (Josselyn and Mathieson 1980)

Furthermore acknowledging spatial variation in the export

of macroalgal and vascular plant biomass macroalgae are

often more significant contributors to surf-zone and beach

wrack than seagrasses (Josselyn and Mathieson 1980 Gomez

et al 2013 Baring et al 2014 Ruiz-Delgado et al 2014)

From genetic and tracking studies we know that exported

macroalgal biomass can be transported long distances (Thiel

and Haye 2006 Fraser et al 2009 2010 2011 Nikula et al

2010) but there is limited information on what happens to

carbon bound within macroalgal biomass once rafts or frag-

ments sink and disintegratemdashie the point at which carbon

bound within macroalgal biomass is broken down into dis-

solved and particulate organic carbon Wada et al (2007)

suggested that macroalgae could release 20ndash40 of their pro-

ductivity as dissolved organic matter (DOM) Much of the

macroalgal DOM is likely to be microbially degraded but

estimates of the refractory component of this DOM will be

important for understanding how much could be donated to

other habitats UV is known to degrade DOM this means

that if this matter can be deposited in regions away from

light such as the deep ocean the breakdown will be further

diminished

There is some evidence to suggest that macroalgal carbon

is donated to other receiver habitats that have long-term

sequestration capacity including the deep sea (Wada et al

2008 Dierssen et al 2009) and other vegetated coastal habi-

tats such as mangrove forests seagrass beds and salt

marshes (Hyndes et al 2012 Macreadie et al 2012) In tropi-

cal estuaries and bays it is estimated that about half of the

macroalgal biomass produced is consumed by herbivores and

the other half is exported to other habitats whereas in the

temperate open coast most of the biomass is decomposed by

detritivores with a lesser amount being exported and only

small fractions being consumed or accumulated as detritus

(Hyndes et al 2013) The fate of macroalgal biomass in tem-

perate estuaries and fjords is largely unknown (Hyndes et al

2013) Most export of macroalgal biomass occurs via advec-

tion but there are also complex biotic pathways that trans-

port macroalgal biomass into receiver habitats such as via

ingestion and concomitant faecal deposition of carbon

within receiver habitats by fish which can contribute to car-

bon sequestration by fertilising receiver habitats and thereby

increasing their productivity and sequestration capacity

(Valiela 1995 Hyndes et al 2013) Breakdown of macroalgae

has been shown to be mostly mediated by microbial proc-

esses (Rieper-Kirchner 1990) however protozoans and meio-

fauna also contribute to the decomposition of macroalgal

tissues as well as enhance microbial degradation Microbial

breakdown rate is also dependent upon the sediment com-

position and oxic status of the water Sassi et al (1988)

found that macroalgal decomposition rates over 25 d under

aerobic vs anaerobic conditions were 35 and 24 respec-

tively Therefore if the macroalgal detritus can be advected

to a rapidly sedimenting region where it can be incorporated

into an anaerobic sediment this will slow the microbial

breakdown and maintain the carbon within the sediment

longer More research is needed to understand how long this

carbon actually remains within anaerobic sediment

All macroalgal carbon that enters the sedimentary carbon

pool will eventually be broken down (oxidised and reminer-

alized) by microbes and converted to inorganic forms and

potentially returned to the atmosphere The rate and effi-

ciency of this remineralization process can dictate whether

macroalgal carbon remains bound within sediments for

months or millennia Macroalgal carbon entering the sedi-

mentary pool has three possible fates (1) particulate and dis-

solved organic carbon that is recalcitrant to microbial

degradation is likely to remain stored within the sediment

for prolonged periods while labile carbon will be recycled by

heterotrophic bacteria and is either (2) assimilated into

microbial biomass or (3) respired as CO2 back to the water

column and possibly the atmosphere The proportion of

nonrespired carbon represents the amount of macroalgal car-

bon that is sequestered

It should be recognised that macroalgae lack the struc-

tural polysaccharide complexity of higher plants and conse-

quently their decomposition rates are faster (Sassi et al

1988) To better understand the degradation pathways of

macroalgal plant material within aquatic sediments

researchers have used several techniques Analyses of ele-

mental composition and stable isotope signatures are rou-

tinely used to ldquofingerprintrdquo carbon and determine its origin

although there is difficultly in separating microalgal and

macroalgal organic carbon signatures (Hardison et al 2011)

Furthermore isotopic signatures may also be variable in

space and time during the decomposition process (Fenton

and Ritz 1988) Similarly a problem with identifying sources

of organic carbon based on carbohydrate composition is that

many groups of organisms contain the same carbohydrates

(Vichkovitten and Holmer 2004) Fatty acid signatures have

proven to offer better resolution of the different plant contri-

butions to organic matter (Hardison et al 2013) although

the level of complexity using this technique is much higher

(Graeve et al 2002) Manipulative approaches using isotopic

tracer studies (Hee et al 2001 Hardison et al 2010 2011

Hyndes et al 2012) and radiolabelling (Chidthaisong et al

1999) have proved to be robust for studying the incorpora-

tion of macroalgal carbon into sediments

Reliable data on the fate of decomposed macroalgal

carbon within sediments (eg macroalgal carbon that is

ldquolostrdquo during litter bag mass loss experiments) is scarce

Hardison et al (2010) traced carbon from senescing macroal-

gae (Gracilaria spp) that were pre-labeled with the 13C stable

isotope and found that 2ndash9 of macroalgal carbon was

incorporated into the sediment This percentage of macroal-

gal carbon uptake by sediments is relatively high suggesting

efficient burial however the fate of this buried carbon was

Hill et al Can macroalgae contribute to blue carbon

10

only monitored for 2 weeks so it is not known whether this

carbon stock was sequestered long-term Other studies sug-

gest that macroalgal carbon is not sequestered long-term For

example Garcia-Robledo et al (2008) found that macroalgal

detritus (tubular and planar Ulva spp) that entered sedimen-

tary organic carbon pools vanished within days after its ini-

tial appearance indicating that carbon from such simple and

ephemeral macroalgae is not retained for durations that

would make them an important component of the long-

term carbon pool within a receiver habitat However given

the diversity in the cell walls and carbon chemistry of mac-

roalgae it is difficult to make conclusions on likely persist-

ence of sequestered macroalgae based on only a handful of

studies

Kristensen (1994) compared the decomposition rate of six

different plant materials (two macroalgae two seagrasses

and two tree leaves) using stepwise thermogravimetry and

found that macroalgae (Fucus vesiculosus and Ulva lactuca)

lost 40ndash44 of their carbon within 70 d whereas seagrasses

(Zostera marina and Ruppia maritima) lost 29ndash55 and tree

leaves (Fagus sylvatica and Rhizophora apiculata) lost only 0ndash

8 Similarly Josselyn and Mathieson (1980) found that

macroalgae (Ascophyllum nodosum and Fucus vesiculosus)

decomposed 3ndash10 times faster than a saltmarsh plant (Spar-

tina alterniflora) and seagrass (Zostera marina) Litter bag stud-

ies have reported a lack of change in sediment carbon

following decomposition of buried macroalgae suggesting

that the organic carbon bound within macroalgal structural

material (eg carbohydrates) is highly labile and rapidly

decomposed by microbes (Vichkovitten and Holmer 2004)

Despite this general pattern of high degradability of macroal-

gae compared with aquatic angiosperms (Trevathan-Tackett

et al in press) there is a high degree of diversity in the

structural complexity of macroalgae particularly in cell-wall

structure and carbon chemistry resulting in high variability

in decay rate estimates within the literature (Rice and Han-

son 1984 Twilley et al 1986 Kristensen 1990 Wada et al

2008 Trevathan-Tackett et al in press)

Nedzarek and Rakusa-Suszczewski (2004) examined the

decomposition of 10 Antarctic macroalgal species finding

they released 80 of the nutrients with the first 3 d of a 69

d decomposition experiment these rates occurred at polar

temperatures (48C) so it would be assumed that tropical

decomposition would be more rapid Similar results were

found with North Sea macroalgae where 50ndash80 of the tis-

sue biomass was lost within 14 d at 188C (Rieper-Kirchner

1990) which included the brown leathery kelp Laminaria

saccharina

Factors influencing the future carbon storage anddonor ability of macroalgae

This review presents a static view on the current state of

carbon cycling sequestration and donor capacity of macroal-

gae with an emphasis on Australian coastal systems In real-

ity the distribution biomass and productivity of these

macroalgae are vulnerable to change due to anthropogenic

activities and as such the dynamic nature of these macroal-

gal systems should be taken into consideration Factors such

as climate change (Duarte et al 2013) and urbanisation (Air-

oldi and Beck 2007 Airoldi et al 2008) can greatly alter the

distribution abundance and productivity of these systems

although the rate of change in global macroalgae population

size remains unknown

Climate change can greatly influence the survival photo-

synthetic capacity growth and competitive interactions of

macroalgae in coastal habitats (Wernberg et al 2011b)

Ocean warming on both the east and west coasts of Australia

have caused pole-ward movement of macroalgal species over

the past five decades (Wernberg et al 2011a) Potentially

hundreds of species are expected to be driven beyond the

edge of the Australian continent as warming continues driv-

ing not only local but global extinctions as 62 of macro-

algal species found in southern Australia are endemic to the

region (Phillips 2001) On the east coast of Australia there

has been a southern retreat of three habitat-forming macro-

algal species (Ecklonia radiata Phyllospora comosa and Durvil-

laea potatorum Millar 2007) and in eastern Tasmania the

once common Macrocystis pyrifera has almost completely dis-

appeared with ocean warming (Edyvane 2003 Johnson et al

2011)

In addition to rising temperatures climate change is

expected to influence macroalgal distribution and productiv-

ity through ocean acidification emergence of marine dis-

eases and shifts in the distribution of consumers In

terrestrial ecosystems there have been climate-driven

increases in global net primary production due to the easing

of critical climatic constraints such as increasing solar radia-

tion from reduced cloud cover (Nemani et al 2003) In the

oceans while increased CO2 dissolution is reducing pH and

disrupting carbonate chemistry this inorganic carbon is a

building block for photosynthesis The predicted changes in

CO2 in the atmosphere over the next 100 yr will translate to

a 25- to 3-fold increase in dissolved CO2 in seawater

although the subsequent drop in pH will cause shifts in the

equilibria between inorganic carbon forms HCO23 concentra-

tions will only rise by 10 and total Ci available for pho-

tosynthesis (HCO23 1 CO2) will thus rise bylt15 However

if CO2 availability is a constraint to the rate of photosynthe-

sis could the more abundant CO2 result in faster macroalgal

growth Most macroalgae have the capacity to use the

HCO23 ion that is dominant in seawater and given that the

HCO23 concentrations will not change much in future an

impact on photosynthesis is unlikely Furthermore most

macroalgae and seagrasses (Beer et al 2014) possess carbon

concentrating mechanisms (CCMs Giordano et al 2005)

which actively take up inorganic carbon (as HCO23 andor

CO2) and thereby accumulate CO2 at the active site of the

Hill et al Can macroalgae contribute to blue carbon

11

CO2-fixing enzyme Rubisco This effectively saturates

Rubisco for CO2 and limits any increased productivity of

macroalgae from elevated atmospheric CO2 and ocean acidi-

fication There are few exceptions mostly subtidal rhodo-

phytes to the rule that macroalgae possess CCMs so

increased CO2 per se is unlikely to increase CO2 drawdown

by coastal primary producers However there are suggestions

that higher CO2 may increase carbon allocation to seagrass

rhizomes under high light (ie in shallow water) and

thereby enhance burial rates (Jiang et al 2010)

Anthropogenic activities such as climate-change-

associated rising sea temperatures are expected to increase

the occurrence of macroalgal diseases through an increased

virulence of opportunistic pathogens as well as reduced

resistance to disease in thermally stressed hosts (Egan et al

2013) For example in the chemically defended macroalgae

Delisea pulchra bacterial bleaching of the thallus occurs in

response to elevated temperatures due to reduced antibacte-

rial chemical defences (Campbell et al 2011 Case et al

2011) Such diseases therefore have the capacity to reduce

macroalgal abundance either through increased consump-

tion (due to reduced herbivory defence) or through direct

host mortality (Goecke et al 2010)

With the delivery of warmer water further south the East

Australian Current not only contracts the range of many

macroalgal species but also extends the range of urchin con-

sumers Urchin barrens are now extensive throughout south-

eastern Australia and are continuing to expand at the detri-

ment of macroalgal populations (Johnson et al 2011) Such

altered ecological interactions with herbivores from this tro-

picalisation of high latitudes are therefore causing macroal-

gal populations to decline in Tasmania

While climate change will have detrimental effects on

macroalgal populations especially in temperate Australia

tropical regions may experience increased macroalgal abun-

dance following thermal pulses on coral-dominated reefs If

temperatures on coral reefs exceed summer averages by as

little as 1ndash28C mass coral bleaching events can occur which

can lead to coral mortality (Hoegh-Guldberg et al 2007)

Phase shifts toward macroalgal-dominated reefs can follow

especially if herbivory has been reduced by overfishing

(McManus et al 2000 Bruno et al 2009 Hughes et al

2010) However not all tropical macroalgal species will bene-

fit from climate change with species such as Chnoospora

implexa expected to decrease in abundance (Bender et al

2013)

When considering the donor capacity of macroalgae algal

rafts have the potential to deliver dislodged macroalgae to

receiver habitats that can bury the carbon and thus enhance

the carbon sink (see above) However changes in climate

will affect raft supply and persistence (Macreadie et al

2011) Increased storm intensities (IPCC 2007) will promote

substratum detachment andor fragmentation and hence

increase the abundance of algal fragments and rafts and

may also increase burial of macroalgal material (Macreadie

et al 2011) Elevated temperatures however may counter

this process by reducing raft longevity due to an increase in

herbivore metabolism and consumption (Macreadie et al

2011) In addition changes in ocean surface currents may

affect advection routes and potential endpoints of deposition

into more or less favorable receiver environments for

sequestration

Given the dynamic nature of macroalgal populations and

changes in abundance and productivity especially from

human activities the potential for carbon storage and export

may be highly variable In considering the role macroalgae

may play in climate change mitigation the factors detailed

above should be taken into account as they are likely to

greatly influence the contribution of macroalgae to blue car-

bon storage

Conclusions and research priorities

Although macroalgal communities in Australia and

around the world produce massive quantities of plant bio-

mass with high organic carbon content the presence of a

hard rocky substrate precludes the potential for long-term

storage of carbon within the macroalgal habitat In isolation

we therefore conclude that macroalgae do not contribute to

blue carbon

However a considerable proportion of macroalgal bio-

mass becomes dislodged from the benthos and is exported

beyond macroalgal habitat boundaries This donor carbon

may be received by habitats with long-term sequestration

capacity such as seagrass beds saltmarshes mangroves and

continental shelf regions Within Australia and globally

geographic differences in macroalgal biomass community

composition and productivity will influence the blue carbon

donor capacity of macroalgae with the greatest contribu-

tions likely to be in the temperate (and possibly polar)

regions In addition to a high rate of biomass production to

be a viable carbon donor macroalgae must be transferred to

a receiver habitat undergo burial and avoid microbial remi-

neralization The fate of detached macroalgal biomass is not

entirely clear and whilst limited data on the composition of

macroalgal biomass indicates that macroalgal carbon is

highly labile recent research has highlighted the potentially

significant role of refractory taxon-specific compounds (car-

bonates long-chain lipids alginates xylans and sulphated

polysaccharides) from macroalgae in contributing to long-

term blue carbon stores (Trevathan-Tackett et al in press)

We therefore conclude that macroalgae have the potential

to make ecologically meaningful contributions toward global

blue carbon sequestration as significant carbon donors but

further research is needed to quantify these contributions

Data on the degradability of macroalgal plant material is

limited to only a handful of taxa so there is considerable

need for additional testing on other taxa The capacity for

Hill et al Can macroalgae contribute to blue carbon

12

any incorporation of organic material from macroalgae into

long-term carbon stores is only possible if the material can

avoid decomposition by microbes potentially by entering a

storage habitat that is a rapidly accreting zone Research

therefore needs to focus on determining the burial rates of

macroalgal tissue at receiver sites which of these sites are

the greatest sink of macroalgal fragments understanding the

environmental conditions that maximise the burial process

and assessing whether burial is fast enough to limit micro-

bial remineralization of the organic macroalgal material

This will also need to include further research identifying

interspecies variation in carbon donor capacity due to rate of

lability and rate of transport to accreting zones In existing

blue carbon habitats methods for identifying macroalgal car-

bon in the storage zone also need to be developed to gauge

historical contributions of macroalgae into these zones

Once these unknowns are addressed the potential for mac-

roalgae to contribute to blue carbon as a carbon donor will

become less ambiguous Focusing future research on these

key areas will provide evidence as to whether macroalgae

should be included under the blue carbon umbrella

Macroalgal aquaculture and the harvesting of natural pop-

ulations are growing industries worldwide and are actions

that can greatly increase the carbon sequestration capacity

afforded by macroalgae (Chung et al 2011) Furthermore

the production of macroalgal biochar (a process involving

the pyrolysis of biomass) for addition to soil may represent

a viable long-term CO2 sink although research in this field

is in its infancy (Lehmann et al 2006 Bird et al 2011)

Given that macroalgal populations have the highest abun-

dance biomass and productivity of all coastal habitats they

not only store an immense amount of carbon in their living

biomass but they also have an outstanding potential to act

as significant carbon donors However macroalgae are vul-

nerable to a range of anthropogenic impacts so it is impor-

tant to protect these ecosystems for their climate-change-

mitigation potential as well as their ecosystem services

References

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particle trapping by a tropical seagrass meadow Estuaries

25 1205ndash1209 doi101007BF02692217

Airoldi L D Balata and M W Beck 2008 The Gray Zone

Relationships between habitat loss and marine diversity

and their applications in conservation J Exp Mar Biol

Ecol 366 8ndash15 doi101016jjembe200807034

Airoldi L and M W Beck 2007 Loss status and trends for

coastal marine habitats of Europe Oceanogr Mar Biol

Ann Rev 45 345ndash405

Ang P O J 1985 Regeneration studies of Sargassum

siliquosum J ag and S paniculatum J Ag (Phaeophyta

Sargassaceae) Botanical Marina 28 231ndash235 doi101515

botm1985286231

Bala G 2013 Digesting 400 ppm for global mean CO2

concentration Curr Sci 104 1471ndash1472

Baring R J P G Fairweather and R E Lester 2014

Storm versus calm Variation in fauna associated with

drifting macrophytes in sandy beach surf zones J Exp

Mar Biol Ecol 461 397ndash406 doi101016jjembe2014

09011

Beer S M Bjeuroork and J Beardall 2014 Photosynthesis in

the marine environment Wiley

Behrenfeld M J E Mara~non D A Siegel and S B Hooker

2002 Photoacclimation and nutrient-based model of

light-saturated photosynthesis for quantifying oceanic pri-

mary production Mar Ecol Prog Ser 228 103ndash117 doi

103354meps228103

Bender D G Diaz-Pulido and S Dove 2013 The impact of

CO2 emission scenarios and nutrient enrichment on a

common coral reef macroalga is modified by temporal

effects J Phycol 50 203ndash215 doi101111jpy12153

Bird M I C M Wurster P H de Paula Silva A M Bass

and D de Nys 2011 Algal biocharmdashproduction and

properties Bioresour Technol 102 1886ndash1891 doi

101111j1757-1707201101109x

Briand X 1991 Seaweed harvesting in Europe p 293ndash308

In M D Guiry and G Blunden [eds] Seaweed resources

in Europe Uses and potential Wiley

Bruno J F H Sweatman W F Precht E R Selig and V

G W Schutte 2009 Assessing evidence of phase shifts

from coral to macroalgal dominance on coral reefs

Ecology 90 1478ndash1484 doi10189008-17811

Cacador I A L Coasta and C Vale 2004 Carbon storage

in Tagus salt marsh sediments Water Air Soil Pollut Focus

4 701ndash714 doi101023BWAFO000002838884544ce

Campbell A H T Harder S Nielsen S Kjelleberg and P D

Steinberg 2011 Climate change and disease Bleaching of

a chemically defended seaweed Glob Chang Biol 17

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Case R J S R Longford A H Campbell A Low N Tujula

P D Steinberg and S Kjelleberg 2011 Temperature

induced bacterial virulence and bleaching disease in a

chemically defended marine macroalga Environ Microbiol

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Che Hasan R D Ierodiaconou and J Monk 2012

Evaluation of four supervised learning methods for Benthic

habitat mapping using backscatter from multi-beam sonar

Remote Sens 4 3427ndash3443 doi103390rs4113427

Cheshire A C and N D Hallam 1988 Biomass and

density of native stands of Durvillaea potatorum (southern

bull-kelp) in south eastern Australia Mar Ecol Prog Ser

48 277ndash283 doi103354meps048277

Cheshire A C G Westphalen A Wenden L J Scriven

and B C Rowland 1996 Photosynthesis and respiration

of phaeophycean-dominated macroalgal communities in

summer and winter Aquat Bot 55 159ndash170 doi

101016S0304-3770(96)01071-6

Hill et al Can macroalgae contribute to blue carbon

13

Tab

le1

C

on

trib

ution

sof

macr

oalg

ae

tosh

ort

-term

carb

on

seq

uest

ration

thro

ug

hout

Aust

ralia

b

ase

don

ava

ilab

led

ata

V

alu

es

rep

rese

nt

those

as

pub

lish

ed

inth

elit

era

ture

exce

pt

wh

ere

oth

erw

ise

ind

icate

db

ysu

pers

crip

tsan

dfo

otn

ote

sto

exp

lain

the

deri

vati

on

of

extr

ap

ola

ted

valu

es

Reg

ion

Lati

tud

eSp

eci

es

Ab

un

dan

ce

co

ver

Are

al

exte

nt

km

2

Dep

th

ran

ge

m

Bio

mass

gm

22

Bio

mass

turn

over

tim

es

yr2

1

Gro

wth

rate

d

21

Gro

wth

mg

g

FW

21

d2

1

Max

net

pro

du

ctio

n

rate

gC

m2

2d

21

To

tal

C

sto

red

inlivin

g

macr

oalg

ae

Mg

Ckm

22

Refe

ren

ces

Nort

hern

GBR

11

8300 S

ndash

15

8350 S

Halim

eda

spp

mead

ow

s

20ndash40

4637

max

525

mean

Dre

wan

d

Ab

e(l

1988)

Nort

hern

GBR

14

8270 S

ndash

15

8020 S

Halim

eda

moun

ds

bio

herm

s

26

shelf

in

nort

hern

sect

ion

of

GBR

2000

(up

to

19

mth

ick)

20ndashgt

50

Mars

hall

an

d

Davi

es

(1988)

Orm

ean

d

Sala

ma

(1988)

Gre

at

Palm

Fan

tom

e

an

dBro

ok

isla

nd

sG

BR

18

8090 S

ndash

18

8410 S

Sarg

ass

um

bacc

ula

ria

2ndash3

190

(AFD

W)

440

3Sch

affelk

ean

d

Klu

mp

p(1

997)

Davi

es

Reef

GBR

18

844

Ep

ilith

icalg

al

com

mun

ity

(cru

stose

cora

llin

es)

20

39

422

daggerK

lum

pp

an

d

McK

inn

on

(1989

1992)

GBR

15

8S

19

8S

25

8S

Ep

ilith

ic

alg

al

com

mun

ity

(turf

s)

60ndash80

reef

sub

stra

te

on

GBR

5ndash20

45

max

30

mean

56

25

253

daggerK

lum

pp

an

d

McK

inn

on

(1989

1992)

Sh

ark

Bay

West

ern

Aust

ralia

26

8D

rift

alg

ae

(pre

dom

inan

tly

Laure

nci

asp

p

Vid

alia

spiralis

Dig

enia

sim

ple

x

an

dEu

cheu

ma

spec

iosu

m)

152

(dw

t-

in

Am

phib

ilos

anta

rctica

bed

)

223

(dw

t-

inPosi

donia

aust

ralis

bed

)

Ken

drick

et

al

(1990)

Moolo

ola

ba

Qld

26

8400 S

Eckl

onia

radia

ta

an

dsu

btid

al

fuco

ids

Turf

s

(multis

peci

es)

0 57

Con

nell

an

d

Irvi

ng

(2008)

Houtm

an

Ab

roh

los

Isla

nd

s

West

ern

Aust

ralia

28

8Sndash29

8SEc

klonia

radia

ta

Red

folio

se

alg

ae

Cru

stose

cora

llin

es

15

15

3

20ndash40

1ndash50

ND

1040

(dw

t)03

Hatc

her

et

al

(1987)

Sm

ale

et

al

(2010)

Balli

na

NSW

28

8520 S

Eckl

onia

radia

ta

an

dsu

btid

al

fuco

ids

Turf

s

(multis

peci

es)

84

15

Con

nell

an

d

Irvi

ng

(2008)

TA

BLE

1

Con

tin

ued

Reg

ion

Lati

tud

eSp

eci

es

Ab

un

dan

ce

co

ver

Are

al

exte

nt

km

2

Dep

th

ran

ge

m

Bio

mass

gm

22

Bio

mass

turn

over

tim

es

yr2

1

Gro

wth

rate

d

21

Gro

wth

mg

g

FW

21

d2

1

Max

net

pro

du

ctio

n

rate

gC

m2

2d

21

To

tal

C

sto

red

inlivin

g

macr

oalg

ae

Mg

Ckm

22

Refe

ren

ces

Rott

nest

Isla

nd

32

8420 S

Eckl

onia

radia

ta

Scy

toth

alia

dory

carp

aRed

folio

sealg

ae

Cru

stose

cora

llin

es

30

4 6 12

1ndash50

1ndash50

1ndash70

ND

Sm

ale

et

al

(2010)

South

ern

Aust

ralia

Coast

33

8050 S

ndash

35

8360 S

Eckl

onia

radia

ta

an

dsu

btid

al

fuco

ids

90

(WA

an

dSA

)

41

(NSW

)

20m

180

00

(ww

tndash

WA

Era

dia

ta)

6(S

A

fuco

ids)

09

(WA

Era

dia

ta)

9(W

A

Era

dia

ta)

6(S

A

fuco

ids)

635 (S

A)

Kirkm

an

(1984

1989)

Ch

esh

ire

et

al

(1996)

Con

nell

an

d

Irvi

ng

(2008)

South

ern

Aust

ralia

Coast

33

8050 S

ndash

35

8510 S

Turf

s

(multis

peci

es)

65

ndash8

(WA

an

dSA

)to

40

wh

ere

can

op

y

rest

rict

ed

(SA

)17

(NSW

)

4an

d10

mfo

r

pro

duct

ivity

measu

res

88ndash100

(AFD

W)

29ndash79

29

(SA

)32ndash36

Cop

ert

ino

et

al

(2005)

Con

nell

an

d

Irvi

ng

(2008)

South

ern

Aust

ralia

Coast

33

8050 S

ndash

35

8360 S

Cru

stose

cora

llin

e

barr

en

s

0(W

Aan

dSA

)

38

(NSW

)

Con

nell

an

d

Irvi

ng

(2008)

South

east

ern

Aust

ralia

35

8Sndash

43

8SD

urv

illaea

pota

toru

m

0ndash5

225

004

891m

ean

1080

002

34

78

max

(ww

td

wt

resp

ect

ively

)

603

sect1526Dagger

Ch

esh

ire

an

d

Halla

m(1

988)

Rave

net

al

(1989)

Vic

toria

(9

of

Vic

coast

line)

38

8110 S

ndash

38

8520 S

Dom

inan

t

macr

oalg

al

ass

em

bla

ges

(pre

dom

inate

ly

ph

aeop

hyte

s

an

drh

od

op

hyte

s)

341

377

10ndash60

Iero

dia

con

ou

et

al

(2007

2011)

Ratt

ray

et

al

(2009)

Ch

eH

asa

n

et

al

(2012)

Mon

ket

al

(2012)

Ratt

ray

et

al

(2013)

Rob

ins

Pass

ag

e

toSw

an

Isla

nd

nort

hco

ast

Tasm

an

ia

40

8420 S

ndash

41

8120 S

Durv

illaea

pota

toru

m

Mix

ed

Era

dia

ta

an

dfu

coid

s

Mix

ed

turf

s

10ndash50

60ndash100

40ndash60

0ndash5

0ndash25

15ndash30

Luci

eer

et

al

(2007b

)

Tasm

an

iandash

east

ern

coast

41

8Sndash

43

8360 S

Macr

ocy

stis

pyr

ifer

a

11

(1940)

131

1(3

45

bed

s1999)

lt1

(2010)

2m

md

21

2400

g

ww

tm

22

yr2

1

San

ders

on

(1990)

Ed

yva

ne

(2003)

Joh

nso

net

al

(2011)

TA

BLE

1

Con

tin

ued

Reg

ion

Lati

tud

eSp

eci

es

Ab

un

dan

ce

co

ver

Are

al

exte

nt

km

2

Dep

th

ran

ge

m

Bio

mass

gm

22

Bio

mass

turn

over

tim

es

yr2

1

Gro

wth

rate

d

21

Gro

wth

mg

g

FW

21

d2

1

Max

net

pro

du

ctio

n

rate

gC

m2

2d

21

To

tal

C

sto

red

inlivin

g

macr

oalg

ae

Mg

Ckm

22

Refe

ren

ces

St

Hele

ns

Poin

t

toSch

oute

n

Isla

nd

SE

Tasm

an

ia

41

8170 S

ndash

42

8S

Tota

lalg

ae

(pre

dom

inan

tly

Phyl

losp

ora

com

osa

an

d

Era

dia

ta)

70ndash100

0ndash25

Eckl

onia

4700

g

ww

tm

22

yr2

1

Phyl

losp

ora

7400

g

ww

tm

22

yr2

1

San

ders

on

(1990)

Luci

eer

et

al

(2007a)

Hig

hYello

w

Blu

ffto

Cap

e

Hauy

Georg

e

III

Rock

SE

Tasm

an

ia

43

8Sndash

43

8300 S

Ph

aeop

hyce

ae

(pre

dom

inan

tly

Era

dia

ta)

Rh

od

op

hyta

Ch

loro

ph

yta

43ndash48

46ndash10

7

20ndash40

20ndash30

to40ndash50

20ndash30

Luci

eer

et

al

(2012)

Valu

es

use

dto

est

imate

carb

on

stora

ge

ass

oci

ated

with

bio

mass

of

south

-east

ern

Aust

ralia

nsu

btid

alm

acr

oalg

ae

daggerV

alu

es

use

dto

est

imate

carb

on

stora

ge

ass

oci

ated

with

bio

mass

of

EA

Con

the

Gre

at

Barr

ier

Reef

DaggerExtr

ap

ola

ted

valu

es

from

pub

lish

ed

dat

ab

ase

don

fwt

d

wt

ratio

of

46

0g

Cg

21

dw

tan

d03

12

gC

g2

1d

wt

(Rave

net

al

1989)

sectExtr

ap

ola

ted

valu

es

from

pub

lish

ed

dat

aan

dass

um

ing

maxim

alp

hoto

syn

thetic

rate

for

12

hd

21

(Rave

net

al

1989)

details and justification for these choices are given in the

next section

Studies from around the world were used for all other pur-

poses of the review and informed the findings from the Aus-

tralian continent in terms of the potential for above- and

below-ground carbon storage across a range of habitats com-

parable to macroalgal communities which are known for

their efficacy in carbon sequestration (terrestrial forests salt-

marshes mangrove forests and seagrass beds) Total carbon

stored in Australia was calculated for each habitat from data

reported in the literature (Table 2) Minimum and maximum

values were calculated by multiplication of the carbon stor-

age capacity per unit area of each habitat type by the area

of that habitat found in Australia Studies from around the

world were also used to provide a rationale for the review

and contributed to the general discussion to provide a global

perspective on calcification decomposition and the influ-

ence of anthropogenic impacts on the blue carbon capacity

of macroalgae

Potential for macroalgae to directly store carbon

Macroalgae are known to have very high rates of primary

productivity and growth and significant biomass on coastal

margins (Mann 1973 Chung et al 2011) particularly in

temperate regions (Mann 1973 Cheshire et al 1996 Connell

and Irving 2008) Macroalgae are typically associated with

hard substrata to which they attach and grow obtaining

their nutritional needs from the surrounding water rather

than via vascular root systems penetrating the sediment As

such and unlike other aquatic macrophytes their biomass is

all ldquoabove groundrdquo with the exception of calcifying algae

that can build up significant calcium carbonate deposits in

the sediments (eg Halimeda in Table 1 and below) and sto-

loniferous taxa such as Caulerpa The capacity for noncalcify-

ing macroalgae to directly store carbon is thus largely

associated with the above ground living biomass and how

long the carbon within living biomass remains fixed before

being remineralized by bacteria

Australia has an extensive coastline with about 30 in

the temperate coastal zone dominated by large macroalgae

such as Durvillaea potatorum (found 0ndash5 m deep) Ecklonia

radiata and mixed fucoids (occurring down to 40 m depth)

including Phyllospora comosa Cystophora spp Sargassum spp

(Table 1) and Scytothalia doryocarpa in the west (Wernberg

et al 2003) However for most of the Australian coast data

on areal extent biomass and productivity of macroalgae are

very fragmented and often reported in non-standardised

units (Table 1) Moreover there are few records of standing

stock of carbon or carbon contents of particular species that

allow extrapolation from available biomass data Thus accu-

rate assessments of the total amount of carbon stored in

Table 2 Organic carbon stored both above and below ground in terrestrial forests and different marine ecosystems in Australia

Ecosystem

Carbon stored (Mg C km22) Area in

Australia

(km2)

Total C

stored in

Australia (Tg C) ReferencesAbove ground Below ground Total

Terrestrial forests 5700ndash21700 6200ndash23000 11900ndash44700 1494000 177786ndash667818 Malhi et al (1999)

Fourqurean

et al (2012)

Department of

Agriculture (2013)

Saltmarsh 67ndash922 207ndash12972 274ndash13894 13029 36ndash1810 Cacador et al (2004)

Howe et al (2009)

OzCoasts (2013)

Mangrove 9750ndash31724 5731ndash67816 16792ndash99540 3976 668ndash3958 Twilley et al (1992)

Howe et al (2009)

Fourqurean

et al (2012)

OzCoasts (2013)

Seagrass 01ndash555 01ndash83678 02ndash84233 296 (temperate

Australia)

21482 (all

of Australia)

592 3 1025ndash249

430 3 1023ndash18095

Fourqurean et al (2012)

Waycott et al (2009)

OzCoasts (2013)

Australian

temperate

macroalgae

2200 0 2200 49939ndash124849 1099ndash2747 This study

Hill et al Can macroalgae contribute to blue carbon

7

living biomass of macroalgae in Australia are at this stage

difficult to determine We estimate however that the coastal

waters of southern Australia with D potatorum in the upper

subtidal and E radiata monospecific andor mixed fucoid

dominated assemblages to 30 m that support an understorey

of turfing algae that may extend to 60 m in depth could

store in excess of 2200 Mg C km22 (Table 1) If we extrapolate

to the temperate coastal waters of Australialt60 m depth

(249697 km2 Whiteway 2009) and assume that approxi-

mately 50 (124849 km2) of coastal waters are rocky reef

(based on data compiled from Victoria Australia in Ierodiaco-

nou et al 2007 Rattray et al 2009 Ierodiaconou et al 2011

Che Hasan et al 2012 Monk et al 2012 Rattray et al 2013)

we estimate 2747 Tg C may be directly stored in living mac-

roalgal biomass in temperate Australia (Table 2) The above

studies targeted reef areas but there are large expanses of

sandy sediments in temperate Australia (eg Ninety-mile

beach Victoria) so if we take a more conservative estimate

of 20 (49939 km2) reef to 60 m we estimate 1099 Tg C

stored in living macroalgal biomass in temperate Australia

(Table 2) For tropical and subtropical Australia data are even

sparser but based on estimates of carbon storage by epilithic

algal communities the Great Barrier Reef may store 232 Tg C

in epilithic algae alone (675 g C m22 3 344400 km2 Table 1)

The capacity for carbon storage per unit area in macroalgae is

generally lower than for other blue carbon habitats and ter-

restrial forests due to the absence of below ground biomass

(Table 2) However the vast extent of temperate macroalgae

communities makes total carbon storage comparable to the

other blue carbon habitats (saltmarsh mangroves and sea-

grass beds) which have both above and below ground carbon

storage (Table 2) We of course acknowledge that there are

temporal and spatial variability in productivity biomass and

carbon content of different species (Table 1) and thus these

values are crude estimates only New data on aerial extent

biomass and carbon storage for algal species and assemblages

from around Australia will improve our estimates Compara-

ble data for other regions are needed for reliable global esti-

mates of carbon storage in macroalgal living biomass

Seasonality in alternation of generations fragmentation

and dislodgment (Thomsen et al 2004 McKenzie and Bell-

grove 2009 Krumhansl et al 2011) of macroalgae all con-

tribute to high turnover of macroalgal biomass High

productivity and growth rates of macroalgae replenish the

biomass There are however no comprehensive data on the

spatial and temporal variability in biomass of any macroalgal

species in Australia (references in Table 1) Assuming rela-

tively stable annual macroalgal standing stock productivity

growth and turnover do not affect the potential for macroal-

gae to directly store carbon in the above ground biomass

High productivity will not result in more carbon storage

unless it equates to greater total biomass However high

rates of productivity growth and turnover do become impor-

tant to carbon-storage potential of macroalgae if we consider

their possible role as carbon donors to other systems which

is a function of their decay rate en route to receiver sites the

burial efficiency of the receiver site and their structural com-

plexity (ie susceptibility to being remineralized) We

explore this role in more detail below (see ldquoMacroalgae as

carbon donorsrdquo)

Calcification in macroalgae

All macroalgal groups contain genera that form calcium

carbonate deposits and calcified algae are found in the

photic zone of all marine habitats from polar to tropical seas

(Nelson 2009) In the Phaeophyceae calcification is most

notable in Padina though a few other brown algae also cal-

cify The calcifying Chlorophyte algae are mostly tropical

and contain genera such as Acetabularia Neomeris Avrainvil-

lea and most importantly in terms of its contribution Hali-

meda Many red algae are calcifying both in tropical and

cold waters but calcification is best known in the Coralli-

nales with both geniculate and nongeniculate or crustose

forms Free-living nongeniculate corallines are known as rho-

doliths and form extensive beds which are harvested in

Europe and elsewhere (eg Brazil) In most cases the calcium

carbonate is found as the mineral aragonite either deposited

at the cell surface (eg Padina) or in intercellular spaces

(eg Halimeda) Calcium carbonate can also be deposited as

calcite which has a different crystal structure to aragonite

making it more stable and less prone to dissolution in sea-

water especially under the lowered carbonate concentrations

likely to be found with increasing ocean acidification in the

future Calcite is found in external crusts on Chaetomorpha

and within the cell walls of coralline genera such as Litho-

phyllum and Lithothamnion (Lobban and Harrison 1994)

Many calcifying algae also grow epiphytically on seagrass

leaves as well as on other marine organisms including

bivalves and molluscs Indeed seagrass photosynthesis can

promote calcification rates by other organisms such as Hali-

meda growing in seagrass beds (Semesi et al 2009)

Although many of the algae that calcify are slow growing

the calcium carbonate (aragonite and especially calcite) can

persist in the marine environment long after the living cells

have decayed Iconic calcium carbonate deposits such as the

White Cliffs of Dover are the remains of marine calcifying

microalgae deposited over geological time The rhodolith

beds in France and Brazil are harvested to the rate of

500 Gg yr21 (Briand 1991) and up to 120 Gg yr21 (Riul et al

2008) respectively for industrial processes including agricul-

ture water purification mineralization and the manufacture

of cosmetics (Grall and Hall-Spencer 2003) Carbonate depo-

sition (accumulation) in coastal waters (including coral reefs)

globally is in the order of 12 Pg CaCO3 yr21 (017 Pg C yr21)

with approximately the same accumulated in the pelagic

ocean though production rates in the open ocean are closer

to 11 Pg C yr21 (Iglesias-Rodriguez et al 2002) Decomposed

Halimeda tissues are important sediment elements in tropical

Hill et al Can macroalgae contribute to blue carbon

8

regions (Table 1) and contribute the major part of the cal-

careous sediment found in the sandy beaches of many tropi-

cal shores Halimeda bioherms alone have been estimated to

contribute 400 Tg CaCO3 yr21 to CaCO3 accumulation (Hillis

1997) Rhodolith forming species can produce in the region

of 60ndash1000 g CaCO3 m22 yr21 with CaCO3 deposits off Bra-

zilrsquos coast alone of 2 Pg (Riul et al 2008 Nelson 2009)

Importantly carbonates deposited by oceanic organisms

have not previously been included in blue carbon budgets

This is because the calcification process (Eq 1) results in the

release of 1 CO2 for every CaCO3 formed

2 HCO23 1Ca21 CaCO31CO21H2O (1)

However the CO2 produced in this way can be rapidly

utilised in photosynthesis and even if it is not (during calcifi-

cation in the dark for instance) there is still the net conver-

sion of one soluble HCO23 into one insoluble carbonate

(ie calcification still results in net drawdown of carbon in

the recalcitrant carbonate minerals aragonite or calcite)

Given the significant contribution of macroalgal calcifica-

tion to the global C budget and the persistence of CaCO3 in

sediments we would argue that calcification should be con-

sidered in any calculations of blue carbon into the future If

included this would constitute a further 034 Pg C yr21

sequestered globally

Macroalgae as carbon donors

So far we have established that most macroalgal species

have limited capacity to act as long-term carbon sinks in

their own right (Table 2) largely due to their inability to

accumulate below-ground stores of carbon relative to other

vegetated coastal habitats such as seagrasses saltmarshes

and mangroves However even though macroalgae do not

develop significant carbon deposits themselves there still

exists the possibility that they could make significant contri-

butions to global carbon sequestration by acting as ldquocarbon

donorsrdquo In this section we explore this possibility

What is a ldquocarbon donorrdquo Here we define a carbon donor

as an autotroph that ldquodonatesrdquo carbon to another ldquoreceiverrdquo

habitat that ultimately buries that carbon Therefore carbon

donors make indirect contributions to carbon sequestration

Such movement of carbon from one system to another is

referred to as ldquoleakagerdquo (or ldquospilloverrdquo) A well-recognised

example of leakage can be seen in seagrass ecosystems Sea-

grasses have a high particle-trapping capacity (Agawin and

Duarte 2002 Gruber and Kemp 2010) and due to their

occurrence at the interface between land and sea they cap-

ture large amounts of terrestrial carbon that runs off the

land following rainfall events (Kennedy et al 2010 Macrea-

die et al 2014) This externally derived carbon that leaks

into a receiver habitat is termed ldquoallochthonousrdquo carbon In

seagrasses allochthonous carbon can contribute as much as

half the total organic carbon that is sequestered in a meadow

(Kennedy et al 2010)

From a carbon accounting perspective leakage of carbon

is a complex issue Can habitats take credit for carbon that

they didnrsquot produce What happens if the carbon was

already credited to another system (double-counting) How

can the origin of carbon be determined These questions are

at the forefront of many terrestrial carbon-offset programs

(eg REDD) but have received comparatively little attention

in the aquatic fields The matter of carbon accounting of

leakage will however become increasingly important with

the rising prominence of blue carbon but is beyond the

scope of this review We recommend Murray et al (2007) for

more information on leakage

For a system to be a significant carbon donor there are

three requirements (1) high rates of biomass production (2)

effective transfer of biomass to receiver habitats and (3) the

donor carbon must undergo efficient burial of allochthonous

biomass within receiver habitats such that it evades micro-

bial attack (the latter is a function of several factors includ-

ing the intrinsic stability of the carbon physical

mechanisms of protection and environmental conditions

that dictate microbial activity) All three requirements are

necessary none are redundant or substitutable The first

requirement has already been discussed earlier in this article

and can be summarised as follows macroalgae have excep-

tionally high biomass production their global extent (2ndash68

million km2) and primary production (019ndash064 Pg C yr21)

exceeds that of all the vegetated coastal habitats (seagrass

beds saltmarshes mangroves) combined (Duarte et al

2013) In the following section we will discuss requirements

2 and 3 which concern the export and fate of this biomass

production

Export and fate of macroalgal biomass

to receiver habitats

Most macroalgal species spend their early life history

attached to benthic (hard) substrata (Leurouning 1990) but then

become dislodged or fragmented and can undergo a period

of transport in surface or bottom waters by wind and water

movement (potentially as rafts that travel significant distan-

ces) until eventually sinking disintegrating or becoming

cast upon land (Thiel 2003 Thiel and Gutow 2005 Macrea-

die et al 2011) Detachment of macroalgal tissue can arise

from natural senescence (Ang 1985) dislodgement by herbi-

vores (Kingsford 1992 Tegner et al 1995) and through

hydrodynamic forces such as waves and storms (Duggins

et al 2003) The supply quality persistence and transport

(trajectory and duration) of macroalgal rafts are all influ-

enced by climate (Macreadie et al 2011) particularly tem-

perature (Graiff et al 2013) Thus whilst there is temporal

variation in the extent of macroalgal rafts related to these

processes there is continuous export of macroalgal biomass

throughout the year whereas saltmarsh and seagrass detrital

Hill et al Can macroalgae contribute to blue carbon

9

export tends to be seasonal (Josselyn and Mathieson 1980)

Furthermore acknowledging spatial variation in the export

of macroalgal and vascular plant biomass macroalgae are

often more significant contributors to surf-zone and beach

wrack than seagrasses (Josselyn and Mathieson 1980 Gomez

et al 2013 Baring et al 2014 Ruiz-Delgado et al 2014)

From genetic and tracking studies we know that exported

macroalgal biomass can be transported long distances (Thiel

and Haye 2006 Fraser et al 2009 2010 2011 Nikula et al

2010) but there is limited information on what happens to

carbon bound within macroalgal biomass once rafts or frag-

ments sink and disintegratemdashie the point at which carbon

bound within macroalgal biomass is broken down into dis-

solved and particulate organic carbon Wada et al (2007)

suggested that macroalgae could release 20ndash40 of their pro-

ductivity as dissolved organic matter (DOM) Much of the

macroalgal DOM is likely to be microbially degraded but

estimates of the refractory component of this DOM will be

important for understanding how much could be donated to

other habitats UV is known to degrade DOM this means

that if this matter can be deposited in regions away from

light such as the deep ocean the breakdown will be further

diminished

There is some evidence to suggest that macroalgal carbon

is donated to other receiver habitats that have long-term

sequestration capacity including the deep sea (Wada et al

2008 Dierssen et al 2009) and other vegetated coastal habi-

tats such as mangrove forests seagrass beds and salt

marshes (Hyndes et al 2012 Macreadie et al 2012) In tropi-

cal estuaries and bays it is estimated that about half of the

macroalgal biomass produced is consumed by herbivores and

the other half is exported to other habitats whereas in the

temperate open coast most of the biomass is decomposed by

detritivores with a lesser amount being exported and only

small fractions being consumed or accumulated as detritus

(Hyndes et al 2013) The fate of macroalgal biomass in tem-

perate estuaries and fjords is largely unknown (Hyndes et al

2013) Most export of macroalgal biomass occurs via advec-

tion but there are also complex biotic pathways that trans-

port macroalgal biomass into receiver habitats such as via

ingestion and concomitant faecal deposition of carbon

within receiver habitats by fish which can contribute to car-

bon sequestration by fertilising receiver habitats and thereby

increasing their productivity and sequestration capacity

(Valiela 1995 Hyndes et al 2013) Breakdown of macroalgae

has been shown to be mostly mediated by microbial proc-

esses (Rieper-Kirchner 1990) however protozoans and meio-

fauna also contribute to the decomposition of macroalgal

tissues as well as enhance microbial degradation Microbial

breakdown rate is also dependent upon the sediment com-

position and oxic status of the water Sassi et al (1988)

found that macroalgal decomposition rates over 25 d under

aerobic vs anaerobic conditions were 35 and 24 respec-

tively Therefore if the macroalgal detritus can be advected

to a rapidly sedimenting region where it can be incorporated

into an anaerobic sediment this will slow the microbial

breakdown and maintain the carbon within the sediment

longer More research is needed to understand how long this

carbon actually remains within anaerobic sediment

All macroalgal carbon that enters the sedimentary carbon

pool will eventually be broken down (oxidised and reminer-

alized) by microbes and converted to inorganic forms and

potentially returned to the atmosphere The rate and effi-

ciency of this remineralization process can dictate whether

macroalgal carbon remains bound within sediments for

months or millennia Macroalgal carbon entering the sedi-

mentary pool has three possible fates (1) particulate and dis-

solved organic carbon that is recalcitrant to microbial

degradation is likely to remain stored within the sediment

for prolonged periods while labile carbon will be recycled by

heterotrophic bacteria and is either (2) assimilated into

microbial biomass or (3) respired as CO2 back to the water

column and possibly the atmosphere The proportion of

nonrespired carbon represents the amount of macroalgal car-

bon that is sequestered

It should be recognised that macroalgae lack the struc-

tural polysaccharide complexity of higher plants and conse-

quently their decomposition rates are faster (Sassi et al

1988) To better understand the degradation pathways of

macroalgal plant material within aquatic sediments

researchers have used several techniques Analyses of ele-

mental composition and stable isotope signatures are rou-

tinely used to ldquofingerprintrdquo carbon and determine its origin

although there is difficultly in separating microalgal and

macroalgal organic carbon signatures (Hardison et al 2011)

Furthermore isotopic signatures may also be variable in

space and time during the decomposition process (Fenton

and Ritz 1988) Similarly a problem with identifying sources

of organic carbon based on carbohydrate composition is that

many groups of organisms contain the same carbohydrates

(Vichkovitten and Holmer 2004) Fatty acid signatures have

proven to offer better resolution of the different plant contri-

butions to organic matter (Hardison et al 2013) although

the level of complexity using this technique is much higher

(Graeve et al 2002) Manipulative approaches using isotopic

tracer studies (Hee et al 2001 Hardison et al 2010 2011

Hyndes et al 2012) and radiolabelling (Chidthaisong et al

1999) have proved to be robust for studying the incorpora-

tion of macroalgal carbon into sediments

Reliable data on the fate of decomposed macroalgal

carbon within sediments (eg macroalgal carbon that is

ldquolostrdquo during litter bag mass loss experiments) is scarce

Hardison et al (2010) traced carbon from senescing macroal-

gae (Gracilaria spp) that were pre-labeled with the 13C stable

isotope and found that 2ndash9 of macroalgal carbon was

incorporated into the sediment This percentage of macroal-

gal carbon uptake by sediments is relatively high suggesting

efficient burial however the fate of this buried carbon was

Hill et al Can macroalgae contribute to blue carbon

10

only monitored for 2 weeks so it is not known whether this

carbon stock was sequestered long-term Other studies sug-

gest that macroalgal carbon is not sequestered long-term For

example Garcia-Robledo et al (2008) found that macroalgal

detritus (tubular and planar Ulva spp) that entered sedimen-

tary organic carbon pools vanished within days after its ini-

tial appearance indicating that carbon from such simple and

ephemeral macroalgae is not retained for durations that

would make them an important component of the long-

term carbon pool within a receiver habitat However given

the diversity in the cell walls and carbon chemistry of mac-

roalgae it is difficult to make conclusions on likely persist-

ence of sequestered macroalgae based on only a handful of

studies

Kristensen (1994) compared the decomposition rate of six

different plant materials (two macroalgae two seagrasses

and two tree leaves) using stepwise thermogravimetry and

found that macroalgae (Fucus vesiculosus and Ulva lactuca)

lost 40ndash44 of their carbon within 70 d whereas seagrasses

(Zostera marina and Ruppia maritima) lost 29ndash55 and tree

leaves (Fagus sylvatica and Rhizophora apiculata) lost only 0ndash

8 Similarly Josselyn and Mathieson (1980) found that

macroalgae (Ascophyllum nodosum and Fucus vesiculosus)

decomposed 3ndash10 times faster than a saltmarsh plant (Spar-

tina alterniflora) and seagrass (Zostera marina) Litter bag stud-

ies have reported a lack of change in sediment carbon

following decomposition of buried macroalgae suggesting

that the organic carbon bound within macroalgal structural

material (eg carbohydrates) is highly labile and rapidly

decomposed by microbes (Vichkovitten and Holmer 2004)

Despite this general pattern of high degradability of macroal-

gae compared with aquatic angiosperms (Trevathan-Tackett

et al in press) there is a high degree of diversity in the

structural complexity of macroalgae particularly in cell-wall

structure and carbon chemistry resulting in high variability

in decay rate estimates within the literature (Rice and Han-

son 1984 Twilley et al 1986 Kristensen 1990 Wada et al

2008 Trevathan-Tackett et al in press)

Nedzarek and Rakusa-Suszczewski (2004) examined the

decomposition of 10 Antarctic macroalgal species finding

they released 80 of the nutrients with the first 3 d of a 69

d decomposition experiment these rates occurred at polar

temperatures (48C) so it would be assumed that tropical

decomposition would be more rapid Similar results were

found with North Sea macroalgae where 50ndash80 of the tis-

sue biomass was lost within 14 d at 188C (Rieper-Kirchner

1990) which included the brown leathery kelp Laminaria

saccharina

Factors influencing the future carbon storage anddonor ability of macroalgae

This review presents a static view on the current state of

carbon cycling sequestration and donor capacity of macroal-

gae with an emphasis on Australian coastal systems In real-

ity the distribution biomass and productivity of these

macroalgae are vulnerable to change due to anthropogenic

activities and as such the dynamic nature of these macroal-

gal systems should be taken into consideration Factors such

as climate change (Duarte et al 2013) and urbanisation (Air-

oldi and Beck 2007 Airoldi et al 2008) can greatly alter the

distribution abundance and productivity of these systems

although the rate of change in global macroalgae population

size remains unknown

Climate change can greatly influence the survival photo-

synthetic capacity growth and competitive interactions of

macroalgae in coastal habitats (Wernberg et al 2011b)

Ocean warming on both the east and west coasts of Australia

have caused pole-ward movement of macroalgal species over

the past five decades (Wernberg et al 2011a) Potentially

hundreds of species are expected to be driven beyond the

edge of the Australian continent as warming continues driv-

ing not only local but global extinctions as 62 of macro-

algal species found in southern Australia are endemic to the

region (Phillips 2001) On the east coast of Australia there

has been a southern retreat of three habitat-forming macro-

algal species (Ecklonia radiata Phyllospora comosa and Durvil-

laea potatorum Millar 2007) and in eastern Tasmania the

once common Macrocystis pyrifera has almost completely dis-

appeared with ocean warming (Edyvane 2003 Johnson et al

2011)

In addition to rising temperatures climate change is

expected to influence macroalgal distribution and productiv-

ity through ocean acidification emergence of marine dis-

eases and shifts in the distribution of consumers In

terrestrial ecosystems there have been climate-driven

increases in global net primary production due to the easing

of critical climatic constraints such as increasing solar radia-

tion from reduced cloud cover (Nemani et al 2003) In the

oceans while increased CO2 dissolution is reducing pH and

disrupting carbonate chemistry this inorganic carbon is a

building block for photosynthesis The predicted changes in

CO2 in the atmosphere over the next 100 yr will translate to

a 25- to 3-fold increase in dissolved CO2 in seawater

although the subsequent drop in pH will cause shifts in the

equilibria between inorganic carbon forms HCO23 concentra-

tions will only rise by 10 and total Ci available for pho-

tosynthesis (HCO23 1 CO2) will thus rise bylt15 However

if CO2 availability is a constraint to the rate of photosynthe-

sis could the more abundant CO2 result in faster macroalgal

growth Most macroalgae have the capacity to use the

HCO23 ion that is dominant in seawater and given that the

HCO23 concentrations will not change much in future an

impact on photosynthesis is unlikely Furthermore most

macroalgae and seagrasses (Beer et al 2014) possess carbon

concentrating mechanisms (CCMs Giordano et al 2005)

which actively take up inorganic carbon (as HCO23 andor

CO2) and thereby accumulate CO2 at the active site of the

Hill et al Can macroalgae contribute to blue carbon

11

CO2-fixing enzyme Rubisco This effectively saturates

Rubisco for CO2 and limits any increased productivity of

macroalgae from elevated atmospheric CO2 and ocean acidi-

fication There are few exceptions mostly subtidal rhodo-

phytes to the rule that macroalgae possess CCMs so

increased CO2 per se is unlikely to increase CO2 drawdown

by coastal primary producers However there are suggestions

that higher CO2 may increase carbon allocation to seagrass

rhizomes under high light (ie in shallow water) and

thereby enhance burial rates (Jiang et al 2010)

Anthropogenic activities such as climate-change-

associated rising sea temperatures are expected to increase

the occurrence of macroalgal diseases through an increased

virulence of opportunistic pathogens as well as reduced

resistance to disease in thermally stressed hosts (Egan et al

2013) For example in the chemically defended macroalgae

Delisea pulchra bacterial bleaching of the thallus occurs in

response to elevated temperatures due to reduced antibacte-

rial chemical defences (Campbell et al 2011 Case et al

2011) Such diseases therefore have the capacity to reduce

macroalgal abundance either through increased consump-

tion (due to reduced herbivory defence) or through direct

host mortality (Goecke et al 2010)

With the delivery of warmer water further south the East

Australian Current not only contracts the range of many

macroalgal species but also extends the range of urchin con-

sumers Urchin barrens are now extensive throughout south-

eastern Australia and are continuing to expand at the detri-

ment of macroalgal populations (Johnson et al 2011) Such

altered ecological interactions with herbivores from this tro-

picalisation of high latitudes are therefore causing macroal-

gal populations to decline in Tasmania

While climate change will have detrimental effects on

macroalgal populations especially in temperate Australia

tropical regions may experience increased macroalgal abun-

dance following thermal pulses on coral-dominated reefs If

temperatures on coral reefs exceed summer averages by as

little as 1ndash28C mass coral bleaching events can occur which

can lead to coral mortality (Hoegh-Guldberg et al 2007)

Phase shifts toward macroalgal-dominated reefs can follow

especially if herbivory has been reduced by overfishing

(McManus et al 2000 Bruno et al 2009 Hughes et al

2010) However not all tropical macroalgal species will bene-

fit from climate change with species such as Chnoospora

implexa expected to decrease in abundance (Bender et al

2013)

When considering the donor capacity of macroalgae algal

rafts have the potential to deliver dislodged macroalgae to

receiver habitats that can bury the carbon and thus enhance

the carbon sink (see above) However changes in climate

will affect raft supply and persistence (Macreadie et al

2011) Increased storm intensities (IPCC 2007) will promote

substratum detachment andor fragmentation and hence

increase the abundance of algal fragments and rafts and

may also increase burial of macroalgal material (Macreadie

et al 2011) Elevated temperatures however may counter

this process by reducing raft longevity due to an increase in

herbivore metabolism and consumption (Macreadie et al

2011) In addition changes in ocean surface currents may

affect advection routes and potential endpoints of deposition

into more or less favorable receiver environments for

sequestration

Given the dynamic nature of macroalgal populations and

changes in abundance and productivity especially from

human activities the potential for carbon storage and export

may be highly variable In considering the role macroalgae

may play in climate change mitigation the factors detailed

above should be taken into account as they are likely to

greatly influence the contribution of macroalgae to blue car-

bon storage

Conclusions and research priorities

Although macroalgal communities in Australia and

around the world produce massive quantities of plant bio-

mass with high organic carbon content the presence of a

hard rocky substrate precludes the potential for long-term

storage of carbon within the macroalgal habitat In isolation

we therefore conclude that macroalgae do not contribute to

blue carbon

However a considerable proportion of macroalgal bio-

mass becomes dislodged from the benthos and is exported

beyond macroalgal habitat boundaries This donor carbon

may be received by habitats with long-term sequestration

capacity such as seagrass beds saltmarshes mangroves and

continental shelf regions Within Australia and globally

geographic differences in macroalgal biomass community

composition and productivity will influence the blue carbon

donor capacity of macroalgae with the greatest contribu-

tions likely to be in the temperate (and possibly polar)

regions In addition to a high rate of biomass production to

be a viable carbon donor macroalgae must be transferred to

a receiver habitat undergo burial and avoid microbial remi-

neralization The fate of detached macroalgal biomass is not

entirely clear and whilst limited data on the composition of

macroalgal biomass indicates that macroalgal carbon is

highly labile recent research has highlighted the potentially

significant role of refractory taxon-specific compounds (car-

bonates long-chain lipids alginates xylans and sulphated

polysaccharides) from macroalgae in contributing to long-

term blue carbon stores (Trevathan-Tackett et al in press)

We therefore conclude that macroalgae have the potential

to make ecologically meaningful contributions toward global

blue carbon sequestration as significant carbon donors but

further research is needed to quantify these contributions

Data on the degradability of macroalgal plant material is

limited to only a handful of taxa so there is considerable

need for additional testing on other taxa The capacity for

Hill et al Can macroalgae contribute to blue carbon

12

any incorporation of organic material from macroalgae into

long-term carbon stores is only possible if the material can

avoid decomposition by microbes potentially by entering a

storage habitat that is a rapidly accreting zone Research

therefore needs to focus on determining the burial rates of

macroalgal tissue at receiver sites which of these sites are

the greatest sink of macroalgal fragments understanding the

environmental conditions that maximise the burial process

and assessing whether burial is fast enough to limit micro-

bial remineralization of the organic macroalgal material

This will also need to include further research identifying

interspecies variation in carbon donor capacity due to rate of

lability and rate of transport to accreting zones In existing

blue carbon habitats methods for identifying macroalgal car-

bon in the storage zone also need to be developed to gauge

historical contributions of macroalgae into these zones

Once these unknowns are addressed the potential for mac-

roalgae to contribute to blue carbon as a carbon donor will

become less ambiguous Focusing future research on these

key areas will provide evidence as to whether macroalgae

should be included under the blue carbon umbrella

Macroalgal aquaculture and the harvesting of natural pop-

ulations are growing industries worldwide and are actions

that can greatly increase the carbon sequestration capacity

afforded by macroalgae (Chung et al 2011) Furthermore

the production of macroalgal biochar (a process involving

the pyrolysis of biomass) for addition to soil may represent

a viable long-term CO2 sink although research in this field

is in its infancy (Lehmann et al 2006 Bird et al 2011)

Given that macroalgal populations have the highest abun-

dance biomass and productivity of all coastal habitats they

not only store an immense amount of carbon in their living

biomass but they also have an outstanding potential to act

as significant carbon donors However macroalgae are vul-

nerable to a range of anthropogenic impacts so it is impor-

tant to protect these ecosystems for their climate-change-

mitigation potential as well as their ecosystem services

References

Agawin N S R and G M Duarte 2002 Evidence of direct

particle trapping by a tropical seagrass meadow Estuaries

25 1205ndash1209 doi101007BF02692217

Airoldi L D Balata and M W Beck 2008 The Gray Zone

Relationships between habitat loss and marine diversity

and their applications in conservation J Exp Mar Biol

Ecol 366 8ndash15 doi101016jjembe200807034

Airoldi L and M W Beck 2007 Loss status and trends for

coastal marine habitats of Europe Oceanogr Mar Biol

Ann Rev 45 345ndash405

Ang P O J 1985 Regeneration studies of Sargassum

siliquosum J ag and S paniculatum J Ag (Phaeophyta

Sargassaceae) Botanical Marina 28 231ndash235 doi101515

botm1985286231

Bala G 2013 Digesting 400 ppm for global mean CO2

concentration Curr Sci 104 1471ndash1472

Baring R J P G Fairweather and R E Lester 2014

Storm versus calm Variation in fauna associated with

drifting macrophytes in sandy beach surf zones J Exp

Mar Biol Ecol 461 397ndash406 doi101016jjembe2014

09011

Beer S M Bjeuroork and J Beardall 2014 Photosynthesis in

the marine environment Wiley

Behrenfeld M J E Mara~non D A Siegel and S B Hooker

2002 Photoacclimation and nutrient-based model of

light-saturated photosynthesis for quantifying oceanic pri-

mary production Mar Ecol Prog Ser 228 103ndash117 doi

103354meps228103

Bender D G Diaz-Pulido and S Dove 2013 The impact of

CO2 emission scenarios and nutrient enrichment on a

common coral reef macroalga is modified by temporal

effects J Phycol 50 203ndash215 doi101111jpy12153

Bird M I C M Wurster P H de Paula Silva A M Bass

and D de Nys 2011 Algal biocharmdashproduction and

properties Bioresour Technol 102 1886ndash1891 doi

101111j1757-1707201101109x

Briand X 1991 Seaweed harvesting in Europe p 293ndash308

In M D Guiry and G Blunden [eds] Seaweed resources

in Europe Uses and potential Wiley

Bruno J F H Sweatman W F Precht E R Selig and V

G W Schutte 2009 Assessing evidence of phase shifts

from coral to macroalgal dominance on coral reefs

Ecology 90 1478ndash1484 doi10189008-17811

Cacador I A L Coasta and C Vale 2004 Carbon storage

in Tagus salt marsh sediments Water Air Soil Pollut Focus

4 701ndash714 doi101023BWAFO000002838884544ce

Campbell A H T Harder S Nielsen S Kjelleberg and P D

Steinberg 2011 Climate change and disease Bleaching of

a chemically defended seaweed Glob Chang Biol 17

2958ndash2970 doi101111j1365-2486201102456x

Case R J S R Longford A H Campbell A Low N Tujula

P D Steinberg and S Kjelleberg 2011 Temperature

induced bacterial virulence and bleaching disease in a

chemically defended marine macroalga Environ Microbiol

13 529ndash537 doi101111j1462-2920201002356x

Che Hasan R D Ierodiaconou and J Monk 2012

Evaluation of four supervised learning methods for Benthic

habitat mapping using backscatter from multi-beam sonar

Remote Sens 4 3427ndash3443 doi103390rs4113427

Cheshire A C and N D Hallam 1988 Biomass and

density of native stands of Durvillaea potatorum (southern

bull-kelp) in south eastern Australia Mar Ecol Prog Ser

48 277ndash283 doi103354meps048277

Cheshire A C G Westphalen A Wenden L J Scriven

and B C Rowland 1996 Photosynthesis and respiration

of phaeophycean-dominated macroalgal communities in

summer and winter Aquat Bot 55 159ndash170 doi

101016S0304-3770(96)01071-6

Hill et al Can macroalgae contribute to blue carbon

13

TA

BLE

1

Con

tin

ued

Reg

ion

Lati

tud

eSp

eci

es

Ab

un

dan

ce

co

ver

Are

al

exte

nt

km

2

Dep

th

ran

ge

m

Bio

mass

gm

22

Bio

mass

turn

over

tim

es

yr2

1

Gro

wth

rate

d

21

Gro

wth

mg

g

FW

21

d2

1

Max

net

pro

du

ctio

n

rate

gC

m2

2d

21

To

tal

C

sto

red

inlivin

g

macr

oalg

ae

Mg

Ckm

22

Refe

ren

ces

Rott

nest

Isla

nd

32

8420 S

Eckl

onia

radia

ta

Scy

toth

alia

dory

carp

aRed

folio

sealg

ae

Cru

stose

cora

llin

es

30

4 6 12

1ndash50

1ndash50

1ndash70

ND

Sm

ale

et

al

(2010)

South

ern

Aust

ralia

Coast

33

8050 S

ndash

35

8360 S

Eckl

onia

radia

ta

an

dsu

btid

al

fuco

ids

90

(WA

an

dSA

)

41

(NSW

)

20m

180

00

(ww

tndash

WA

Era

dia

ta)

6(S

A

fuco

ids)

09

(WA

Era

dia

ta)

9(W

A

Era

dia

ta)

6(S

A

fuco

ids)

635 (S

A)

Kirkm

an

(1984

1989)

Ch

esh

ire

et

al

(1996)

Con

nell

an

d

Irvi

ng

(2008)

South

ern

Aust

ralia

Coast

33

8050 S

ndash

35

8510 S

Turf

s

(multis

peci

es)

65

ndash8

(WA

an

dSA

)to

40

wh

ere

can

op

y

rest

rict

ed

(SA

)17

(NSW

)

4an

d10

mfo

r

pro

duct

ivity

measu

res

88ndash100

(AFD

W)

29ndash79

29

(SA

)32ndash36

Cop

ert

ino

et

al

(2005)

Con

nell

an

d

Irvi

ng

(2008)

South

ern

Aust

ralia

Coast

33

8050 S

ndash

35

8360 S

Cru

stose

cora

llin

e

barr

en

s

0(W

Aan

dSA

)

38

(NSW

)

Con

nell

an

d

Irvi

ng

(2008)

South

east

ern

Aust

ralia

35

8Sndash

43

8SD

urv

illaea

pota

toru

m

0ndash5

225

004

891m

ean

1080

002

34

78

max

(ww

td

wt

resp

ect

ively

)

603

sect1526Dagger

Ch

esh

ire

an

d

Halla

m(1

988)

Rave

net

al

(1989)

Vic

toria

(9

of

Vic

coast

line)

38

8110 S

ndash

38

8520 S

Dom

inan

t

macr

oalg

al

ass

em

bla

ges

(pre

dom

inate

ly

ph

aeop

hyte

s

an

drh

od

op

hyte

s)

341

377

10ndash60

Iero

dia

con

ou

et

al

(2007

2011)

Ratt

ray

et

al

(2009)

Ch

eH

asa

n

et

al

(2012)

Mon

ket

al

(2012)

Ratt

ray

et

al

(2013)

Rob

ins

Pass

ag

e

toSw

an

Isla

nd

nort

hco

ast

Tasm

an

ia

40

8420 S

ndash

41

8120 S

Durv

illaea

pota

toru

m

Mix

ed

Era

dia

ta

an

dfu

coid

s

Mix

ed

turf

s

10ndash50

60ndash100

40ndash60

0ndash5

0ndash25

15ndash30

Luci

eer

et

al

(2007b

)

Tasm

an

iandash

east

ern

coast

41

8Sndash

43

8360 S

Macr

ocy

stis

pyr

ifer

a

11

(1940)

131

1(3

45

bed

s1999)

lt1

(2010)

2m

md

21

2400

g

ww

tm

22

yr2

1

San

ders

on

(1990)

Ed

yva

ne

(2003)

Joh

nso

net

al

(2011)

TA

BLE

1

Con

tin

ued

Reg

ion

Lati

tud

eSp

eci

es

Ab

un

dan

ce

co

ver

Are

al

exte

nt

km

2

Dep

th

ran

ge

m

Bio

mass

gm

22

Bio

mass

turn

over

tim

es

yr2

1

Gro

wth

rate

d

21

Gro

wth

mg

g

FW

21

d2

1

Max

net

pro

du

ctio

n

rate

gC

m2

2d

21

To

tal

C

sto

red

inlivin

g

macr

oalg

ae

Mg

Ckm

22

Refe

ren

ces

St

Hele

ns

Poin

t

toSch

oute

n

Isla

nd

SE

Tasm

an

ia

41

8170 S

ndash

42

8S

Tota

lalg

ae

(pre

dom

inan

tly

Phyl

losp

ora

com

osa

an

d

Era

dia

ta)

70ndash100

0ndash25

Eckl

onia

4700

g

ww

tm

22

yr2

1

Phyl

losp

ora

7400

g

ww

tm

22

yr2

1

San

ders

on

(1990)

Luci

eer

et

al

(2007a)

Hig

hYello

w

Blu

ffto

Cap

e

Hauy

Georg

e

III

Rock

SE

Tasm

an

ia

43

8Sndash

43

8300 S

Ph

aeop

hyce

ae

(pre

dom

inan

tly

Era

dia

ta)

Rh

od

op

hyta

Ch

loro

ph

yta

43ndash48

46ndash10

7

20ndash40

20ndash30

to40ndash50

20ndash30

Luci

eer

et

al

(2012)

Valu

es

use

dto

est

imate

carb

on

stora

ge

ass

oci

ated

with

bio

mass

of

south

-east

ern

Aust

ralia

nsu

btid

alm

acr

oalg

ae

daggerV

alu

es

use

dto

est

imate

carb

on

stora

ge

ass

oci

ated

with

bio

mass

of

EA

Con

the

Gre

at

Barr

ier

Reef

DaggerExtr

ap

ola

ted

valu

es

from

pub

lish

ed

dat

ab

ase

don

fwt

d

wt

ratio

of

46

0g

Cg

21

dw

tan

d03

12

gC

g2

1d

wt

(Rave

net

al

1989)

sectExtr

ap

ola

ted

valu

es

from

pub

lish

ed

dat

aan

dass

um

ing

maxim

alp

hoto

syn

thetic

rate

for

12

hd

21

(Rave

net

al

1989)

details and justification for these choices are given in the

next section

Studies from around the world were used for all other pur-

poses of the review and informed the findings from the Aus-

tralian continent in terms of the potential for above- and

below-ground carbon storage across a range of habitats com-

parable to macroalgal communities which are known for

their efficacy in carbon sequestration (terrestrial forests salt-

marshes mangrove forests and seagrass beds) Total carbon

stored in Australia was calculated for each habitat from data

reported in the literature (Table 2) Minimum and maximum

values were calculated by multiplication of the carbon stor-

age capacity per unit area of each habitat type by the area

of that habitat found in Australia Studies from around the

world were also used to provide a rationale for the review

and contributed to the general discussion to provide a global

perspective on calcification decomposition and the influ-

ence of anthropogenic impacts on the blue carbon capacity

of macroalgae

Potential for macroalgae to directly store carbon

Macroalgae are known to have very high rates of primary

productivity and growth and significant biomass on coastal

margins (Mann 1973 Chung et al 2011) particularly in

temperate regions (Mann 1973 Cheshire et al 1996 Connell

and Irving 2008) Macroalgae are typically associated with

hard substrata to which they attach and grow obtaining

their nutritional needs from the surrounding water rather

than via vascular root systems penetrating the sediment As

such and unlike other aquatic macrophytes their biomass is

all ldquoabove groundrdquo with the exception of calcifying algae

that can build up significant calcium carbonate deposits in

the sediments (eg Halimeda in Table 1 and below) and sto-

loniferous taxa such as Caulerpa The capacity for noncalcify-

ing macroalgae to directly store carbon is thus largely

associated with the above ground living biomass and how

long the carbon within living biomass remains fixed before

being remineralized by bacteria

Australia has an extensive coastline with about 30 in

the temperate coastal zone dominated by large macroalgae

such as Durvillaea potatorum (found 0ndash5 m deep) Ecklonia

radiata and mixed fucoids (occurring down to 40 m depth)

including Phyllospora comosa Cystophora spp Sargassum spp

(Table 1) and Scytothalia doryocarpa in the west (Wernberg

et al 2003) However for most of the Australian coast data

on areal extent biomass and productivity of macroalgae are

very fragmented and often reported in non-standardised

units (Table 1) Moreover there are few records of standing

stock of carbon or carbon contents of particular species that

allow extrapolation from available biomass data Thus accu-

rate assessments of the total amount of carbon stored in

Table 2 Organic carbon stored both above and below ground in terrestrial forests and different marine ecosystems in Australia

Ecosystem

Carbon stored (Mg C km22) Area in

Australia

(km2)

Total C

stored in

Australia (Tg C) ReferencesAbove ground Below ground Total

Terrestrial forests 5700ndash21700 6200ndash23000 11900ndash44700 1494000 177786ndash667818 Malhi et al (1999)

Fourqurean

et al (2012)

Department of

Agriculture (2013)

Saltmarsh 67ndash922 207ndash12972 274ndash13894 13029 36ndash1810 Cacador et al (2004)

Howe et al (2009)

OzCoasts (2013)

Mangrove 9750ndash31724 5731ndash67816 16792ndash99540 3976 668ndash3958 Twilley et al (1992)

Howe et al (2009)

Fourqurean

et al (2012)

OzCoasts (2013)

Seagrass 01ndash555 01ndash83678 02ndash84233 296 (temperate

Australia)

21482 (all

of Australia)

592 3 1025ndash249

430 3 1023ndash18095

Fourqurean et al (2012)

Waycott et al (2009)

OzCoasts (2013)

Australian

temperate

macroalgae

2200 0 2200 49939ndash124849 1099ndash2747 This study

Hill et al Can macroalgae contribute to blue carbon

7

living biomass of macroalgae in Australia are at this stage

difficult to determine We estimate however that the coastal

waters of southern Australia with D potatorum in the upper

subtidal and E radiata monospecific andor mixed fucoid

dominated assemblages to 30 m that support an understorey

of turfing algae that may extend to 60 m in depth could

store in excess of 2200 Mg C km22 (Table 1) If we extrapolate

to the temperate coastal waters of Australialt60 m depth

(249697 km2 Whiteway 2009) and assume that approxi-

mately 50 (124849 km2) of coastal waters are rocky reef

(based on data compiled from Victoria Australia in Ierodiaco-

nou et al 2007 Rattray et al 2009 Ierodiaconou et al 2011

Che Hasan et al 2012 Monk et al 2012 Rattray et al 2013)

we estimate 2747 Tg C may be directly stored in living mac-

roalgal biomass in temperate Australia (Table 2) The above

studies targeted reef areas but there are large expanses of

sandy sediments in temperate Australia (eg Ninety-mile

beach Victoria) so if we take a more conservative estimate

of 20 (49939 km2) reef to 60 m we estimate 1099 Tg C

stored in living macroalgal biomass in temperate Australia

(Table 2) For tropical and subtropical Australia data are even

sparser but based on estimates of carbon storage by epilithic

algal communities the Great Barrier Reef may store 232 Tg C

in epilithic algae alone (675 g C m22 3 344400 km2 Table 1)

The capacity for carbon storage per unit area in macroalgae is

generally lower than for other blue carbon habitats and ter-

restrial forests due to the absence of below ground biomass

(Table 2) However the vast extent of temperate macroalgae

communities makes total carbon storage comparable to the

other blue carbon habitats (saltmarsh mangroves and sea-

grass beds) which have both above and below ground carbon

storage (Table 2) We of course acknowledge that there are

temporal and spatial variability in productivity biomass and

carbon content of different species (Table 1) and thus these

values are crude estimates only New data on aerial extent

biomass and carbon storage for algal species and assemblages

from around Australia will improve our estimates Compara-

ble data for other regions are needed for reliable global esti-

mates of carbon storage in macroalgal living biomass

Seasonality in alternation of generations fragmentation

and dislodgment (Thomsen et al 2004 McKenzie and Bell-

grove 2009 Krumhansl et al 2011) of macroalgae all con-

tribute to high turnover of macroalgal biomass High

productivity and growth rates of macroalgae replenish the

biomass There are however no comprehensive data on the

spatial and temporal variability in biomass of any macroalgal

species in Australia (references in Table 1) Assuming rela-

tively stable annual macroalgal standing stock productivity

growth and turnover do not affect the potential for macroal-

gae to directly store carbon in the above ground biomass

High productivity will not result in more carbon storage

unless it equates to greater total biomass However high

rates of productivity growth and turnover do become impor-

tant to carbon-storage potential of macroalgae if we consider

their possible role as carbon donors to other systems which

is a function of their decay rate en route to receiver sites the

burial efficiency of the receiver site and their structural com-

plexity (ie susceptibility to being remineralized) We

explore this role in more detail below (see ldquoMacroalgae as

carbon donorsrdquo)

Calcification in macroalgae

All macroalgal groups contain genera that form calcium

carbonate deposits and calcified algae are found in the

photic zone of all marine habitats from polar to tropical seas

(Nelson 2009) In the Phaeophyceae calcification is most

notable in Padina though a few other brown algae also cal-

cify The calcifying Chlorophyte algae are mostly tropical

and contain genera such as Acetabularia Neomeris Avrainvil-

lea and most importantly in terms of its contribution Hali-

meda Many red algae are calcifying both in tropical and

cold waters but calcification is best known in the Coralli-

nales with both geniculate and nongeniculate or crustose

forms Free-living nongeniculate corallines are known as rho-

doliths and form extensive beds which are harvested in

Europe and elsewhere (eg Brazil) In most cases the calcium

carbonate is found as the mineral aragonite either deposited

at the cell surface (eg Padina) or in intercellular spaces

(eg Halimeda) Calcium carbonate can also be deposited as

calcite which has a different crystal structure to aragonite

making it more stable and less prone to dissolution in sea-

water especially under the lowered carbonate concentrations

likely to be found with increasing ocean acidification in the

future Calcite is found in external crusts on Chaetomorpha

and within the cell walls of coralline genera such as Litho-

phyllum and Lithothamnion (Lobban and Harrison 1994)

Many calcifying algae also grow epiphytically on seagrass

leaves as well as on other marine organisms including

bivalves and molluscs Indeed seagrass photosynthesis can

promote calcification rates by other organisms such as Hali-

meda growing in seagrass beds (Semesi et al 2009)

Although many of the algae that calcify are slow growing

the calcium carbonate (aragonite and especially calcite) can

persist in the marine environment long after the living cells

have decayed Iconic calcium carbonate deposits such as the

White Cliffs of Dover are the remains of marine calcifying

microalgae deposited over geological time The rhodolith

beds in France and Brazil are harvested to the rate of

500 Gg yr21 (Briand 1991) and up to 120 Gg yr21 (Riul et al

2008) respectively for industrial processes including agricul-

ture water purification mineralization and the manufacture

of cosmetics (Grall and Hall-Spencer 2003) Carbonate depo-

sition (accumulation) in coastal waters (including coral reefs)

globally is in the order of 12 Pg CaCO3 yr21 (017 Pg C yr21)

with approximately the same accumulated in the pelagic

ocean though production rates in the open ocean are closer

to 11 Pg C yr21 (Iglesias-Rodriguez et al 2002) Decomposed

Halimeda tissues are important sediment elements in tropical

Hill et al Can macroalgae contribute to blue carbon

8

regions (Table 1) and contribute the major part of the cal-

careous sediment found in the sandy beaches of many tropi-

cal shores Halimeda bioherms alone have been estimated to

contribute 400 Tg CaCO3 yr21 to CaCO3 accumulation (Hillis

1997) Rhodolith forming species can produce in the region

of 60ndash1000 g CaCO3 m22 yr21 with CaCO3 deposits off Bra-

zilrsquos coast alone of 2 Pg (Riul et al 2008 Nelson 2009)

Importantly carbonates deposited by oceanic organisms

have not previously been included in blue carbon budgets

This is because the calcification process (Eq 1) results in the

release of 1 CO2 for every CaCO3 formed

2 HCO23 1Ca21 CaCO31CO21H2O (1)

However the CO2 produced in this way can be rapidly

utilised in photosynthesis and even if it is not (during calcifi-

cation in the dark for instance) there is still the net conver-

sion of one soluble HCO23 into one insoluble carbonate

(ie calcification still results in net drawdown of carbon in

the recalcitrant carbonate minerals aragonite or calcite)

Given the significant contribution of macroalgal calcifica-

tion to the global C budget and the persistence of CaCO3 in

sediments we would argue that calcification should be con-

sidered in any calculations of blue carbon into the future If

included this would constitute a further 034 Pg C yr21

sequestered globally

Macroalgae as carbon donors

So far we have established that most macroalgal species

have limited capacity to act as long-term carbon sinks in

their own right (Table 2) largely due to their inability to

accumulate below-ground stores of carbon relative to other

vegetated coastal habitats such as seagrasses saltmarshes

and mangroves However even though macroalgae do not

develop significant carbon deposits themselves there still

exists the possibility that they could make significant contri-

butions to global carbon sequestration by acting as ldquocarbon

donorsrdquo In this section we explore this possibility

What is a ldquocarbon donorrdquo Here we define a carbon donor

as an autotroph that ldquodonatesrdquo carbon to another ldquoreceiverrdquo

habitat that ultimately buries that carbon Therefore carbon

donors make indirect contributions to carbon sequestration

Such movement of carbon from one system to another is

referred to as ldquoleakagerdquo (or ldquospilloverrdquo) A well-recognised

example of leakage can be seen in seagrass ecosystems Sea-

grasses have a high particle-trapping capacity (Agawin and

Duarte 2002 Gruber and Kemp 2010) and due to their

occurrence at the interface between land and sea they cap-

ture large amounts of terrestrial carbon that runs off the

land following rainfall events (Kennedy et al 2010 Macrea-

die et al 2014) This externally derived carbon that leaks

into a receiver habitat is termed ldquoallochthonousrdquo carbon In

seagrasses allochthonous carbon can contribute as much as

half the total organic carbon that is sequestered in a meadow

(Kennedy et al 2010)

From a carbon accounting perspective leakage of carbon

is a complex issue Can habitats take credit for carbon that

they didnrsquot produce What happens if the carbon was

already credited to another system (double-counting) How

can the origin of carbon be determined These questions are

at the forefront of many terrestrial carbon-offset programs

(eg REDD) but have received comparatively little attention

in the aquatic fields The matter of carbon accounting of

leakage will however become increasingly important with

the rising prominence of blue carbon but is beyond the

scope of this review We recommend Murray et al (2007) for

more information on leakage

For a system to be a significant carbon donor there are

three requirements (1) high rates of biomass production (2)

effective transfer of biomass to receiver habitats and (3) the

donor carbon must undergo efficient burial of allochthonous

biomass within receiver habitats such that it evades micro-

bial attack (the latter is a function of several factors includ-

ing the intrinsic stability of the carbon physical

mechanisms of protection and environmental conditions

that dictate microbial activity) All three requirements are

necessary none are redundant or substitutable The first

requirement has already been discussed earlier in this article

and can be summarised as follows macroalgae have excep-

tionally high biomass production their global extent (2ndash68

million km2) and primary production (019ndash064 Pg C yr21)

exceeds that of all the vegetated coastal habitats (seagrass

beds saltmarshes mangroves) combined (Duarte et al

2013) In the following section we will discuss requirements

2 and 3 which concern the export and fate of this biomass

production

Export and fate of macroalgal biomass

to receiver habitats

Most macroalgal species spend their early life history

attached to benthic (hard) substrata (Leurouning 1990) but then

become dislodged or fragmented and can undergo a period

of transport in surface or bottom waters by wind and water

movement (potentially as rafts that travel significant distan-

ces) until eventually sinking disintegrating or becoming

cast upon land (Thiel 2003 Thiel and Gutow 2005 Macrea-

die et al 2011) Detachment of macroalgal tissue can arise

from natural senescence (Ang 1985) dislodgement by herbi-

vores (Kingsford 1992 Tegner et al 1995) and through

hydrodynamic forces such as waves and storms (Duggins

et al 2003) The supply quality persistence and transport

(trajectory and duration) of macroalgal rafts are all influ-

enced by climate (Macreadie et al 2011) particularly tem-

perature (Graiff et al 2013) Thus whilst there is temporal

variation in the extent of macroalgal rafts related to these

processes there is continuous export of macroalgal biomass

throughout the year whereas saltmarsh and seagrass detrital

Hill et al Can macroalgae contribute to blue carbon

9

export tends to be seasonal (Josselyn and Mathieson 1980)

Furthermore acknowledging spatial variation in the export

of macroalgal and vascular plant biomass macroalgae are

often more significant contributors to surf-zone and beach

wrack than seagrasses (Josselyn and Mathieson 1980 Gomez

et al 2013 Baring et al 2014 Ruiz-Delgado et al 2014)

From genetic and tracking studies we know that exported

macroalgal biomass can be transported long distances (Thiel

and Haye 2006 Fraser et al 2009 2010 2011 Nikula et al

2010) but there is limited information on what happens to

carbon bound within macroalgal biomass once rafts or frag-

ments sink and disintegratemdashie the point at which carbon

bound within macroalgal biomass is broken down into dis-

solved and particulate organic carbon Wada et al (2007)

suggested that macroalgae could release 20ndash40 of their pro-

ductivity as dissolved organic matter (DOM) Much of the

macroalgal DOM is likely to be microbially degraded but

estimates of the refractory component of this DOM will be

important for understanding how much could be donated to

other habitats UV is known to degrade DOM this means

that if this matter can be deposited in regions away from

light such as the deep ocean the breakdown will be further

diminished

There is some evidence to suggest that macroalgal carbon

is donated to other receiver habitats that have long-term

sequestration capacity including the deep sea (Wada et al

2008 Dierssen et al 2009) and other vegetated coastal habi-

tats such as mangrove forests seagrass beds and salt

marshes (Hyndes et al 2012 Macreadie et al 2012) In tropi-

cal estuaries and bays it is estimated that about half of the

macroalgal biomass produced is consumed by herbivores and

the other half is exported to other habitats whereas in the

temperate open coast most of the biomass is decomposed by

detritivores with a lesser amount being exported and only

small fractions being consumed or accumulated as detritus

(Hyndes et al 2013) The fate of macroalgal biomass in tem-

perate estuaries and fjords is largely unknown (Hyndes et al

2013) Most export of macroalgal biomass occurs via advec-

tion but there are also complex biotic pathways that trans-

port macroalgal biomass into receiver habitats such as via

ingestion and concomitant faecal deposition of carbon

within receiver habitats by fish which can contribute to car-

bon sequestration by fertilising receiver habitats and thereby

increasing their productivity and sequestration capacity

(Valiela 1995 Hyndes et al 2013) Breakdown of macroalgae

has been shown to be mostly mediated by microbial proc-

esses (Rieper-Kirchner 1990) however protozoans and meio-

fauna also contribute to the decomposition of macroalgal

tissues as well as enhance microbial degradation Microbial

breakdown rate is also dependent upon the sediment com-

position and oxic status of the water Sassi et al (1988)

found that macroalgal decomposition rates over 25 d under

aerobic vs anaerobic conditions were 35 and 24 respec-

tively Therefore if the macroalgal detritus can be advected

to a rapidly sedimenting region where it can be incorporated

into an anaerobic sediment this will slow the microbial

breakdown and maintain the carbon within the sediment

longer More research is needed to understand how long this

carbon actually remains within anaerobic sediment

All macroalgal carbon that enters the sedimentary carbon

pool will eventually be broken down (oxidised and reminer-

alized) by microbes and converted to inorganic forms and

potentially returned to the atmosphere The rate and effi-

ciency of this remineralization process can dictate whether

macroalgal carbon remains bound within sediments for

months or millennia Macroalgal carbon entering the sedi-

mentary pool has three possible fates (1) particulate and dis-

solved organic carbon that is recalcitrant to microbial

degradation is likely to remain stored within the sediment

for prolonged periods while labile carbon will be recycled by

heterotrophic bacteria and is either (2) assimilated into

microbial biomass or (3) respired as CO2 back to the water

column and possibly the atmosphere The proportion of

nonrespired carbon represents the amount of macroalgal car-

bon that is sequestered

It should be recognised that macroalgae lack the struc-

tural polysaccharide complexity of higher plants and conse-

quently their decomposition rates are faster (Sassi et al

1988) To better understand the degradation pathways of

macroalgal plant material within aquatic sediments

researchers have used several techniques Analyses of ele-

mental composition and stable isotope signatures are rou-

tinely used to ldquofingerprintrdquo carbon and determine its origin

although there is difficultly in separating microalgal and

macroalgal organic carbon signatures (Hardison et al 2011)

Furthermore isotopic signatures may also be variable in

space and time during the decomposition process (Fenton

and Ritz 1988) Similarly a problem with identifying sources

of organic carbon based on carbohydrate composition is that

many groups of organisms contain the same carbohydrates

(Vichkovitten and Holmer 2004) Fatty acid signatures have

proven to offer better resolution of the different plant contri-

butions to organic matter (Hardison et al 2013) although

the level of complexity using this technique is much higher

(Graeve et al 2002) Manipulative approaches using isotopic

tracer studies (Hee et al 2001 Hardison et al 2010 2011

Hyndes et al 2012) and radiolabelling (Chidthaisong et al

1999) have proved to be robust for studying the incorpora-

tion of macroalgal carbon into sediments

Reliable data on the fate of decomposed macroalgal

carbon within sediments (eg macroalgal carbon that is

ldquolostrdquo during litter bag mass loss experiments) is scarce

Hardison et al (2010) traced carbon from senescing macroal-

gae (Gracilaria spp) that were pre-labeled with the 13C stable

isotope and found that 2ndash9 of macroalgal carbon was

incorporated into the sediment This percentage of macroal-

gal carbon uptake by sediments is relatively high suggesting

efficient burial however the fate of this buried carbon was

Hill et al Can macroalgae contribute to blue carbon

10

only monitored for 2 weeks so it is not known whether this

carbon stock was sequestered long-term Other studies sug-

gest that macroalgal carbon is not sequestered long-term For

example Garcia-Robledo et al (2008) found that macroalgal

detritus (tubular and planar Ulva spp) that entered sedimen-

tary organic carbon pools vanished within days after its ini-

tial appearance indicating that carbon from such simple and

ephemeral macroalgae is not retained for durations that

would make them an important component of the long-

term carbon pool within a receiver habitat However given

the diversity in the cell walls and carbon chemistry of mac-

roalgae it is difficult to make conclusions on likely persist-

ence of sequestered macroalgae based on only a handful of

studies

Kristensen (1994) compared the decomposition rate of six

different plant materials (two macroalgae two seagrasses

and two tree leaves) using stepwise thermogravimetry and

found that macroalgae (Fucus vesiculosus and Ulva lactuca)

lost 40ndash44 of their carbon within 70 d whereas seagrasses

(Zostera marina and Ruppia maritima) lost 29ndash55 and tree

leaves (Fagus sylvatica and Rhizophora apiculata) lost only 0ndash

8 Similarly Josselyn and Mathieson (1980) found that

macroalgae (Ascophyllum nodosum and Fucus vesiculosus)

decomposed 3ndash10 times faster than a saltmarsh plant (Spar-

tina alterniflora) and seagrass (Zostera marina) Litter bag stud-

ies have reported a lack of change in sediment carbon

following decomposition of buried macroalgae suggesting

that the organic carbon bound within macroalgal structural

material (eg carbohydrates) is highly labile and rapidly

decomposed by microbes (Vichkovitten and Holmer 2004)

Despite this general pattern of high degradability of macroal-

gae compared with aquatic angiosperms (Trevathan-Tackett

et al in press) there is a high degree of diversity in the

structural complexity of macroalgae particularly in cell-wall

structure and carbon chemistry resulting in high variability

in decay rate estimates within the literature (Rice and Han-

son 1984 Twilley et al 1986 Kristensen 1990 Wada et al

2008 Trevathan-Tackett et al in press)

Nedzarek and Rakusa-Suszczewski (2004) examined the

decomposition of 10 Antarctic macroalgal species finding

they released 80 of the nutrients with the first 3 d of a 69

d decomposition experiment these rates occurred at polar

temperatures (48C) so it would be assumed that tropical

decomposition would be more rapid Similar results were

found with North Sea macroalgae where 50ndash80 of the tis-

sue biomass was lost within 14 d at 188C (Rieper-Kirchner

1990) which included the brown leathery kelp Laminaria

saccharina

Factors influencing the future carbon storage anddonor ability of macroalgae

This review presents a static view on the current state of

carbon cycling sequestration and donor capacity of macroal-

gae with an emphasis on Australian coastal systems In real-

ity the distribution biomass and productivity of these

macroalgae are vulnerable to change due to anthropogenic

activities and as such the dynamic nature of these macroal-

gal systems should be taken into consideration Factors such

as climate change (Duarte et al 2013) and urbanisation (Air-

oldi and Beck 2007 Airoldi et al 2008) can greatly alter the

distribution abundance and productivity of these systems

although the rate of change in global macroalgae population

size remains unknown

Climate change can greatly influence the survival photo-

synthetic capacity growth and competitive interactions of

macroalgae in coastal habitats (Wernberg et al 2011b)

Ocean warming on both the east and west coasts of Australia

have caused pole-ward movement of macroalgal species over

the past five decades (Wernberg et al 2011a) Potentially

hundreds of species are expected to be driven beyond the

edge of the Australian continent as warming continues driv-

ing not only local but global extinctions as 62 of macro-

algal species found in southern Australia are endemic to the

region (Phillips 2001) On the east coast of Australia there

has been a southern retreat of three habitat-forming macro-

algal species (Ecklonia radiata Phyllospora comosa and Durvil-

laea potatorum Millar 2007) and in eastern Tasmania the

once common Macrocystis pyrifera has almost completely dis-

appeared with ocean warming (Edyvane 2003 Johnson et al

2011)

In addition to rising temperatures climate change is

expected to influence macroalgal distribution and productiv-

ity through ocean acidification emergence of marine dis-

eases and shifts in the distribution of consumers In

terrestrial ecosystems there have been climate-driven

increases in global net primary production due to the easing

of critical climatic constraints such as increasing solar radia-

tion from reduced cloud cover (Nemani et al 2003) In the

oceans while increased CO2 dissolution is reducing pH and

disrupting carbonate chemistry this inorganic carbon is a

building block for photosynthesis The predicted changes in

CO2 in the atmosphere over the next 100 yr will translate to

a 25- to 3-fold increase in dissolved CO2 in seawater

although the subsequent drop in pH will cause shifts in the

equilibria between inorganic carbon forms HCO23 concentra-

tions will only rise by 10 and total Ci available for pho-

tosynthesis (HCO23 1 CO2) will thus rise bylt15 However

if CO2 availability is a constraint to the rate of photosynthe-

sis could the more abundant CO2 result in faster macroalgal

growth Most macroalgae have the capacity to use the

HCO23 ion that is dominant in seawater and given that the

HCO23 concentrations will not change much in future an

impact on photosynthesis is unlikely Furthermore most

macroalgae and seagrasses (Beer et al 2014) possess carbon

concentrating mechanisms (CCMs Giordano et al 2005)

which actively take up inorganic carbon (as HCO23 andor

CO2) and thereby accumulate CO2 at the active site of the

Hill et al Can macroalgae contribute to blue carbon

11

CO2-fixing enzyme Rubisco This effectively saturates

Rubisco for CO2 and limits any increased productivity of

macroalgae from elevated atmospheric CO2 and ocean acidi-

fication There are few exceptions mostly subtidal rhodo-

phytes to the rule that macroalgae possess CCMs so

increased CO2 per se is unlikely to increase CO2 drawdown

by coastal primary producers However there are suggestions

that higher CO2 may increase carbon allocation to seagrass

rhizomes under high light (ie in shallow water) and

thereby enhance burial rates (Jiang et al 2010)

Anthropogenic activities such as climate-change-

associated rising sea temperatures are expected to increase

the occurrence of macroalgal diseases through an increased

virulence of opportunistic pathogens as well as reduced

resistance to disease in thermally stressed hosts (Egan et al

2013) For example in the chemically defended macroalgae

Delisea pulchra bacterial bleaching of the thallus occurs in

response to elevated temperatures due to reduced antibacte-

rial chemical defences (Campbell et al 2011 Case et al

2011) Such diseases therefore have the capacity to reduce

macroalgal abundance either through increased consump-

tion (due to reduced herbivory defence) or through direct

host mortality (Goecke et al 2010)

With the delivery of warmer water further south the East

Australian Current not only contracts the range of many

macroalgal species but also extends the range of urchin con-

sumers Urchin barrens are now extensive throughout south-

eastern Australia and are continuing to expand at the detri-

ment of macroalgal populations (Johnson et al 2011) Such

altered ecological interactions with herbivores from this tro-

picalisation of high latitudes are therefore causing macroal-

gal populations to decline in Tasmania

While climate change will have detrimental effects on

macroalgal populations especially in temperate Australia

tropical regions may experience increased macroalgal abun-

dance following thermal pulses on coral-dominated reefs If

temperatures on coral reefs exceed summer averages by as

little as 1ndash28C mass coral bleaching events can occur which

can lead to coral mortality (Hoegh-Guldberg et al 2007)

Phase shifts toward macroalgal-dominated reefs can follow

especially if herbivory has been reduced by overfishing

(McManus et al 2000 Bruno et al 2009 Hughes et al

2010) However not all tropical macroalgal species will bene-

fit from climate change with species such as Chnoospora

implexa expected to decrease in abundance (Bender et al

2013)

When considering the donor capacity of macroalgae algal

rafts have the potential to deliver dislodged macroalgae to

receiver habitats that can bury the carbon and thus enhance

the carbon sink (see above) However changes in climate

will affect raft supply and persistence (Macreadie et al

2011) Increased storm intensities (IPCC 2007) will promote

substratum detachment andor fragmentation and hence

increase the abundance of algal fragments and rafts and

may also increase burial of macroalgal material (Macreadie

et al 2011) Elevated temperatures however may counter

this process by reducing raft longevity due to an increase in

herbivore metabolism and consumption (Macreadie et al

2011) In addition changes in ocean surface currents may

affect advection routes and potential endpoints of deposition

into more or less favorable receiver environments for

sequestration

Given the dynamic nature of macroalgal populations and

changes in abundance and productivity especially from

human activities the potential for carbon storage and export

may be highly variable In considering the role macroalgae

may play in climate change mitigation the factors detailed

above should be taken into account as they are likely to

greatly influence the contribution of macroalgae to blue car-

bon storage

Conclusions and research priorities

Although macroalgal communities in Australia and

around the world produce massive quantities of plant bio-

mass with high organic carbon content the presence of a

hard rocky substrate precludes the potential for long-term

storage of carbon within the macroalgal habitat In isolation

we therefore conclude that macroalgae do not contribute to

blue carbon

However a considerable proportion of macroalgal bio-

mass becomes dislodged from the benthos and is exported

beyond macroalgal habitat boundaries This donor carbon

may be received by habitats with long-term sequestration

capacity such as seagrass beds saltmarshes mangroves and

continental shelf regions Within Australia and globally

geographic differences in macroalgal biomass community

composition and productivity will influence the blue carbon

donor capacity of macroalgae with the greatest contribu-

tions likely to be in the temperate (and possibly polar)

regions In addition to a high rate of biomass production to

be a viable carbon donor macroalgae must be transferred to

a receiver habitat undergo burial and avoid microbial remi-

neralization The fate of detached macroalgal biomass is not

entirely clear and whilst limited data on the composition of

macroalgal biomass indicates that macroalgal carbon is

highly labile recent research has highlighted the potentially

significant role of refractory taxon-specific compounds (car-

bonates long-chain lipids alginates xylans and sulphated

polysaccharides) from macroalgae in contributing to long-

term blue carbon stores (Trevathan-Tackett et al in press)

We therefore conclude that macroalgae have the potential

to make ecologically meaningful contributions toward global

blue carbon sequestration as significant carbon donors but

further research is needed to quantify these contributions

Data on the degradability of macroalgal plant material is

limited to only a handful of taxa so there is considerable

need for additional testing on other taxa The capacity for

Hill et al Can macroalgae contribute to blue carbon

12

any incorporation of organic material from macroalgae into

long-term carbon stores is only possible if the material can

avoid decomposition by microbes potentially by entering a

storage habitat that is a rapidly accreting zone Research

therefore needs to focus on determining the burial rates of

macroalgal tissue at receiver sites which of these sites are

the greatest sink of macroalgal fragments understanding the

environmental conditions that maximise the burial process

and assessing whether burial is fast enough to limit micro-

bial remineralization of the organic macroalgal material

This will also need to include further research identifying

interspecies variation in carbon donor capacity due to rate of

lability and rate of transport to accreting zones In existing

blue carbon habitats methods for identifying macroalgal car-

bon in the storage zone also need to be developed to gauge

historical contributions of macroalgae into these zones

Once these unknowns are addressed the potential for mac-

roalgae to contribute to blue carbon as a carbon donor will

become less ambiguous Focusing future research on these

key areas will provide evidence as to whether macroalgae

should be included under the blue carbon umbrella

Macroalgal aquaculture and the harvesting of natural pop-

ulations are growing industries worldwide and are actions

that can greatly increase the carbon sequestration capacity

afforded by macroalgae (Chung et al 2011) Furthermore

the production of macroalgal biochar (a process involving

the pyrolysis of biomass) for addition to soil may represent

a viable long-term CO2 sink although research in this field

is in its infancy (Lehmann et al 2006 Bird et al 2011)

Given that macroalgal populations have the highest abun-

dance biomass and productivity of all coastal habitats they

not only store an immense amount of carbon in their living

biomass but they also have an outstanding potential to act

as significant carbon donors However macroalgae are vul-

nerable to a range of anthropogenic impacts so it is impor-

tant to protect these ecosystems for their climate-change-

mitigation potential as well as their ecosystem services

References

Agawin N S R and G M Duarte 2002 Evidence of direct

particle trapping by a tropical seagrass meadow Estuaries

25 1205ndash1209 doi101007BF02692217

Airoldi L D Balata and M W Beck 2008 The Gray Zone

Relationships between habitat loss and marine diversity

and their applications in conservation J Exp Mar Biol

Ecol 366 8ndash15 doi101016jjembe200807034

Airoldi L and M W Beck 2007 Loss status and trends for

coastal marine habitats of Europe Oceanogr Mar Biol

Ann Rev 45 345ndash405

Ang P O J 1985 Regeneration studies of Sargassum

siliquosum J ag and S paniculatum J Ag (Phaeophyta

Sargassaceae) Botanical Marina 28 231ndash235 doi101515

botm1985286231

Bala G 2013 Digesting 400 ppm for global mean CO2

concentration Curr Sci 104 1471ndash1472

Baring R J P G Fairweather and R E Lester 2014

Storm versus calm Variation in fauna associated with

drifting macrophytes in sandy beach surf zones J Exp

Mar Biol Ecol 461 397ndash406 doi101016jjembe2014

09011

Beer S M Bjeuroork and J Beardall 2014 Photosynthesis in

the marine environment Wiley

Behrenfeld M J E Mara~non D A Siegel and S B Hooker

2002 Photoacclimation and nutrient-based model of

light-saturated photosynthesis for quantifying oceanic pri-

mary production Mar Ecol Prog Ser 228 103ndash117 doi

103354meps228103

Bender D G Diaz-Pulido and S Dove 2013 The impact of

CO2 emission scenarios and nutrient enrichment on a

common coral reef macroalga is modified by temporal

effects J Phycol 50 203ndash215 doi101111jpy12153

Bird M I C M Wurster P H de Paula Silva A M Bass

and D de Nys 2011 Algal biocharmdashproduction and

properties Bioresour Technol 102 1886ndash1891 doi

101111j1757-1707201101109x

Briand X 1991 Seaweed harvesting in Europe p 293ndash308

In M D Guiry and G Blunden [eds] Seaweed resources

in Europe Uses and potential Wiley

Bruno J F H Sweatman W F Precht E R Selig and V

G W Schutte 2009 Assessing evidence of phase shifts

from coral to macroalgal dominance on coral reefs

Ecology 90 1478ndash1484 doi10189008-17811

Cacador I A L Coasta and C Vale 2004 Carbon storage

in Tagus salt marsh sediments Water Air Soil Pollut Focus

4 701ndash714 doi101023BWAFO000002838884544ce

Campbell A H T Harder S Nielsen S Kjelleberg and P D

Steinberg 2011 Climate change and disease Bleaching of

a chemically defended seaweed Glob Chang Biol 17

2958ndash2970 doi101111j1365-2486201102456x

Case R J S R Longford A H Campbell A Low N Tujula

P D Steinberg and S Kjelleberg 2011 Temperature

induced bacterial virulence and bleaching disease in a

chemically defended marine macroalga Environ Microbiol

13 529ndash537 doi101111j1462-2920201002356x

Che Hasan R D Ierodiaconou and J Monk 2012

Evaluation of four supervised learning methods for Benthic

habitat mapping using backscatter from multi-beam sonar

Remote Sens 4 3427ndash3443 doi103390rs4113427

Cheshire A C and N D Hallam 1988 Biomass and

density of native stands of Durvillaea potatorum (southern

bull-kelp) in south eastern Australia Mar Ecol Prog Ser

48 277ndash283 doi103354meps048277

Cheshire A C G Westphalen A Wenden L J Scriven

and B C Rowland 1996 Photosynthesis and respiration

of phaeophycean-dominated macroalgal communities in

summer and winter Aquat Bot 55 159ndash170 doi

101016S0304-3770(96)01071-6

Hill et al Can macroalgae contribute to blue carbon

13

TA

BLE

1

Con

tin

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Reg

ion

Lati

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eci

es

Ab

un

dan

ce

co

ver

Are

al

exte

nt

km

2

Dep

th

ran

ge

m

Bio

mass

gm

22

Bio

mass

turn

over

tim

es

yr2

1

Gro

wth

rate

d

21

Gro

wth

mg

g

FW

21

d2

1

Max

net

pro

du

ctio

n

rate

gC

m2

2d

21

To

tal

C

sto

red

inlivin

g

macr

oalg

ae

Mg

Ckm

22

Refe

ren

ces

St

Hele

ns

Poin

t

toSch

oute

n

Isla

nd

SE

Tasm

an

ia

41

8170 S

ndash

42

8S

Tota

lalg

ae

(pre

dom

inan

tly

Phyl

losp

ora

com

osa

an

d

Era

dia

ta)

70ndash100

0ndash25

Eckl

onia

4700

g

ww

tm

22

yr2

1

Phyl

losp

ora

7400

g

ww

tm

22

yr2

1

San

ders

on

(1990)

Luci

eer

et

al

(2007a)

Hig

hYello

w

Blu

ffto

Cap

e

Hauy

Georg

e

III

Rock

SE

Tasm

an

ia

43

8Sndash

43

8300 S

Ph

aeop

hyce

ae

(pre

dom

inan

tly

Era

dia

ta)

Rh

od

op

hyta

Ch

loro

ph

yta

43ndash48

46ndash10

7

20ndash40

20ndash30

to40ndash50

20ndash30

Luci

eer

et

al

(2012)

Valu

es

use

dto

est

imate

carb

on

stora

ge

ass

oci

ated

with

bio

mass

of

south

-east

ern

Aust

ralia

nsu

btid

alm

acr

oalg

ae

daggerV

alu

es

use

dto

est

imate

carb

on

stora

ge

ass

oci

ated

with

bio

mass

of

EA

Con

the

Gre

at

Barr

ier

Reef

DaggerExtr

ap

ola

ted

valu

es

from

pub

lish

ed

dat

ab

ase

don

fwt

d

wt

ratio

of

46

0g

Cg

21

dw

tan

d03

12

gC

g2

1d

wt

(Rave

net

al

1989)

sectExtr

ap

ola

ted

valu

es

from

pub

lish

ed

dat

aan

dass

um

ing

maxim

alp

hoto

syn

thetic

rate

for

12

hd

21

(Rave

net

al

1989)

details and justification for these choices are given in the

next section

Studies from around the world were used for all other pur-

poses of the review and informed the findings from the Aus-

tralian continent in terms of the potential for above- and

below-ground carbon storage across a range of habitats com-

parable to macroalgal communities which are known for

their efficacy in carbon sequestration (terrestrial forests salt-

marshes mangrove forests and seagrass beds) Total carbon

stored in Australia was calculated for each habitat from data

reported in the literature (Table 2) Minimum and maximum

values were calculated by multiplication of the carbon stor-

age capacity per unit area of each habitat type by the area

of that habitat found in Australia Studies from around the

world were also used to provide a rationale for the review

and contributed to the general discussion to provide a global

perspective on calcification decomposition and the influ-

ence of anthropogenic impacts on the blue carbon capacity

of macroalgae

Potential for macroalgae to directly store carbon

Macroalgae are known to have very high rates of primary

productivity and growth and significant biomass on coastal

margins (Mann 1973 Chung et al 2011) particularly in

temperate regions (Mann 1973 Cheshire et al 1996 Connell

and Irving 2008) Macroalgae are typically associated with

hard substrata to which they attach and grow obtaining

their nutritional needs from the surrounding water rather

than via vascular root systems penetrating the sediment As

such and unlike other aquatic macrophytes their biomass is

all ldquoabove groundrdquo with the exception of calcifying algae

that can build up significant calcium carbonate deposits in

the sediments (eg Halimeda in Table 1 and below) and sto-

loniferous taxa such as Caulerpa The capacity for noncalcify-

ing macroalgae to directly store carbon is thus largely

associated with the above ground living biomass and how

long the carbon within living biomass remains fixed before

being remineralized by bacteria

Australia has an extensive coastline with about 30 in

the temperate coastal zone dominated by large macroalgae

such as Durvillaea potatorum (found 0ndash5 m deep) Ecklonia

radiata and mixed fucoids (occurring down to 40 m depth)

including Phyllospora comosa Cystophora spp Sargassum spp

(Table 1) and Scytothalia doryocarpa in the west (Wernberg

et al 2003) However for most of the Australian coast data

on areal extent biomass and productivity of macroalgae are

very fragmented and often reported in non-standardised

units (Table 1) Moreover there are few records of standing

stock of carbon or carbon contents of particular species that

allow extrapolation from available biomass data Thus accu-

rate assessments of the total amount of carbon stored in

Table 2 Organic carbon stored both above and below ground in terrestrial forests and different marine ecosystems in Australia

Ecosystem

Carbon stored (Mg C km22) Area in

Australia

(km2)

Total C

stored in

Australia (Tg C) ReferencesAbove ground Below ground Total

Terrestrial forests 5700ndash21700 6200ndash23000 11900ndash44700 1494000 177786ndash667818 Malhi et al (1999)

Fourqurean

et al (2012)

Department of

Agriculture (2013)

Saltmarsh 67ndash922 207ndash12972 274ndash13894 13029 36ndash1810 Cacador et al (2004)

Howe et al (2009)

OzCoasts (2013)

Mangrove 9750ndash31724 5731ndash67816 16792ndash99540 3976 668ndash3958 Twilley et al (1992)

Howe et al (2009)

Fourqurean

et al (2012)

OzCoasts (2013)

Seagrass 01ndash555 01ndash83678 02ndash84233 296 (temperate

Australia)

21482 (all

of Australia)

592 3 1025ndash249

430 3 1023ndash18095

Fourqurean et al (2012)

Waycott et al (2009)

OzCoasts (2013)

Australian

temperate

macroalgae

2200 0 2200 49939ndash124849 1099ndash2747 This study

Hill et al Can macroalgae contribute to blue carbon

7

living biomass of macroalgae in Australia are at this stage

difficult to determine We estimate however that the coastal

waters of southern Australia with D potatorum in the upper

subtidal and E radiata monospecific andor mixed fucoid

dominated assemblages to 30 m that support an understorey

of turfing algae that may extend to 60 m in depth could

store in excess of 2200 Mg C km22 (Table 1) If we extrapolate

to the temperate coastal waters of Australialt60 m depth

(249697 km2 Whiteway 2009) and assume that approxi-

mately 50 (124849 km2) of coastal waters are rocky reef

(based on data compiled from Victoria Australia in Ierodiaco-

nou et al 2007 Rattray et al 2009 Ierodiaconou et al 2011

Che Hasan et al 2012 Monk et al 2012 Rattray et al 2013)

we estimate 2747 Tg C may be directly stored in living mac-

roalgal biomass in temperate Australia (Table 2) The above

studies targeted reef areas but there are large expanses of

sandy sediments in temperate Australia (eg Ninety-mile

beach Victoria) so if we take a more conservative estimate

of 20 (49939 km2) reef to 60 m we estimate 1099 Tg C

stored in living macroalgal biomass in temperate Australia

(Table 2) For tropical and subtropical Australia data are even

sparser but based on estimates of carbon storage by epilithic

algal communities the Great Barrier Reef may store 232 Tg C

in epilithic algae alone (675 g C m22 3 344400 km2 Table 1)

The capacity for carbon storage per unit area in macroalgae is

generally lower than for other blue carbon habitats and ter-

restrial forests due to the absence of below ground biomass

(Table 2) However the vast extent of temperate macroalgae

communities makes total carbon storage comparable to the

other blue carbon habitats (saltmarsh mangroves and sea-

grass beds) which have both above and below ground carbon

storage (Table 2) We of course acknowledge that there are

temporal and spatial variability in productivity biomass and

carbon content of different species (Table 1) and thus these

values are crude estimates only New data on aerial extent

biomass and carbon storage for algal species and assemblages

from around Australia will improve our estimates Compara-

ble data for other regions are needed for reliable global esti-

mates of carbon storage in macroalgal living biomass

Seasonality in alternation of generations fragmentation

and dislodgment (Thomsen et al 2004 McKenzie and Bell-

grove 2009 Krumhansl et al 2011) of macroalgae all con-

tribute to high turnover of macroalgal biomass High

productivity and growth rates of macroalgae replenish the

biomass There are however no comprehensive data on the

spatial and temporal variability in biomass of any macroalgal

species in Australia (references in Table 1) Assuming rela-

tively stable annual macroalgal standing stock productivity

growth and turnover do not affect the potential for macroal-

gae to directly store carbon in the above ground biomass

High productivity will not result in more carbon storage

unless it equates to greater total biomass However high

rates of productivity growth and turnover do become impor-

tant to carbon-storage potential of macroalgae if we consider

their possible role as carbon donors to other systems which

is a function of their decay rate en route to receiver sites the

burial efficiency of the receiver site and their structural com-

plexity (ie susceptibility to being remineralized) We

explore this role in more detail below (see ldquoMacroalgae as

carbon donorsrdquo)

Calcification in macroalgae

All macroalgal groups contain genera that form calcium

carbonate deposits and calcified algae are found in the

photic zone of all marine habitats from polar to tropical seas

(Nelson 2009) In the Phaeophyceae calcification is most

notable in Padina though a few other brown algae also cal-

cify The calcifying Chlorophyte algae are mostly tropical

and contain genera such as Acetabularia Neomeris Avrainvil-

lea and most importantly in terms of its contribution Hali-

meda Many red algae are calcifying both in tropical and

cold waters but calcification is best known in the Coralli-

nales with both geniculate and nongeniculate or crustose

forms Free-living nongeniculate corallines are known as rho-

doliths and form extensive beds which are harvested in

Europe and elsewhere (eg Brazil) In most cases the calcium

carbonate is found as the mineral aragonite either deposited

at the cell surface (eg Padina) or in intercellular spaces

(eg Halimeda) Calcium carbonate can also be deposited as

calcite which has a different crystal structure to aragonite

making it more stable and less prone to dissolution in sea-

water especially under the lowered carbonate concentrations

likely to be found with increasing ocean acidification in the

future Calcite is found in external crusts on Chaetomorpha

and within the cell walls of coralline genera such as Litho-

phyllum and Lithothamnion (Lobban and Harrison 1994)

Many calcifying algae also grow epiphytically on seagrass

leaves as well as on other marine organisms including

bivalves and molluscs Indeed seagrass photosynthesis can

promote calcification rates by other organisms such as Hali-

meda growing in seagrass beds (Semesi et al 2009)

Although many of the algae that calcify are slow growing

the calcium carbonate (aragonite and especially calcite) can

persist in the marine environment long after the living cells

have decayed Iconic calcium carbonate deposits such as the

White Cliffs of Dover are the remains of marine calcifying

microalgae deposited over geological time The rhodolith

beds in France and Brazil are harvested to the rate of

500 Gg yr21 (Briand 1991) and up to 120 Gg yr21 (Riul et al

2008) respectively for industrial processes including agricul-

ture water purification mineralization and the manufacture

of cosmetics (Grall and Hall-Spencer 2003) Carbonate depo-

sition (accumulation) in coastal waters (including coral reefs)

globally is in the order of 12 Pg CaCO3 yr21 (017 Pg C yr21)

with approximately the same accumulated in the pelagic

ocean though production rates in the open ocean are closer

to 11 Pg C yr21 (Iglesias-Rodriguez et al 2002) Decomposed

Halimeda tissues are important sediment elements in tropical

Hill et al Can macroalgae contribute to blue carbon

8

regions (Table 1) and contribute the major part of the cal-

careous sediment found in the sandy beaches of many tropi-

cal shores Halimeda bioherms alone have been estimated to

contribute 400 Tg CaCO3 yr21 to CaCO3 accumulation (Hillis

1997) Rhodolith forming species can produce in the region

of 60ndash1000 g CaCO3 m22 yr21 with CaCO3 deposits off Bra-

zilrsquos coast alone of 2 Pg (Riul et al 2008 Nelson 2009)

Importantly carbonates deposited by oceanic organisms

have not previously been included in blue carbon budgets

This is because the calcification process (Eq 1) results in the

release of 1 CO2 for every CaCO3 formed

2 HCO23 1Ca21 CaCO31CO21H2O (1)

However the CO2 produced in this way can be rapidly

utilised in photosynthesis and even if it is not (during calcifi-

cation in the dark for instance) there is still the net conver-

sion of one soluble HCO23 into one insoluble carbonate

(ie calcification still results in net drawdown of carbon in

the recalcitrant carbonate minerals aragonite or calcite)

Given the significant contribution of macroalgal calcifica-

tion to the global C budget and the persistence of CaCO3 in

sediments we would argue that calcification should be con-

sidered in any calculations of blue carbon into the future If

included this would constitute a further 034 Pg C yr21

sequestered globally

Macroalgae as carbon donors

So far we have established that most macroalgal species

have limited capacity to act as long-term carbon sinks in

their own right (Table 2) largely due to their inability to

accumulate below-ground stores of carbon relative to other

vegetated coastal habitats such as seagrasses saltmarshes

and mangroves However even though macroalgae do not

develop significant carbon deposits themselves there still

exists the possibility that they could make significant contri-

butions to global carbon sequestration by acting as ldquocarbon

donorsrdquo In this section we explore this possibility

What is a ldquocarbon donorrdquo Here we define a carbon donor

as an autotroph that ldquodonatesrdquo carbon to another ldquoreceiverrdquo

habitat that ultimately buries that carbon Therefore carbon

donors make indirect contributions to carbon sequestration

Such movement of carbon from one system to another is

referred to as ldquoleakagerdquo (or ldquospilloverrdquo) A well-recognised

example of leakage can be seen in seagrass ecosystems Sea-

grasses have a high particle-trapping capacity (Agawin and

Duarte 2002 Gruber and Kemp 2010) and due to their

occurrence at the interface between land and sea they cap-

ture large amounts of terrestrial carbon that runs off the

land following rainfall events (Kennedy et al 2010 Macrea-

die et al 2014) This externally derived carbon that leaks

into a receiver habitat is termed ldquoallochthonousrdquo carbon In

seagrasses allochthonous carbon can contribute as much as

half the total organic carbon that is sequestered in a meadow

(Kennedy et al 2010)

From a carbon accounting perspective leakage of carbon

is a complex issue Can habitats take credit for carbon that

they didnrsquot produce What happens if the carbon was

already credited to another system (double-counting) How

can the origin of carbon be determined These questions are

at the forefront of many terrestrial carbon-offset programs

(eg REDD) but have received comparatively little attention

in the aquatic fields The matter of carbon accounting of

leakage will however become increasingly important with

the rising prominence of blue carbon but is beyond the

scope of this review We recommend Murray et al (2007) for

more information on leakage

For a system to be a significant carbon donor there are

three requirements (1) high rates of biomass production (2)

effective transfer of biomass to receiver habitats and (3) the

donor carbon must undergo efficient burial of allochthonous

biomass within receiver habitats such that it evades micro-

bial attack (the latter is a function of several factors includ-

ing the intrinsic stability of the carbon physical

mechanisms of protection and environmental conditions

that dictate microbial activity) All three requirements are

necessary none are redundant or substitutable The first

requirement has already been discussed earlier in this article

and can be summarised as follows macroalgae have excep-

tionally high biomass production their global extent (2ndash68

million km2) and primary production (019ndash064 Pg C yr21)

exceeds that of all the vegetated coastal habitats (seagrass

beds saltmarshes mangroves) combined (Duarte et al

2013) In the following section we will discuss requirements

2 and 3 which concern the export and fate of this biomass

production

Export and fate of macroalgal biomass

to receiver habitats

Most macroalgal species spend their early life history

attached to benthic (hard) substrata (Leurouning 1990) but then

become dislodged or fragmented and can undergo a period

of transport in surface or bottom waters by wind and water

movement (potentially as rafts that travel significant distan-

ces) until eventually sinking disintegrating or becoming

cast upon land (Thiel 2003 Thiel and Gutow 2005 Macrea-

die et al 2011) Detachment of macroalgal tissue can arise

from natural senescence (Ang 1985) dislodgement by herbi-

vores (Kingsford 1992 Tegner et al 1995) and through

hydrodynamic forces such as waves and storms (Duggins

et al 2003) The supply quality persistence and transport

(trajectory and duration) of macroalgal rafts are all influ-

enced by climate (Macreadie et al 2011) particularly tem-

perature (Graiff et al 2013) Thus whilst there is temporal

variation in the extent of macroalgal rafts related to these

processes there is continuous export of macroalgal biomass

throughout the year whereas saltmarsh and seagrass detrital

Hill et al Can macroalgae contribute to blue carbon

9

export tends to be seasonal (Josselyn and Mathieson 1980)

Furthermore acknowledging spatial variation in the export

of macroalgal and vascular plant biomass macroalgae are

often more significant contributors to surf-zone and beach

wrack than seagrasses (Josselyn and Mathieson 1980 Gomez

et al 2013 Baring et al 2014 Ruiz-Delgado et al 2014)

From genetic and tracking studies we know that exported

macroalgal biomass can be transported long distances (Thiel

and Haye 2006 Fraser et al 2009 2010 2011 Nikula et al

2010) but there is limited information on what happens to

carbon bound within macroalgal biomass once rafts or frag-

ments sink and disintegratemdashie the point at which carbon

bound within macroalgal biomass is broken down into dis-

solved and particulate organic carbon Wada et al (2007)

suggested that macroalgae could release 20ndash40 of their pro-

ductivity as dissolved organic matter (DOM) Much of the

macroalgal DOM is likely to be microbially degraded but

estimates of the refractory component of this DOM will be

important for understanding how much could be donated to

other habitats UV is known to degrade DOM this means

that if this matter can be deposited in regions away from

light such as the deep ocean the breakdown will be further

diminished

There is some evidence to suggest that macroalgal carbon

is donated to other receiver habitats that have long-term

sequestration capacity including the deep sea (Wada et al

2008 Dierssen et al 2009) and other vegetated coastal habi-

tats such as mangrove forests seagrass beds and salt

marshes (Hyndes et al 2012 Macreadie et al 2012) In tropi-

cal estuaries and bays it is estimated that about half of the

macroalgal biomass produced is consumed by herbivores and

the other half is exported to other habitats whereas in the

temperate open coast most of the biomass is decomposed by

detritivores with a lesser amount being exported and only

small fractions being consumed or accumulated as detritus

(Hyndes et al 2013) The fate of macroalgal biomass in tem-

perate estuaries and fjords is largely unknown (Hyndes et al

2013) Most export of macroalgal biomass occurs via advec-

tion but there are also complex biotic pathways that trans-

port macroalgal biomass into receiver habitats such as via

ingestion and concomitant faecal deposition of carbon

within receiver habitats by fish which can contribute to car-

bon sequestration by fertilising receiver habitats and thereby

increasing their productivity and sequestration capacity

(Valiela 1995 Hyndes et al 2013) Breakdown of macroalgae

has been shown to be mostly mediated by microbial proc-

esses (Rieper-Kirchner 1990) however protozoans and meio-

fauna also contribute to the decomposition of macroalgal

tissues as well as enhance microbial degradation Microbial

breakdown rate is also dependent upon the sediment com-

position and oxic status of the water Sassi et al (1988)

found that macroalgal decomposition rates over 25 d under

aerobic vs anaerobic conditions were 35 and 24 respec-

tively Therefore if the macroalgal detritus can be advected

to a rapidly sedimenting region where it can be incorporated

into an anaerobic sediment this will slow the microbial

breakdown and maintain the carbon within the sediment

longer More research is needed to understand how long this

carbon actually remains within anaerobic sediment

All macroalgal carbon that enters the sedimentary carbon

pool will eventually be broken down (oxidised and reminer-

alized) by microbes and converted to inorganic forms and

potentially returned to the atmosphere The rate and effi-

ciency of this remineralization process can dictate whether

macroalgal carbon remains bound within sediments for

months or millennia Macroalgal carbon entering the sedi-

mentary pool has three possible fates (1) particulate and dis-

solved organic carbon that is recalcitrant to microbial

degradation is likely to remain stored within the sediment

for prolonged periods while labile carbon will be recycled by

heterotrophic bacteria and is either (2) assimilated into

microbial biomass or (3) respired as CO2 back to the water

column and possibly the atmosphere The proportion of

nonrespired carbon represents the amount of macroalgal car-

bon that is sequestered

It should be recognised that macroalgae lack the struc-

tural polysaccharide complexity of higher plants and conse-

quently their decomposition rates are faster (Sassi et al

1988) To better understand the degradation pathways of

macroalgal plant material within aquatic sediments

researchers have used several techniques Analyses of ele-

mental composition and stable isotope signatures are rou-

tinely used to ldquofingerprintrdquo carbon and determine its origin

although there is difficultly in separating microalgal and

macroalgal organic carbon signatures (Hardison et al 2011)

Furthermore isotopic signatures may also be variable in

space and time during the decomposition process (Fenton

and Ritz 1988) Similarly a problem with identifying sources

of organic carbon based on carbohydrate composition is that

many groups of organisms contain the same carbohydrates

(Vichkovitten and Holmer 2004) Fatty acid signatures have

proven to offer better resolution of the different plant contri-

butions to organic matter (Hardison et al 2013) although

the level of complexity using this technique is much higher

(Graeve et al 2002) Manipulative approaches using isotopic

tracer studies (Hee et al 2001 Hardison et al 2010 2011

Hyndes et al 2012) and radiolabelling (Chidthaisong et al

1999) have proved to be robust for studying the incorpora-

tion of macroalgal carbon into sediments

Reliable data on the fate of decomposed macroalgal

carbon within sediments (eg macroalgal carbon that is

ldquolostrdquo during litter bag mass loss experiments) is scarce

Hardison et al (2010) traced carbon from senescing macroal-

gae (Gracilaria spp) that were pre-labeled with the 13C stable

isotope and found that 2ndash9 of macroalgal carbon was

incorporated into the sediment This percentage of macroal-

gal carbon uptake by sediments is relatively high suggesting

efficient burial however the fate of this buried carbon was

Hill et al Can macroalgae contribute to blue carbon

10

only monitored for 2 weeks so it is not known whether this

carbon stock was sequestered long-term Other studies sug-

gest that macroalgal carbon is not sequestered long-term For

example Garcia-Robledo et al (2008) found that macroalgal

detritus (tubular and planar Ulva spp) that entered sedimen-

tary organic carbon pools vanished within days after its ini-

tial appearance indicating that carbon from such simple and

ephemeral macroalgae is not retained for durations that

would make them an important component of the long-

term carbon pool within a receiver habitat However given

the diversity in the cell walls and carbon chemistry of mac-

roalgae it is difficult to make conclusions on likely persist-

ence of sequestered macroalgae based on only a handful of

studies

Kristensen (1994) compared the decomposition rate of six

different plant materials (two macroalgae two seagrasses

and two tree leaves) using stepwise thermogravimetry and

found that macroalgae (Fucus vesiculosus and Ulva lactuca)

lost 40ndash44 of their carbon within 70 d whereas seagrasses

(Zostera marina and Ruppia maritima) lost 29ndash55 and tree

leaves (Fagus sylvatica and Rhizophora apiculata) lost only 0ndash

8 Similarly Josselyn and Mathieson (1980) found that

macroalgae (Ascophyllum nodosum and Fucus vesiculosus)

decomposed 3ndash10 times faster than a saltmarsh plant (Spar-

tina alterniflora) and seagrass (Zostera marina) Litter bag stud-

ies have reported a lack of change in sediment carbon

following decomposition of buried macroalgae suggesting

that the organic carbon bound within macroalgal structural

material (eg carbohydrates) is highly labile and rapidly

decomposed by microbes (Vichkovitten and Holmer 2004)

Despite this general pattern of high degradability of macroal-

gae compared with aquatic angiosperms (Trevathan-Tackett

et al in press) there is a high degree of diversity in the

structural complexity of macroalgae particularly in cell-wall

structure and carbon chemistry resulting in high variability

in decay rate estimates within the literature (Rice and Han-

son 1984 Twilley et al 1986 Kristensen 1990 Wada et al

2008 Trevathan-Tackett et al in press)

Nedzarek and Rakusa-Suszczewski (2004) examined the

decomposition of 10 Antarctic macroalgal species finding

they released 80 of the nutrients with the first 3 d of a 69

d decomposition experiment these rates occurred at polar

temperatures (48C) so it would be assumed that tropical

decomposition would be more rapid Similar results were

found with North Sea macroalgae where 50ndash80 of the tis-

sue biomass was lost within 14 d at 188C (Rieper-Kirchner

1990) which included the brown leathery kelp Laminaria

saccharina

Factors influencing the future carbon storage anddonor ability of macroalgae

This review presents a static view on the current state of

carbon cycling sequestration and donor capacity of macroal-

gae with an emphasis on Australian coastal systems In real-

ity the distribution biomass and productivity of these

macroalgae are vulnerable to change due to anthropogenic

activities and as such the dynamic nature of these macroal-

gal systems should be taken into consideration Factors such

as climate change (Duarte et al 2013) and urbanisation (Air-

oldi and Beck 2007 Airoldi et al 2008) can greatly alter the

distribution abundance and productivity of these systems

although the rate of change in global macroalgae population

size remains unknown

Climate change can greatly influence the survival photo-

synthetic capacity growth and competitive interactions of

macroalgae in coastal habitats (Wernberg et al 2011b)

Ocean warming on both the east and west coasts of Australia

have caused pole-ward movement of macroalgal species over

the past five decades (Wernberg et al 2011a) Potentially

hundreds of species are expected to be driven beyond the

edge of the Australian continent as warming continues driv-

ing not only local but global extinctions as 62 of macro-

algal species found in southern Australia are endemic to the

region (Phillips 2001) On the east coast of Australia there

has been a southern retreat of three habitat-forming macro-

algal species (Ecklonia radiata Phyllospora comosa and Durvil-

laea potatorum Millar 2007) and in eastern Tasmania the

once common Macrocystis pyrifera has almost completely dis-

appeared with ocean warming (Edyvane 2003 Johnson et al

2011)

In addition to rising temperatures climate change is

expected to influence macroalgal distribution and productiv-

ity through ocean acidification emergence of marine dis-

eases and shifts in the distribution of consumers In

terrestrial ecosystems there have been climate-driven

increases in global net primary production due to the easing

of critical climatic constraints such as increasing solar radia-

tion from reduced cloud cover (Nemani et al 2003) In the

oceans while increased CO2 dissolution is reducing pH and

disrupting carbonate chemistry this inorganic carbon is a

building block for photosynthesis The predicted changes in

CO2 in the atmosphere over the next 100 yr will translate to

a 25- to 3-fold increase in dissolved CO2 in seawater

although the subsequent drop in pH will cause shifts in the

equilibria between inorganic carbon forms HCO23 concentra-

tions will only rise by 10 and total Ci available for pho-

tosynthesis (HCO23 1 CO2) will thus rise bylt15 However

if CO2 availability is a constraint to the rate of photosynthe-

sis could the more abundant CO2 result in faster macroalgal

growth Most macroalgae have the capacity to use the

HCO23 ion that is dominant in seawater and given that the

HCO23 concentrations will not change much in future an

impact on photosynthesis is unlikely Furthermore most

macroalgae and seagrasses (Beer et al 2014) possess carbon

concentrating mechanisms (CCMs Giordano et al 2005)

which actively take up inorganic carbon (as HCO23 andor

CO2) and thereby accumulate CO2 at the active site of the

Hill et al Can macroalgae contribute to blue carbon

11

CO2-fixing enzyme Rubisco This effectively saturates

Rubisco for CO2 and limits any increased productivity of

macroalgae from elevated atmospheric CO2 and ocean acidi-

fication There are few exceptions mostly subtidal rhodo-

phytes to the rule that macroalgae possess CCMs so

increased CO2 per se is unlikely to increase CO2 drawdown

by coastal primary producers However there are suggestions

that higher CO2 may increase carbon allocation to seagrass

rhizomes under high light (ie in shallow water) and

thereby enhance burial rates (Jiang et al 2010)

Anthropogenic activities such as climate-change-

associated rising sea temperatures are expected to increase

the occurrence of macroalgal diseases through an increased

virulence of opportunistic pathogens as well as reduced

resistance to disease in thermally stressed hosts (Egan et al

2013) For example in the chemically defended macroalgae

Delisea pulchra bacterial bleaching of the thallus occurs in

response to elevated temperatures due to reduced antibacte-

rial chemical defences (Campbell et al 2011 Case et al

2011) Such diseases therefore have the capacity to reduce

macroalgal abundance either through increased consump-

tion (due to reduced herbivory defence) or through direct

host mortality (Goecke et al 2010)

With the delivery of warmer water further south the East

Australian Current not only contracts the range of many

macroalgal species but also extends the range of urchin con-

sumers Urchin barrens are now extensive throughout south-

eastern Australia and are continuing to expand at the detri-

ment of macroalgal populations (Johnson et al 2011) Such

altered ecological interactions with herbivores from this tro-

picalisation of high latitudes are therefore causing macroal-

gal populations to decline in Tasmania

While climate change will have detrimental effects on

macroalgal populations especially in temperate Australia

tropical regions may experience increased macroalgal abun-

dance following thermal pulses on coral-dominated reefs If

temperatures on coral reefs exceed summer averages by as

little as 1ndash28C mass coral bleaching events can occur which

can lead to coral mortality (Hoegh-Guldberg et al 2007)

Phase shifts toward macroalgal-dominated reefs can follow

especially if herbivory has been reduced by overfishing

(McManus et al 2000 Bruno et al 2009 Hughes et al

2010) However not all tropical macroalgal species will bene-

fit from climate change with species such as Chnoospora

implexa expected to decrease in abundance (Bender et al

2013)

When considering the donor capacity of macroalgae algal

rafts have the potential to deliver dislodged macroalgae to

receiver habitats that can bury the carbon and thus enhance

the carbon sink (see above) However changes in climate

will affect raft supply and persistence (Macreadie et al

2011) Increased storm intensities (IPCC 2007) will promote

substratum detachment andor fragmentation and hence

increase the abundance of algal fragments and rafts and

may also increase burial of macroalgal material (Macreadie

et al 2011) Elevated temperatures however may counter

this process by reducing raft longevity due to an increase in

herbivore metabolism and consumption (Macreadie et al

2011) In addition changes in ocean surface currents may

affect advection routes and potential endpoints of deposition

into more or less favorable receiver environments for

sequestration

Given the dynamic nature of macroalgal populations and

changes in abundance and productivity especially from

human activities the potential for carbon storage and export

may be highly variable In considering the role macroalgae

may play in climate change mitigation the factors detailed

above should be taken into account as they are likely to

greatly influence the contribution of macroalgae to blue car-

bon storage

Conclusions and research priorities

Although macroalgal communities in Australia and

around the world produce massive quantities of plant bio-

mass with high organic carbon content the presence of a

hard rocky substrate precludes the potential for long-term

storage of carbon within the macroalgal habitat In isolation

we therefore conclude that macroalgae do not contribute to

blue carbon

However a considerable proportion of macroalgal bio-

mass becomes dislodged from the benthos and is exported

beyond macroalgal habitat boundaries This donor carbon

may be received by habitats with long-term sequestration

capacity such as seagrass beds saltmarshes mangroves and

continental shelf regions Within Australia and globally

geographic differences in macroalgal biomass community

composition and productivity will influence the blue carbon

donor capacity of macroalgae with the greatest contribu-

tions likely to be in the temperate (and possibly polar)

regions In addition to a high rate of biomass production to

be a viable carbon donor macroalgae must be transferred to

a receiver habitat undergo burial and avoid microbial remi-

neralization The fate of detached macroalgal biomass is not

entirely clear and whilst limited data on the composition of

macroalgal biomass indicates that macroalgal carbon is

highly labile recent research has highlighted the potentially

significant role of refractory taxon-specific compounds (car-

bonates long-chain lipids alginates xylans and sulphated

polysaccharides) from macroalgae in contributing to long-

term blue carbon stores (Trevathan-Tackett et al in press)

We therefore conclude that macroalgae have the potential

to make ecologically meaningful contributions toward global

blue carbon sequestration as significant carbon donors but

further research is needed to quantify these contributions

Data on the degradability of macroalgal plant material is

limited to only a handful of taxa so there is considerable

need for additional testing on other taxa The capacity for

Hill et al Can macroalgae contribute to blue carbon

12

any incorporation of organic material from macroalgae into

long-term carbon stores is only possible if the material can

avoid decomposition by microbes potentially by entering a

storage habitat that is a rapidly accreting zone Research

therefore needs to focus on determining the burial rates of

macroalgal tissue at receiver sites which of these sites are

the greatest sink of macroalgal fragments understanding the

environmental conditions that maximise the burial process

and assessing whether burial is fast enough to limit micro-

bial remineralization of the organic macroalgal material

This will also need to include further research identifying

interspecies variation in carbon donor capacity due to rate of

lability and rate of transport to accreting zones In existing

blue carbon habitats methods for identifying macroalgal car-

bon in the storage zone also need to be developed to gauge

historical contributions of macroalgae into these zones

Once these unknowns are addressed the potential for mac-

roalgae to contribute to blue carbon as a carbon donor will

become less ambiguous Focusing future research on these

key areas will provide evidence as to whether macroalgae

should be included under the blue carbon umbrella

Macroalgal aquaculture and the harvesting of natural pop-

ulations are growing industries worldwide and are actions

that can greatly increase the carbon sequestration capacity

afforded by macroalgae (Chung et al 2011) Furthermore

the production of macroalgal biochar (a process involving

the pyrolysis of biomass) for addition to soil may represent

a viable long-term CO2 sink although research in this field

is in its infancy (Lehmann et al 2006 Bird et al 2011)

Given that macroalgal populations have the highest abun-

dance biomass and productivity of all coastal habitats they

not only store an immense amount of carbon in their living

biomass but they also have an outstanding potential to act

as significant carbon donors However macroalgae are vul-

nerable to a range of anthropogenic impacts so it is impor-

tant to protect these ecosystems for their climate-change-

mitigation potential as well as their ecosystem services

References

Agawin N S R and G M Duarte 2002 Evidence of direct

particle trapping by a tropical seagrass meadow Estuaries

25 1205ndash1209 doi101007BF02692217

Airoldi L D Balata and M W Beck 2008 The Gray Zone

Relationships between habitat loss and marine diversity

and their applications in conservation J Exp Mar Biol

Ecol 366 8ndash15 doi101016jjembe200807034

Airoldi L and M W Beck 2007 Loss status and trends for

coastal marine habitats of Europe Oceanogr Mar Biol

Ann Rev 45 345ndash405

Ang P O J 1985 Regeneration studies of Sargassum

siliquosum J ag and S paniculatum J Ag (Phaeophyta

Sargassaceae) Botanical Marina 28 231ndash235 doi101515

botm1985286231

Bala G 2013 Digesting 400 ppm for global mean CO2

concentration Curr Sci 104 1471ndash1472

Baring R J P G Fairweather and R E Lester 2014

Storm versus calm Variation in fauna associated with

drifting macrophytes in sandy beach surf zones J Exp

Mar Biol Ecol 461 397ndash406 doi101016jjembe2014

09011

Beer S M Bjeuroork and J Beardall 2014 Photosynthesis in

the marine environment Wiley

Behrenfeld M J E Mara~non D A Siegel and S B Hooker

2002 Photoacclimation and nutrient-based model of

light-saturated photosynthesis for quantifying oceanic pri-

mary production Mar Ecol Prog Ser 228 103ndash117 doi

103354meps228103

Bender D G Diaz-Pulido and S Dove 2013 The impact of

CO2 emission scenarios and nutrient enrichment on a

common coral reef macroalga is modified by temporal

effects J Phycol 50 203ndash215 doi101111jpy12153

Bird M I C M Wurster P H de Paula Silva A M Bass

and D de Nys 2011 Algal biocharmdashproduction and

properties Bioresour Technol 102 1886ndash1891 doi

101111j1757-1707201101109x

Briand X 1991 Seaweed harvesting in Europe p 293ndash308

In M D Guiry and G Blunden [eds] Seaweed resources

in Europe Uses and potential Wiley

Bruno J F H Sweatman W F Precht E R Selig and V

G W Schutte 2009 Assessing evidence of phase shifts

from coral to macroalgal dominance on coral reefs

Ecology 90 1478ndash1484 doi10189008-17811

Cacador I A L Coasta and C Vale 2004 Carbon storage

in Tagus salt marsh sediments Water Air Soil Pollut Focus

4 701ndash714 doi101023BWAFO000002838884544ce

Campbell A H T Harder S Nielsen S Kjelleberg and P D

Steinberg 2011 Climate change and disease Bleaching of

a chemically defended seaweed Glob Chang Biol 17

2958ndash2970 doi101111j1365-2486201102456x

Case R J S R Longford A H Campbell A Low N Tujula

P D Steinberg and S Kjelleberg 2011 Temperature

induced bacterial virulence and bleaching disease in a

chemically defended marine macroalga Environ Microbiol

13 529ndash537 doi101111j1462-2920201002356x

Che Hasan R D Ierodiaconou and J Monk 2012

Evaluation of four supervised learning methods for Benthic

habitat mapping using backscatter from multi-beam sonar

Remote Sens 4 3427ndash3443 doi103390rs4113427

Cheshire A C and N D Hallam 1988 Biomass and

density of native stands of Durvillaea potatorum (southern

bull-kelp) in south eastern Australia Mar Ecol Prog Ser

48 277ndash283 doi103354meps048277

Cheshire A C G Westphalen A Wenden L J Scriven

and B C Rowland 1996 Photosynthesis and respiration

of phaeophycean-dominated macroalgal communities in

summer and winter Aquat Bot 55 159ndash170 doi

101016S0304-3770(96)01071-6

Hill et al Can macroalgae contribute to blue carbon

13

details and justification for these choices are given in the

next section

Studies from around the world were used for all other pur-

poses of the review and informed the findings from the Aus-

tralian continent in terms of the potential for above- and

below-ground carbon storage across a range of habitats com-

parable to macroalgal communities which are known for

their efficacy in carbon sequestration (terrestrial forests salt-

marshes mangrove forests and seagrass beds) Total carbon

stored in Australia was calculated for each habitat from data

reported in the literature (Table 2) Minimum and maximum

values were calculated by multiplication of the carbon stor-

age capacity per unit area of each habitat type by the area

of that habitat found in Australia Studies from around the

world were also used to provide a rationale for the review

and contributed to the general discussion to provide a global

perspective on calcification decomposition and the influ-

ence of anthropogenic impacts on the blue carbon capacity

of macroalgae

Potential for macroalgae to directly store carbon

Macroalgae are known to have very high rates of primary

productivity and growth and significant biomass on coastal

margins (Mann 1973 Chung et al 2011) particularly in

temperate regions (Mann 1973 Cheshire et al 1996 Connell

and Irving 2008) Macroalgae are typically associated with

hard substrata to which they attach and grow obtaining

their nutritional needs from the surrounding water rather

than via vascular root systems penetrating the sediment As

such and unlike other aquatic macrophytes their biomass is

all ldquoabove groundrdquo with the exception of calcifying algae

that can build up significant calcium carbonate deposits in

the sediments (eg Halimeda in Table 1 and below) and sto-

loniferous taxa such as Caulerpa The capacity for noncalcify-

ing macroalgae to directly store carbon is thus largely

associated with the above ground living biomass and how

long the carbon within living biomass remains fixed before

being remineralized by bacteria

Australia has an extensive coastline with about 30 in

the temperate coastal zone dominated by large macroalgae

such as Durvillaea potatorum (found 0ndash5 m deep) Ecklonia

radiata and mixed fucoids (occurring down to 40 m depth)

including Phyllospora comosa Cystophora spp Sargassum spp

(Table 1) and Scytothalia doryocarpa in the west (Wernberg

et al 2003) However for most of the Australian coast data

on areal extent biomass and productivity of macroalgae are

very fragmented and often reported in non-standardised

units (Table 1) Moreover there are few records of standing

stock of carbon or carbon contents of particular species that

allow extrapolation from available biomass data Thus accu-

rate assessments of the total amount of carbon stored in

Table 2 Organic carbon stored both above and below ground in terrestrial forests and different marine ecosystems in Australia

Ecosystem

Carbon stored (Mg C km22) Area in

Australia

(km2)

Total C

stored in

Australia (Tg C) ReferencesAbove ground Below ground Total

Terrestrial forests 5700ndash21700 6200ndash23000 11900ndash44700 1494000 177786ndash667818 Malhi et al (1999)

Fourqurean

et al (2012)

Department of

Agriculture (2013)

Saltmarsh 67ndash922 207ndash12972 274ndash13894 13029 36ndash1810 Cacador et al (2004)

Howe et al (2009)

OzCoasts (2013)

Mangrove 9750ndash31724 5731ndash67816 16792ndash99540 3976 668ndash3958 Twilley et al (1992)

Howe et al (2009)

Fourqurean

et al (2012)

OzCoasts (2013)

Seagrass 01ndash555 01ndash83678 02ndash84233 296 (temperate

Australia)

21482 (all

of Australia)

592 3 1025ndash249

430 3 1023ndash18095

Fourqurean et al (2012)

Waycott et al (2009)

OzCoasts (2013)

Australian

temperate

macroalgae

2200 0 2200 49939ndash124849 1099ndash2747 This study

Hill et al Can macroalgae contribute to blue carbon

7

living biomass of macroalgae in Australia are at this stage

difficult to determine We estimate however that the coastal

waters of southern Australia with D potatorum in the upper

subtidal and E radiata monospecific andor mixed fucoid

dominated assemblages to 30 m that support an understorey

of turfing algae that may extend to 60 m in depth could

store in excess of 2200 Mg C km22 (Table 1) If we extrapolate

to the temperate coastal waters of Australialt60 m depth

(249697 km2 Whiteway 2009) and assume that approxi-

mately 50 (124849 km2) of coastal waters are rocky reef

(based on data compiled from Victoria Australia in Ierodiaco-

nou et al 2007 Rattray et al 2009 Ierodiaconou et al 2011

Che Hasan et al 2012 Monk et al 2012 Rattray et al 2013)

we estimate 2747 Tg C may be directly stored in living mac-

roalgal biomass in temperate Australia (Table 2) The above

studies targeted reef areas but there are large expanses of

sandy sediments in temperate Australia (eg Ninety-mile

beach Victoria) so if we take a more conservative estimate

of 20 (49939 km2) reef to 60 m we estimate 1099 Tg C

stored in living macroalgal biomass in temperate Australia

(Table 2) For tropical and subtropical Australia data are even

sparser but based on estimates of carbon storage by epilithic

algal communities the Great Barrier Reef may store 232 Tg C

in epilithic algae alone (675 g C m22 3 344400 km2 Table 1)

The capacity for carbon storage per unit area in macroalgae is

generally lower than for other blue carbon habitats and ter-

restrial forests due to the absence of below ground biomass

(Table 2) However the vast extent of temperate macroalgae

communities makes total carbon storage comparable to the

other blue carbon habitats (saltmarsh mangroves and sea-

grass beds) which have both above and below ground carbon

storage (Table 2) We of course acknowledge that there are

temporal and spatial variability in productivity biomass and

carbon content of different species (Table 1) and thus these

values are crude estimates only New data on aerial extent

biomass and carbon storage for algal species and assemblages

from around Australia will improve our estimates Compara-

ble data for other regions are needed for reliable global esti-

mates of carbon storage in macroalgal living biomass

Seasonality in alternation of generations fragmentation

and dislodgment (Thomsen et al 2004 McKenzie and Bell-

grove 2009 Krumhansl et al 2011) of macroalgae all con-

tribute to high turnover of macroalgal biomass High

productivity and growth rates of macroalgae replenish the

biomass There are however no comprehensive data on the

spatial and temporal variability in biomass of any macroalgal

species in Australia (references in Table 1) Assuming rela-

tively stable annual macroalgal standing stock productivity

growth and turnover do not affect the potential for macroal-

gae to directly store carbon in the above ground biomass

High productivity will not result in more carbon storage

unless it equates to greater total biomass However high

rates of productivity growth and turnover do become impor-

tant to carbon-storage potential of macroalgae if we consider

their possible role as carbon donors to other systems which

is a function of their decay rate en route to receiver sites the

burial efficiency of the receiver site and their structural com-

plexity (ie susceptibility to being remineralized) We

explore this role in more detail below (see ldquoMacroalgae as

carbon donorsrdquo)

Calcification in macroalgae

All macroalgal groups contain genera that form calcium

carbonate deposits and calcified algae are found in the

photic zone of all marine habitats from polar to tropical seas

(Nelson 2009) In the Phaeophyceae calcification is most

notable in Padina though a few other brown algae also cal-

cify The calcifying Chlorophyte algae are mostly tropical

and contain genera such as Acetabularia Neomeris Avrainvil-

lea and most importantly in terms of its contribution Hali-

meda Many red algae are calcifying both in tropical and

cold waters but calcification is best known in the Coralli-

nales with both geniculate and nongeniculate or crustose

forms Free-living nongeniculate corallines are known as rho-

doliths and form extensive beds which are harvested in

Europe and elsewhere (eg Brazil) In most cases the calcium

carbonate is found as the mineral aragonite either deposited

at the cell surface (eg Padina) or in intercellular spaces

(eg Halimeda) Calcium carbonate can also be deposited as

calcite which has a different crystal structure to aragonite

making it more stable and less prone to dissolution in sea-

water especially under the lowered carbonate concentrations

likely to be found with increasing ocean acidification in the

future Calcite is found in external crusts on Chaetomorpha

and within the cell walls of coralline genera such as Litho-

phyllum and Lithothamnion (Lobban and Harrison 1994)

Many calcifying algae also grow epiphytically on seagrass

leaves as well as on other marine organisms including

bivalves and molluscs Indeed seagrass photosynthesis can

promote calcification rates by other organisms such as Hali-

meda growing in seagrass beds (Semesi et al 2009)

Although many of the algae that calcify are slow growing

the calcium carbonate (aragonite and especially calcite) can

persist in the marine environment long after the living cells

have decayed Iconic calcium carbonate deposits such as the

White Cliffs of Dover are the remains of marine calcifying

microalgae deposited over geological time The rhodolith

beds in France and Brazil are harvested to the rate of

500 Gg yr21 (Briand 1991) and up to 120 Gg yr21 (Riul et al

2008) respectively for industrial processes including agricul-

ture water purification mineralization and the manufacture

of cosmetics (Grall and Hall-Spencer 2003) Carbonate depo-

sition (accumulation) in coastal waters (including coral reefs)

globally is in the order of 12 Pg CaCO3 yr21 (017 Pg C yr21)

with approximately the same accumulated in the pelagic

ocean though production rates in the open ocean are closer

to 11 Pg C yr21 (Iglesias-Rodriguez et al 2002) Decomposed

Halimeda tissues are important sediment elements in tropical

Hill et al Can macroalgae contribute to blue carbon

8

regions (Table 1) and contribute the major part of the cal-

careous sediment found in the sandy beaches of many tropi-

cal shores Halimeda bioherms alone have been estimated to

contribute 400 Tg CaCO3 yr21 to CaCO3 accumulation (Hillis

1997) Rhodolith forming species can produce in the region

of 60ndash1000 g CaCO3 m22 yr21 with CaCO3 deposits off Bra-

zilrsquos coast alone of 2 Pg (Riul et al 2008 Nelson 2009)

Importantly carbonates deposited by oceanic organisms

have not previously been included in blue carbon budgets

This is because the calcification process (Eq 1) results in the

release of 1 CO2 for every CaCO3 formed

2 HCO23 1Ca21 CaCO31CO21H2O (1)

However the CO2 produced in this way can be rapidly

utilised in photosynthesis and even if it is not (during calcifi-

cation in the dark for instance) there is still the net conver-

sion of one soluble HCO23 into one insoluble carbonate

(ie calcification still results in net drawdown of carbon in

the recalcitrant carbonate minerals aragonite or calcite)

Given the significant contribution of macroalgal calcifica-

tion to the global C budget and the persistence of CaCO3 in

sediments we would argue that calcification should be con-

sidered in any calculations of blue carbon into the future If

included this would constitute a further 034 Pg C yr21

sequestered globally

Macroalgae as carbon donors

So far we have established that most macroalgal species

have limited capacity to act as long-term carbon sinks in

their own right (Table 2) largely due to their inability to

accumulate below-ground stores of carbon relative to other

vegetated coastal habitats such as seagrasses saltmarshes

and mangroves However even though macroalgae do not

develop significant carbon deposits themselves there still

exists the possibility that they could make significant contri-

butions to global carbon sequestration by acting as ldquocarbon

donorsrdquo In this section we explore this possibility

What is a ldquocarbon donorrdquo Here we define a carbon donor

as an autotroph that ldquodonatesrdquo carbon to another ldquoreceiverrdquo

habitat that ultimately buries that carbon Therefore carbon

donors make indirect contributions to carbon sequestration

Such movement of carbon from one system to another is

referred to as ldquoleakagerdquo (or ldquospilloverrdquo) A well-recognised

example of leakage can be seen in seagrass ecosystems Sea-

grasses have a high particle-trapping capacity (Agawin and

Duarte 2002 Gruber and Kemp 2010) and due to their

occurrence at the interface between land and sea they cap-

ture large amounts of terrestrial carbon that runs off the

land following rainfall events (Kennedy et al 2010 Macrea-

die et al 2014) This externally derived carbon that leaks

into a receiver habitat is termed ldquoallochthonousrdquo carbon In

seagrasses allochthonous carbon can contribute as much as

half the total organic carbon that is sequestered in a meadow

(Kennedy et al 2010)

From a carbon accounting perspective leakage of carbon

is a complex issue Can habitats take credit for carbon that

they didnrsquot produce What happens if the carbon was

already credited to another system (double-counting) How

can the origin of carbon be determined These questions are

at the forefront of many terrestrial carbon-offset programs

(eg REDD) but have received comparatively little attention

in the aquatic fields The matter of carbon accounting of

leakage will however become increasingly important with

the rising prominence of blue carbon but is beyond the

scope of this review We recommend Murray et al (2007) for

more information on leakage

For a system to be a significant carbon donor there are

three requirements (1) high rates of biomass production (2)

effective transfer of biomass to receiver habitats and (3) the

donor carbon must undergo efficient burial of allochthonous

biomass within receiver habitats such that it evades micro-

bial attack (the latter is a function of several factors includ-

ing the intrinsic stability of the carbon physical

mechanisms of protection and environmental conditions

that dictate microbial activity) All three requirements are

necessary none are redundant or substitutable The first

requirement has already been discussed earlier in this article

and can be summarised as follows macroalgae have excep-

tionally high biomass production their global extent (2ndash68

million km2) and primary production (019ndash064 Pg C yr21)

exceeds that of all the vegetated coastal habitats (seagrass

beds saltmarshes mangroves) combined (Duarte et al

2013) In the following section we will discuss requirements

2 and 3 which concern the export and fate of this biomass

production

Export and fate of macroalgal biomass

to receiver habitats

Most macroalgal species spend their early life history

attached to benthic (hard) substrata (Leurouning 1990) but then

become dislodged or fragmented and can undergo a period

of transport in surface or bottom waters by wind and water

movement (potentially as rafts that travel significant distan-

ces) until eventually sinking disintegrating or becoming

cast upon land (Thiel 2003 Thiel and Gutow 2005 Macrea-

die et al 2011) Detachment of macroalgal tissue can arise

from natural senescence (Ang 1985) dislodgement by herbi-

vores (Kingsford 1992 Tegner et al 1995) and through

hydrodynamic forces such as waves and storms (Duggins

et al 2003) The supply quality persistence and transport

(trajectory and duration) of macroalgal rafts are all influ-

enced by climate (Macreadie et al 2011) particularly tem-

perature (Graiff et al 2013) Thus whilst there is temporal

variation in the extent of macroalgal rafts related to these

processes there is continuous export of macroalgal biomass

throughout the year whereas saltmarsh and seagrass detrital

Hill et al Can macroalgae contribute to blue carbon

9

export tends to be seasonal (Josselyn and Mathieson 1980)

Furthermore acknowledging spatial variation in the export

of macroalgal and vascular plant biomass macroalgae are

often more significant contributors to surf-zone and beach

wrack than seagrasses (Josselyn and Mathieson 1980 Gomez

et al 2013 Baring et al 2014 Ruiz-Delgado et al 2014)

From genetic and tracking studies we know that exported

macroalgal biomass can be transported long distances (Thiel

and Haye 2006 Fraser et al 2009 2010 2011 Nikula et al

2010) but there is limited information on what happens to

carbon bound within macroalgal biomass once rafts or frag-

ments sink and disintegratemdashie the point at which carbon

bound within macroalgal biomass is broken down into dis-

solved and particulate organic carbon Wada et al (2007)

suggested that macroalgae could release 20ndash40 of their pro-

ductivity as dissolved organic matter (DOM) Much of the

macroalgal DOM is likely to be microbially degraded but

estimates of the refractory component of this DOM will be

important for understanding how much could be donated to

other habitats UV is known to degrade DOM this means

that if this matter can be deposited in regions away from

light such as the deep ocean the breakdown will be further

diminished

There is some evidence to suggest that macroalgal carbon

is donated to other receiver habitats that have long-term

sequestration capacity including the deep sea (Wada et al

2008 Dierssen et al 2009) and other vegetated coastal habi-

tats such as mangrove forests seagrass beds and salt

marshes (Hyndes et al 2012 Macreadie et al 2012) In tropi-

cal estuaries and bays it is estimated that about half of the

macroalgal biomass produced is consumed by herbivores and

the other half is exported to other habitats whereas in the

temperate open coast most of the biomass is decomposed by

detritivores with a lesser amount being exported and only

small fractions being consumed or accumulated as detritus

(Hyndes et al 2013) The fate of macroalgal biomass in tem-

perate estuaries and fjords is largely unknown (Hyndes et al

2013) Most export of macroalgal biomass occurs via advec-

tion but there are also complex biotic pathways that trans-

port macroalgal biomass into receiver habitats such as via

ingestion and concomitant faecal deposition of carbon

within receiver habitats by fish which can contribute to car-

bon sequestration by fertilising receiver habitats and thereby

increasing their productivity and sequestration capacity

(Valiela 1995 Hyndes et al 2013) Breakdown of macroalgae

has been shown to be mostly mediated by microbial proc-

esses (Rieper-Kirchner 1990) however protozoans and meio-

fauna also contribute to the decomposition of macroalgal

tissues as well as enhance microbial degradation Microbial

breakdown rate is also dependent upon the sediment com-

position and oxic status of the water Sassi et al (1988)

found that macroalgal decomposition rates over 25 d under

aerobic vs anaerobic conditions were 35 and 24 respec-

tively Therefore if the macroalgal detritus can be advected

to a rapidly sedimenting region where it can be incorporated

into an anaerobic sediment this will slow the microbial

breakdown and maintain the carbon within the sediment

longer More research is needed to understand how long this

carbon actually remains within anaerobic sediment

All macroalgal carbon that enters the sedimentary carbon

pool will eventually be broken down (oxidised and reminer-

alized) by microbes and converted to inorganic forms and

potentially returned to the atmosphere The rate and effi-

ciency of this remineralization process can dictate whether

macroalgal carbon remains bound within sediments for

months or millennia Macroalgal carbon entering the sedi-

mentary pool has three possible fates (1) particulate and dis-

solved organic carbon that is recalcitrant to microbial

degradation is likely to remain stored within the sediment

for prolonged periods while labile carbon will be recycled by

heterotrophic bacteria and is either (2) assimilated into

microbial biomass or (3) respired as CO2 back to the water

column and possibly the atmosphere The proportion of

nonrespired carbon represents the amount of macroalgal car-

bon that is sequestered

It should be recognised that macroalgae lack the struc-

tural polysaccharide complexity of higher plants and conse-

quently their decomposition rates are faster (Sassi et al

1988) To better understand the degradation pathways of

macroalgal plant material within aquatic sediments

researchers have used several techniques Analyses of ele-

mental composition and stable isotope signatures are rou-

tinely used to ldquofingerprintrdquo carbon and determine its origin

although there is difficultly in separating microalgal and

macroalgal organic carbon signatures (Hardison et al 2011)

Furthermore isotopic signatures may also be variable in

space and time during the decomposition process (Fenton

and Ritz 1988) Similarly a problem with identifying sources

of organic carbon based on carbohydrate composition is that

many groups of organisms contain the same carbohydrates

(Vichkovitten and Holmer 2004) Fatty acid signatures have

proven to offer better resolution of the different plant contri-

butions to organic matter (Hardison et al 2013) although

the level of complexity using this technique is much higher

(Graeve et al 2002) Manipulative approaches using isotopic

tracer studies (Hee et al 2001 Hardison et al 2010 2011

Hyndes et al 2012) and radiolabelling (Chidthaisong et al

1999) have proved to be robust for studying the incorpora-

tion of macroalgal carbon into sediments

Reliable data on the fate of decomposed macroalgal

carbon within sediments (eg macroalgal carbon that is

ldquolostrdquo during litter bag mass loss experiments) is scarce

Hardison et al (2010) traced carbon from senescing macroal-

gae (Gracilaria spp) that were pre-labeled with the 13C stable

isotope and found that 2ndash9 of macroalgal carbon was

incorporated into the sediment This percentage of macroal-

gal carbon uptake by sediments is relatively high suggesting

efficient burial however the fate of this buried carbon was

Hill et al Can macroalgae contribute to blue carbon

10

only monitored for 2 weeks so it is not known whether this

carbon stock was sequestered long-term Other studies sug-

gest that macroalgal carbon is not sequestered long-term For

example Garcia-Robledo et al (2008) found that macroalgal

detritus (tubular and planar Ulva spp) that entered sedimen-

tary organic carbon pools vanished within days after its ini-

tial appearance indicating that carbon from such simple and

ephemeral macroalgae is not retained for durations that

would make them an important component of the long-

term carbon pool within a receiver habitat However given

the diversity in the cell walls and carbon chemistry of mac-

roalgae it is difficult to make conclusions on likely persist-

ence of sequestered macroalgae based on only a handful of

studies

Kristensen (1994) compared the decomposition rate of six

different plant materials (two macroalgae two seagrasses

and two tree leaves) using stepwise thermogravimetry and

found that macroalgae (Fucus vesiculosus and Ulva lactuca)

lost 40ndash44 of their carbon within 70 d whereas seagrasses

(Zostera marina and Ruppia maritima) lost 29ndash55 and tree

leaves (Fagus sylvatica and Rhizophora apiculata) lost only 0ndash

8 Similarly Josselyn and Mathieson (1980) found that

macroalgae (Ascophyllum nodosum and Fucus vesiculosus)

decomposed 3ndash10 times faster than a saltmarsh plant (Spar-

tina alterniflora) and seagrass (Zostera marina) Litter bag stud-

ies have reported a lack of change in sediment carbon

following decomposition of buried macroalgae suggesting

that the organic carbon bound within macroalgal structural

material (eg carbohydrates) is highly labile and rapidly

decomposed by microbes (Vichkovitten and Holmer 2004)

Despite this general pattern of high degradability of macroal-

gae compared with aquatic angiosperms (Trevathan-Tackett

et al in press) there is a high degree of diversity in the

structural complexity of macroalgae particularly in cell-wall

structure and carbon chemistry resulting in high variability

in decay rate estimates within the literature (Rice and Han-

son 1984 Twilley et al 1986 Kristensen 1990 Wada et al

2008 Trevathan-Tackett et al in press)

Nedzarek and Rakusa-Suszczewski (2004) examined the

decomposition of 10 Antarctic macroalgal species finding

they released 80 of the nutrients with the first 3 d of a 69

d decomposition experiment these rates occurred at polar

temperatures (48C) so it would be assumed that tropical

decomposition would be more rapid Similar results were

found with North Sea macroalgae where 50ndash80 of the tis-

sue biomass was lost within 14 d at 188C (Rieper-Kirchner

1990) which included the brown leathery kelp Laminaria

saccharina

Factors influencing the future carbon storage anddonor ability of macroalgae

This review presents a static view on the current state of

carbon cycling sequestration and donor capacity of macroal-

gae with an emphasis on Australian coastal systems In real-

ity the distribution biomass and productivity of these

macroalgae are vulnerable to change due to anthropogenic

activities and as such the dynamic nature of these macroal-

gal systems should be taken into consideration Factors such

as climate change (Duarte et al 2013) and urbanisation (Air-

oldi and Beck 2007 Airoldi et al 2008) can greatly alter the

distribution abundance and productivity of these systems

although the rate of change in global macroalgae population

size remains unknown

Climate change can greatly influence the survival photo-

synthetic capacity growth and competitive interactions of

macroalgae in coastal habitats (Wernberg et al 2011b)

Ocean warming on both the east and west coasts of Australia

have caused pole-ward movement of macroalgal species over

the past five decades (Wernberg et al 2011a) Potentially

hundreds of species are expected to be driven beyond the

edge of the Australian continent as warming continues driv-

ing not only local but global extinctions as 62 of macro-

algal species found in southern Australia are endemic to the

region (Phillips 2001) On the east coast of Australia there

has been a southern retreat of three habitat-forming macro-

algal species (Ecklonia radiata Phyllospora comosa and Durvil-

laea potatorum Millar 2007) and in eastern Tasmania the

once common Macrocystis pyrifera has almost completely dis-

appeared with ocean warming (Edyvane 2003 Johnson et al

2011)

In addition to rising temperatures climate change is

expected to influence macroalgal distribution and productiv-

ity through ocean acidification emergence of marine dis-

eases and shifts in the distribution of consumers In

terrestrial ecosystems there have been climate-driven

increases in global net primary production due to the easing

of critical climatic constraints such as increasing solar radia-

tion from reduced cloud cover (Nemani et al 2003) In the

oceans while increased CO2 dissolution is reducing pH and

disrupting carbonate chemistry this inorganic carbon is a

building block for photosynthesis The predicted changes in

CO2 in the atmosphere over the next 100 yr will translate to

a 25- to 3-fold increase in dissolved CO2 in seawater

although the subsequent drop in pH will cause shifts in the

equilibria between inorganic carbon forms HCO23 concentra-

tions will only rise by 10 and total Ci available for pho-

tosynthesis (HCO23 1 CO2) will thus rise bylt15 However

if CO2 availability is a constraint to the rate of photosynthe-

sis could the more abundant CO2 result in faster macroalgal

growth Most macroalgae have the capacity to use the

HCO23 ion that is dominant in seawater and given that the

HCO23 concentrations will not change much in future an

impact on photosynthesis is unlikely Furthermore most

macroalgae and seagrasses (Beer et al 2014) possess carbon

concentrating mechanisms (CCMs Giordano et al 2005)

which actively take up inorganic carbon (as HCO23 andor

CO2) and thereby accumulate CO2 at the active site of the

Hill et al Can macroalgae contribute to blue carbon

11

CO2-fixing enzyme Rubisco This effectively saturates

Rubisco for CO2 and limits any increased productivity of

macroalgae from elevated atmospheric CO2 and ocean acidi-

fication There are few exceptions mostly subtidal rhodo-

phytes to the rule that macroalgae possess CCMs so

increased CO2 per se is unlikely to increase CO2 drawdown

by coastal primary producers However there are suggestions

that higher CO2 may increase carbon allocation to seagrass

rhizomes under high light (ie in shallow water) and

thereby enhance burial rates (Jiang et al 2010)

Anthropogenic activities such as climate-change-

associated rising sea temperatures are expected to increase

the occurrence of macroalgal diseases through an increased

virulence of opportunistic pathogens as well as reduced

resistance to disease in thermally stressed hosts (Egan et al

2013) For example in the chemically defended macroalgae

Delisea pulchra bacterial bleaching of the thallus occurs in

response to elevated temperatures due to reduced antibacte-

rial chemical defences (Campbell et al 2011 Case et al

2011) Such diseases therefore have the capacity to reduce

macroalgal abundance either through increased consump-

tion (due to reduced herbivory defence) or through direct

host mortality (Goecke et al 2010)

With the delivery of warmer water further south the East

Australian Current not only contracts the range of many

macroalgal species but also extends the range of urchin con-

sumers Urchin barrens are now extensive throughout south-

eastern Australia and are continuing to expand at the detri-

ment of macroalgal populations (Johnson et al 2011) Such

altered ecological interactions with herbivores from this tro-

picalisation of high latitudes are therefore causing macroal-

gal populations to decline in Tasmania

While climate change will have detrimental effects on

macroalgal populations especially in temperate Australia

tropical regions may experience increased macroalgal abun-

dance following thermal pulses on coral-dominated reefs If

temperatures on coral reefs exceed summer averages by as

little as 1ndash28C mass coral bleaching events can occur which

can lead to coral mortality (Hoegh-Guldberg et al 2007)

Phase shifts toward macroalgal-dominated reefs can follow

especially if herbivory has been reduced by overfishing

(McManus et al 2000 Bruno et al 2009 Hughes et al

2010) However not all tropical macroalgal species will bene-

fit from climate change with species such as Chnoospora

implexa expected to decrease in abundance (Bender et al

2013)

When considering the donor capacity of macroalgae algal

rafts have the potential to deliver dislodged macroalgae to

receiver habitats that can bury the carbon and thus enhance

the carbon sink (see above) However changes in climate

will affect raft supply and persistence (Macreadie et al

2011) Increased storm intensities (IPCC 2007) will promote

substratum detachment andor fragmentation and hence

increase the abundance of algal fragments and rafts and

may also increase burial of macroalgal material (Macreadie

et al 2011) Elevated temperatures however may counter

this process by reducing raft longevity due to an increase in

herbivore metabolism and consumption (Macreadie et al

2011) In addition changes in ocean surface currents may

affect advection routes and potential endpoints of deposition

into more or less favorable receiver environments for

sequestration

Given the dynamic nature of macroalgal populations and

changes in abundance and productivity especially from

human activities the potential for carbon storage and export

may be highly variable In considering the role macroalgae

may play in climate change mitigation the factors detailed

above should be taken into account as they are likely to

greatly influence the contribution of macroalgae to blue car-

bon storage

Conclusions and research priorities

Although macroalgal communities in Australia and

around the world produce massive quantities of plant bio-

mass with high organic carbon content the presence of a

hard rocky substrate precludes the potential for long-term

storage of carbon within the macroalgal habitat In isolation

we therefore conclude that macroalgae do not contribute to

blue carbon

However a considerable proportion of macroalgal bio-

mass becomes dislodged from the benthos and is exported

beyond macroalgal habitat boundaries This donor carbon

may be received by habitats with long-term sequestration

capacity such as seagrass beds saltmarshes mangroves and

continental shelf regions Within Australia and globally

geographic differences in macroalgal biomass community

composition and productivity will influence the blue carbon

donor capacity of macroalgae with the greatest contribu-

tions likely to be in the temperate (and possibly polar)

regions In addition to a high rate of biomass production to

be a viable carbon donor macroalgae must be transferred to

a receiver habitat undergo burial and avoid microbial remi-

neralization The fate of detached macroalgal biomass is not

entirely clear and whilst limited data on the composition of

macroalgal biomass indicates that macroalgal carbon is

highly labile recent research has highlighted the potentially

significant role of refractory taxon-specific compounds (car-

bonates long-chain lipids alginates xylans and sulphated

polysaccharides) from macroalgae in contributing to long-

term blue carbon stores (Trevathan-Tackett et al in press)

We therefore conclude that macroalgae have the potential

to make ecologically meaningful contributions toward global

blue carbon sequestration as significant carbon donors but

further research is needed to quantify these contributions

Data on the degradability of macroalgal plant material is

limited to only a handful of taxa so there is considerable

need for additional testing on other taxa The capacity for

Hill et al Can macroalgae contribute to blue carbon

12

any incorporation of organic material from macroalgae into

long-term carbon stores is only possible if the material can

avoid decomposition by microbes potentially by entering a

storage habitat that is a rapidly accreting zone Research

therefore needs to focus on determining the burial rates of

macroalgal tissue at receiver sites which of these sites are

the greatest sink of macroalgal fragments understanding the

environmental conditions that maximise the burial process

and assessing whether burial is fast enough to limit micro-

bial remineralization of the organic macroalgal material

This will also need to include further research identifying

interspecies variation in carbon donor capacity due to rate of

lability and rate of transport to accreting zones In existing

blue carbon habitats methods for identifying macroalgal car-

bon in the storage zone also need to be developed to gauge

historical contributions of macroalgae into these zones

Once these unknowns are addressed the potential for mac-

roalgae to contribute to blue carbon as a carbon donor will

become less ambiguous Focusing future research on these

key areas will provide evidence as to whether macroalgae

should be included under the blue carbon umbrella

Macroalgal aquaculture and the harvesting of natural pop-

ulations are growing industries worldwide and are actions

that can greatly increase the carbon sequestration capacity

afforded by macroalgae (Chung et al 2011) Furthermore

the production of macroalgal biochar (a process involving

the pyrolysis of biomass) for addition to soil may represent

a viable long-term CO2 sink although research in this field

is in its infancy (Lehmann et al 2006 Bird et al 2011)

Given that macroalgal populations have the highest abun-

dance biomass and productivity of all coastal habitats they

not only store an immense amount of carbon in their living

biomass but they also have an outstanding potential to act

as significant carbon donors However macroalgae are vul-

nerable to a range of anthropogenic impacts so it is impor-

tant to protect these ecosystems for their climate-change-

mitigation potential as well as their ecosystem services

References

Agawin N S R and G M Duarte 2002 Evidence of direct

particle trapping by a tropical seagrass meadow Estuaries

25 1205ndash1209 doi101007BF02692217

Airoldi L D Balata and M W Beck 2008 The Gray Zone

Relationships between habitat loss and marine diversity

and their applications in conservation J Exp Mar Biol

Ecol 366 8ndash15 doi101016jjembe200807034

Airoldi L and M W Beck 2007 Loss status and trends for

coastal marine habitats of Europe Oceanogr Mar Biol

Ann Rev 45 345ndash405

Ang P O J 1985 Regeneration studies of Sargassum

siliquosum J ag and S paniculatum J Ag (Phaeophyta

Sargassaceae) Botanical Marina 28 231ndash235 doi101515

botm1985286231

Bala G 2013 Digesting 400 ppm for global mean CO2

concentration Curr Sci 104 1471ndash1472

Baring R J P G Fairweather and R E Lester 2014

Storm versus calm Variation in fauna associated with

drifting macrophytes in sandy beach surf zones J Exp

Mar Biol Ecol 461 397ndash406 doi101016jjembe2014

09011

Beer S M Bjeuroork and J Beardall 2014 Photosynthesis in

the marine environment Wiley

Behrenfeld M J E Mara~non D A Siegel and S B Hooker

2002 Photoacclimation and nutrient-based model of

light-saturated photosynthesis for quantifying oceanic pri-

mary production Mar Ecol Prog Ser 228 103ndash117 doi

103354meps228103

Bender D G Diaz-Pulido and S Dove 2013 The impact of

CO2 emission scenarios and nutrient enrichment on a

common coral reef macroalga is modified by temporal

effects J Phycol 50 203ndash215 doi101111jpy12153

Bird M I C M Wurster P H de Paula Silva A M Bass

and D de Nys 2011 Algal biocharmdashproduction and

properties Bioresour Technol 102 1886ndash1891 doi

101111j1757-1707201101109x

Briand X 1991 Seaweed harvesting in Europe p 293ndash308

In M D Guiry and G Blunden [eds] Seaweed resources

in Europe Uses and potential Wiley

Bruno J F H Sweatman W F Precht E R Selig and V

G W Schutte 2009 Assessing evidence of phase shifts

from coral to macroalgal dominance on coral reefs

Ecology 90 1478ndash1484 doi10189008-17811

Cacador I A L Coasta and C Vale 2004 Carbon storage

in Tagus salt marsh sediments Water Air Soil Pollut Focus

4 701ndash714 doi101023BWAFO000002838884544ce

Campbell A H T Harder S Nielsen S Kjelleberg and P D

Steinberg 2011 Climate change and disease Bleaching of

a chemically defended seaweed Glob Chang Biol 17

2958ndash2970 doi101111j1365-2486201102456x

Case R J S R Longford A H Campbell A Low N Tujula

P D Steinberg and S Kjelleberg 2011 Temperature

induced bacterial virulence and bleaching disease in a

chemically defended marine macroalga Environ Microbiol

13 529ndash537 doi101111j1462-2920201002356x

Che Hasan R D Ierodiaconou and J Monk 2012

Evaluation of four supervised learning methods for Benthic

habitat mapping using backscatter from multi-beam sonar

Remote Sens 4 3427ndash3443 doi103390rs4113427

Cheshire A C and N D Hallam 1988 Biomass and

density of native stands of Durvillaea potatorum (southern

bull-kelp) in south eastern Australia Mar Ecol Prog Ser

48 277ndash283 doi103354meps048277

Cheshire A C G Westphalen A Wenden L J Scriven

and B C Rowland 1996 Photosynthesis and respiration

of phaeophycean-dominated macroalgal communities in

summer and winter Aquat Bot 55 159ndash170 doi

101016S0304-3770(96)01071-6

Hill et al Can macroalgae contribute to blue carbon

13

living biomass of macroalgae in Australia are at this stage

difficult to determine We estimate however that the coastal

waters of southern Australia with D potatorum in the upper

subtidal and E radiata monospecific andor mixed fucoid

dominated assemblages to 30 m that support an understorey

of turfing algae that may extend to 60 m in depth could

store in excess of 2200 Mg C km22 (Table 1) If we extrapolate

to the temperate coastal waters of Australialt60 m depth

(249697 km2 Whiteway 2009) and assume that approxi-

mately 50 (124849 km2) of coastal waters are rocky reef

(based on data compiled from Victoria Australia in Ierodiaco-

nou et al 2007 Rattray et al 2009 Ierodiaconou et al 2011

Che Hasan et al 2012 Monk et al 2012 Rattray et al 2013)

we estimate 2747 Tg C may be directly stored in living mac-

roalgal biomass in temperate Australia (Table 2) The above

studies targeted reef areas but there are large expanses of

sandy sediments in temperate Australia (eg Ninety-mile

beach Victoria) so if we take a more conservative estimate

of 20 (49939 km2) reef to 60 m we estimate 1099 Tg C

stored in living macroalgal biomass in temperate Australia

(Table 2) For tropical and subtropical Australia data are even

sparser but based on estimates of carbon storage by epilithic

algal communities the Great Barrier Reef may store 232 Tg C

in epilithic algae alone (675 g C m22 3 344400 km2 Table 1)

The capacity for carbon storage per unit area in macroalgae is

generally lower than for other blue carbon habitats and ter-

restrial forests due to the absence of below ground biomass

(Table 2) However the vast extent of temperate macroalgae

communities makes total carbon storage comparable to the

other blue carbon habitats (saltmarsh mangroves and sea-

grass beds) which have both above and below ground carbon

storage (Table 2) We of course acknowledge that there are

temporal and spatial variability in productivity biomass and

carbon content of different species (Table 1) and thus these

values are crude estimates only New data on aerial extent

biomass and carbon storage for algal species and assemblages

from around Australia will improve our estimates Compara-

ble data for other regions are needed for reliable global esti-

mates of carbon storage in macroalgal living biomass

Seasonality in alternation of generations fragmentation

and dislodgment (Thomsen et al 2004 McKenzie and Bell-

grove 2009 Krumhansl et al 2011) of macroalgae all con-

tribute to high turnover of macroalgal biomass High

productivity and growth rates of macroalgae replenish the

biomass There are however no comprehensive data on the

spatial and temporal variability in biomass of any macroalgal

species in Australia (references in Table 1) Assuming rela-

tively stable annual macroalgal standing stock productivity

growth and turnover do not affect the potential for macroal-

gae to directly store carbon in the above ground biomass

High productivity will not result in more carbon storage

unless it equates to greater total biomass However high

rates of productivity growth and turnover do become impor-

tant to carbon-storage potential of macroalgae if we consider

their possible role as carbon donors to other systems which

is a function of their decay rate en route to receiver sites the

burial efficiency of the receiver site and their structural com-

plexity (ie susceptibility to being remineralized) We

explore this role in more detail below (see ldquoMacroalgae as

carbon donorsrdquo)

Calcification in macroalgae

All macroalgal groups contain genera that form calcium

carbonate deposits and calcified algae are found in the

photic zone of all marine habitats from polar to tropical seas

(Nelson 2009) In the Phaeophyceae calcification is most

notable in Padina though a few other brown algae also cal-

cify The calcifying Chlorophyte algae are mostly tropical

and contain genera such as Acetabularia Neomeris Avrainvil-

lea and most importantly in terms of its contribution Hali-

meda Many red algae are calcifying both in tropical and

cold waters but calcification is best known in the Coralli-

nales with both geniculate and nongeniculate or crustose

forms Free-living nongeniculate corallines are known as rho-

doliths and form extensive beds which are harvested in

Europe and elsewhere (eg Brazil) In most cases the calcium

carbonate is found as the mineral aragonite either deposited

at the cell surface (eg Padina) or in intercellular spaces

(eg Halimeda) Calcium carbonate can also be deposited as

calcite which has a different crystal structure to aragonite

making it more stable and less prone to dissolution in sea-

water especially under the lowered carbonate concentrations

likely to be found with increasing ocean acidification in the

future Calcite is found in external crusts on Chaetomorpha

and within the cell walls of coralline genera such as Litho-

phyllum and Lithothamnion (Lobban and Harrison 1994)

Many calcifying algae also grow epiphytically on seagrass

leaves as well as on other marine organisms including

bivalves and molluscs Indeed seagrass photosynthesis can

promote calcification rates by other organisms such as Hali-

meda growing in seagrass beds (Semesi et al 2009)

Although many of the algae that calcify are slow growing

the calcium carbonate (aragonite and especially calcite) can

persist in the marine environment long after the living cells

have decayed Iconic calcium carbonate deposits such as the

White Cliffs of Dover are the remains of marine calcifying

microalgae deposited over geological time The rhodolith

beds in France and Brazil are harvested to the rate of

500 Gg yr21 (Briand 1991) and up to 120 Gg yr21 (Riul et al

2008) respectively for industrial processes including agricul-

ture water purification mineralization and the manufacture

of cosmetics (Grall and Hall-Spencer 2003) Carbonate depo-

sition (accumulation) in coastal waters (including coral reefs)

globally is in the order of 12 Pg CaCO3 yr21 (017 Pg C yr21)

with approximately the same accumulated in the pelagic

ocean though production rates in the open ocean are closer

to 11 Pg C yr21 (Iglesias-Rodriguez et al 2002) Decomposed

Halimeda tissues are important sediment elements in tropical

Hill et al Can macroalgae contribute to blue carbon

8

regions (Table 1) and contribute the major part of the cal-

careous sediment found in the sandy beaches of many tropi-

cal shores Halimeda bioherms alone have been estimated to

contribute 400 Tg CaCO3 yr21 to CaCO3 accumulation (Hillis

1997) Rhodolith forming species can produce in the region

of 60ndash1000 g CaCO3 m22 yr21 with CaCO3 deposits off Bra-

zilrsquos coast alone of 2 Pg (Riul et al 2008 Nelson 2009)

Importantly carbonates deposited by oceanic organisms

have not previously been included in blue carbon budgets

This is because the calcification process (Eq 1) results in the

release of 1 CO2 for every CaCO3 formed

2 HCO23 1Ca21 CaCO31CO21H2O (1)

However the CO2 produced in this way can be rapidly

utilised in photosynthesis and even if it is not (during calcifi-

cation in the dark for instance) there is still the net conver-

sion of one soluble HCO23 into one insoluble carbonate

(ie calcification still results in net drawdown of carbon in

the recalcitrant carbonate minerals aragonite or calcite)

Given the significant contribution of macroalgal calcifica-

tion to the global C budget and the persistence of CaCO3 in

sediments we would argue that calcification should be con-

sidered in any calculations of blue carbon into the future If

included this would constitute a further 034 Pg C yr21

sequestered globally

Macroalgae as carbon donors

So far we have established that most macroalgal species

have limited capacity to act as long-term carbon sinks in

their own right (Table 2) largely due to their inability to

accumulate below-ground stores of carbon relative to other

vegetated coastal habitats such as seagrasses saltmarshes

and mangroves However even though macroalgae do not

develop significant carbon deposits themselves there still

exists the possibility that they could make significant contri-

butions to global carbon sequestration by acting as ldquocarbon

donorsrdquo In this section we explore this possibility

What is a ldquocarbon donorrdquo Here we define a carbon donor

as an autotroph that ldquodonatesrdquo carbon to another ldquoreceiverrdquo

habitat that ultimately buries that carbon Therefore carbon

donors make indirect contributions to carbon sequestration

Such movement of carbon from one system to another is

referred to as ldquoleakagerdquo (or ldquospilloverrdquo) A well-recognised

example of leakage can be seen in seagrass ecosystems Sea-

grasses have a high particle-trapping capacity (Agawin and

Duarte 2002 Gruber and Kemp 2010) and due to their

occurrence at the interface between land and sea they cap-

ture large amounts of terrestrial carbon that runs off the

land following rainfall events (Kennedy et al 2010 Macrea-

die et al 2014) This externally derived carbon that leaks

into a receiver habitat is termed ldquoallochthonousrdquo carbon In

seagrasses allochthonous carbon can contribute as much as

half the total organic carbon that is sequestered in a meadow

(Kennedy et al 2010)

From a carbon accounting perspective leakage of carbon

is a complex issue Can habitats take credit for carbon that

they didnrsquot produce What happens if the carbon was

already credited to another system (double-counting) How

can the origin of carbon be determined These questions are

at the forefront of many terrestrial carbon-offset programs

(eg REDD) but have received comparatively little attention

in the aquatic fields The matter of carbon accounting of

leakage will however become increasingly important with

the rising prominence of blue carbon but is beyond the

scope of this review We recommend Murray et al (2007) for

more information on leakage

For a system to be a significant carbon donor there are

three requirements (1) high rates of biomass production (2)

effective transfer of biomass to receiver habitats and (3) the

donor carbon must undergo efficient burial of allochthonous

biomass within receiver habitats such that it evades micro-

bial attack (the latter is a function of several factors includ-

ing the intrinsic stability of the carbon physical

mechanisms of protection and environmental conditions

that dictate microbial activity) All three requirements are

necessary none are redundant or substitutable The first

requirement has already been discussed earlier in this article

and can be summarised as follows macroalgae have excep-

tionally high biomass production their global extent (2ndash68

million km2) and primary production (019ndash064 Pg C yr21)

exceeds that of all the vegetated coastal habitats (seagrass

beds saltmarshes mangroves) combined (Duarte et al

2013) In the following section we will discuss requirements

2 and 3 which concern the export and fate of this biomass

production

Export and fate of macroalgal biomass

to receiver habitats

Most macroalgal species spend their early life history

attached to benthic (hard) substrata (Leurouning 1990) but then

become dislodged or fragmented and can undergo a period

of transport in surface or bottom waters by wind and water

movement (potentially as rafts that travel significant distan-

ces) until eventually sinking disintegrating or becoming

cast upon land (Thiel 2003 Thiel and Gutow 2005 Macrea-

die et al 2011) Detachment of macroalgal tissue can arise

from natural senescence (Ang 1985) dislodgement by herbi-

vores (Kingsford 1992 Tegner et al 1995) and through

hydrodynamic forces such as waves and storms (Duggins

et al 2003) The supply quality persistence and transport

(trajectory and duration) of macroalgal rafts are all influ-

enced by climate (Macreadie et al 2011) particularly tem-

perature (Graiff et al 2013) Thus whilst there is temporal

variation in the extent of macroalgal rafts related to these

processes there is continuous export of macroalgal biomass

throughout the year whereas saltmarsh and seagrass detrital

Hill et al Can macroalgae contribute to blue carbon

9

export tends to be seasonal (Josselyn and Mathieson 1980)

Furthermore acknowledging spatial variation in the export

of macroalgal and vascular plant biomass macroalgae are

often more significant contributors to surf-zone and beach

wrack than seagrasses (Josselyn and Mathieson 1980 Gomez

et al 2013 Baring et al 2014 Ruiz-Delgado et al 2014)

From genetic and tracking studies we know that exported

macroalgal biomass can be transported long distances (Thiel

and Haye 2006 Fraser et al 2009 2010 2011 Nikula et al

2010) but there is limited information on what happens to

carbon bound within macroalgal biomass once rafts or frag-

ments sink and disintegratemdashie the point at which carbon

bound within macroalgal biomass is broken down into dis-

solved and particulate organic carbon Wada et al (2007)

suggested that macroalgae could release 20ndash40 of their pro-

ductivity as dissolved organic matter (DOM) Much of the

macroalgal DOM is likely to be microbially degraded but

estimates of the refractory component of this DOM will be

important for understanding how much could be donated to

other habitats UV is known to degrade DOM this means

that if this matter can be deposited in regions away from

light such as the deep ocean the breakdown will be further

diminished

There is some evidence to suggest that macroalgal carbon

is donated to other receiver habitats that have long-term

sequestration capacity including the deep sea (Wada et al

2008 Dierssen et al 2009) and other vegetated coastal habi-

tats such as mangrove forests seagrass beds and salt

marshes (Hyndes et al 2012 Macreadie et al 2012) In tropi-

cal estuaries and bays it is estimated that about half of the

macroalgal biomass produced is consumed by herbivores and

the other half is exported to other habitats whereas in the

temperate open coast most of the biomass is decomposed by

detritivores with a lesser amount being exported and only

small fractions being consumed or accumulated as detritus

(Hyndes et al 2013) The fate of macroalgal biomass in tem-

perate estuaries and fjords is largely unknown (Hyndes et al

2013) Most export of macroalgal biomass occurs via advec-

tion but there are also complex biotic pathways that trans-

port macroalgal biomass into receiver habitats such as via

ingestion and concomitant faecal deposition of carbon

within receiver habitats by fish which can contribute to car-

bon sequestration by fertilising receiver habitats and thereby

increasing their productivity and sequestration capacity

(Valiela 1995 Hyndes et al 2013) Breakdown of macroalgae

has been shown to be mostly mediated by microbial proc-

esses (Rieper-Kirchner 1990) however protozoans and meio-

fauna also contribute to the decomposition of macroalgal

tissues as well as enhance microbial degradation Microbial

breakdown rate is also dependent upon the sediment com-

position and oxic status of the water Sassi et al (1988)

found that macroalgal decomposition rates over 25 d under

aerobic vs anaerobic conditions were 35 and 24 respec-

tively Therefore if the macroalgal detritus can be advected

to a rapidly sedimenting region where it can be incorporated

into an anaerobic sediment this will slow the microbial

breakdown and maintain the carbon within the sediment

longer More research is needed to understand how long this

carbon actually remains within anaerobic sediment

All macroalgal carbon that enters the sedimentary carbon

pool will eventually be broken down (oxidised and reminer-

alized) by microbes and converted to inorganic forms and

potentially returned to the atmosphere The rate and effi-

ciency of this remineralization process can dictate whether

macroalgal carbon remains bound within sediments for

months or millennia Macroalgal carbon entering the sedi-

mentary pool has three possible fates (1) particulate and dis-

solved organic carbon that is recalcitrant to microbial

degradation is likely to remain stored within the sediment

for prolonged periods while labile carbon will be recycled by

heterotrophic bacteria and is either (2) assimilated into

microbial biomass or (3) respired as CO2 back to the water

column and possibly the atmosphere The proportion of

nonrespired carbon represents the amount of macroalgal car-

bon that is sequestered

It should be recognised that macroalgae lack the struc-

tural polysaccharide complexity of higher plants and conse-

quently their decomposition rates are faster (Sassi et al

1988) To better understand the degradation pathways of

macroalgal plant material within aquatic sediments

researchers have used several techniques Analyses of ele-

mental composition and stable isotope signatures are rou-

tinely used to ldquofingerprintrdquo carbon and determine its origin

although there is difficultly in separating microalgal and

macroalgal organic carbon signatures (Hardison et al 2011)

Furthermore isotopic signatures may also be variable in

space and time during the decomposition process (Fenton

and Ritz 1988) Similarly a problem with identifying sources

of organic carbon based on carbohydrate composition is that

many groups of organisms contain the same carbohydrates

(Vichkovitten and Holmer 2004) Fatty acid signatures have

proven to offer better resolution of the different plant contri-

butions to organic matter (Hardison et al 2013) although

the level of complexity using this technique is much higher

(Graeve et al 2002) Manipulative approaches using isotopic

tracer studies (Hee et al 2001 Hardison et al 2010 2011

Hyndes et al 2012) and radiolabelling (Chidthaisong et al

1999) have proved to be robust for studying the incorpora-

tion of macroalgal carbon into sediments

Reliable data on the fate of decomposed macroalgal

carbon within sediments (eg macroalgal carbon that is

ldquolostrdquo during litter bag mass loss experiments) is scarce

Hardison et al (2010) traced carbon from senescing macroal-

gae (Gracilaria spp) that were pre-labeled with the 13C stable

isotope and found that 2ndash9 of macroalgal carbon was

incorporated into the sediment This percentage of macroal-

gal carbon uptake by sediments is relatively high suggesting

efficient burial however the fate of this buried carbon was

Hill et al Can macroalgae contribute to blue carbon

10

only monitored for 2 weeks so it is not known whether this

carbon stock was sequestered long-term Other studies sug-

gest that macroalgal carbon is not sequestered long-term For

example Garcia-Robledo et al (2008) found that macroalgal

detritus (tubular and planar Ulva spp) that entered sedimen-

tary organic carbon pools vanished within days after its ini-

tial appearance indicating that carbon from such simple and

ephemeral macroalgae is not retained for durations that

would make them an important component of the long-

term carbon pool within a receiver habitat However given

the diversity in the cell walls and carbon chemistry of mac-

roalgae it is difficult to make conclusions on likely persist-

ence of sequestered macroalgae based on only a handful of

studies

Kristensen (1994) compared the decomposition rate of six

different plant materials (two macroalgae two seagrasses

and two tree leaves) using stepwise thermogravimetry and

found that macroalgae (Fucus vesiculosus and Ulva lactuca)

lost 40ndash44 of their carbon within 70 d whereas seagrasses

(Zostera marina and Ruppia maritima) lost 29ndash55 and tree

leaves (Fagus sylvatica and Rhizophora apiculata) lost only 0ndash

8 Similarly Josselyn and Mathieson (1980) found that

macroalgae (Ascophyllum nodosum and Fucus vesiculosus)

decomposed 3ndash10 times faster than a saltmarsh plant (Spar-

tina alterniflora) and seagrass (Zostera marina) Litter bag stud-

ies have reported a lack of change in sediment carbon

following decomposition of buried macroalgae suggesting

that the organic carbon bound within macroalgal structural

material (eg carbohydrates) is highly labile and rapidly

decomposed by microbes (Vichkovitten and Holmer 2004)

Despite this general pattern of high degradability of macroal-

gae compared with aquatic angiosperms (Trevathan-Tackett

et al in press) there is a high degree of diversity in the

structural complexity of macroalgae particularly in cell-wall

structure and carbon chemistry resulting in high variability

in decay rate estimates within the literature (Rice and Han-

son 1984 Twilley et al 1986 Kristensen 1990 Wada et al

2008 Trevathan-Tackett et al in press)

Nedzarek and Rakusa-Suszczewski (2004) examined the

decomposition of 10 Antarctic macroalgal species finding

they released 80 of the nutrients with the first 3 d of a 69

d decomposition experiment these rates occurred at polar

temperatures (48C) so it would be assumed that tropical

decomposition would be more rapid Similar results were

found with North Sea macroalgae where 50ndash80 of the tis-

sue biomass was lost within 14 d at 188C (Rieper-Kirchner

1990) which included the brown leathery kelp Laminaria

saccharina

Factors influencing the future carbon storage anddonor ability of macroalgae

This review presents a static view on the current state of

carbon cycling sequestration and donor capacity of macroal-

gae with an emphasis on Australian coastal systems In real-

ity the distribution biomass and productivity of these

macroalgae are vulnerable to change due to anthropogenic

activities and as such the dynamic nature of these macroal-

gal systems should be taken into consideration Factors such

as climate change (Duarte et al 2013) and urbanisation (Air-

oldi and Beck 2007 Airoldi et al 2008) can greatly alter the

distribution abundance and productivity of these systems

although the rate of change in global macroalgae population

size remains unknown

Climate change can greatly influence the survival photo-

synthetic capacity growth and competitive interactions of

macroalgae in coastal habitats (Wernberg et al 2011b)

Ocean warming on both the east and west coasts of Australia

have caused pole-ward movement of macroalgal species over

the past five decades (Wernberg et al 2011a) Potentially

hundreds of species are expected to be driven beyond the

edge of the Australian continent as warming continues driv-

ing not only local but global extinctions as 62 of macro-

algal species found in southern Australia are endemic to the

region (Phillips 2001) On the east coast of Australia there

has been a southern retreat of three habitat-forming macro-

algal species (Ecklonia radiata Phyllospora comosa and Durvil-

laea potatorum Millar 2007) and in eastern Tasmania the

once common Macrocystis pyrifera has almost completely dis-

appeared with ocean warming (Edyvane 2003 Johnson et al

2011)

In addition to rising temperatures climate change is

expected to influence macroalgal distribution and productiv-

ity through ocean acidification emergence of marine dis-

eases and shifts in the distribution of consumers In

terrestrial ecosystems there have been climate-driven

increases in global net primary production due to the easing

of critical climatic constraints such as increasing solar radia-

tion from reduced cloud cover (Nemani et al 2003) In the

oceans while increased CO2 dissolution is reducing pH and

disrupting carbonate chemistry this inorganic carbon is a

building block for photosynthesis The predicted changes in

CO2 in the atmosphere over the next 100 yr will translate to

a 25- to 3-fold increase in dissolved CO2 in seawater

although the subsequent drop in pH will cause shifts in the

equilibria between inorganic carbon forms HCO23 concentra-

tions will only rise by 10 and total Ci available for pho-

tosynthesis (HCO23 1 CO2) will thus rise bylt15 However

if CO2 availability is a constraint to the rate of photosynthe-

sis could the more abundant CO2 result in faster macroalgal

growth Most macroalgae have the capacity to use the

HCO23 ion that is dominant in seawater and given that the

HCO23 concentrations will not change much in future an

impact on photosynthesis is unlikely Furthermore most

macroalgae and seagrasses (Beer et al 2014) possess carbon

concentrating mechanisms (CCMs Giordano et al 2005)

which actively take up inorganic carbon (as HCO23 andor

CO2) and thereby accumulate CO2 at the active site of the

Hill et al Can macroalgae contribute to blue carbon

11

CO2-fixing enzyme Rubisco This effectively saturates

Rubisco for CO2 and limits any increased productivity of

macroalgae from elevated atmospheric CO2 and ocean acidi-

fication There are few exceptions mostly subtidal rhodo-

phytes to the rule that macroalgae possess CCMs so

increased CO2 per se is unlikely to increase CO2 drawdown

by coastal primary producers However there are suggestions

that higher CO2 may increase carbon allocation to seagrass

rhizomes under high light (ie in shallow water) and

thereby enhance burial rates (Jiang et al 2010)

Anthropogenic activities such as climate-change-

associated rising sea temperatures are expected to increase

the occurrence of macroalgal diseases through an increased

virulence of opportunistic pathogens as well as reduced

resistance to disease in thermally stressed hosts (Egan et al

2013) For example in the chemically defended macroalgae

Delisea pulchra bacterial bleaching of the thallus occurs in

response to elevated temperatures due to reduced antibacte-

rial chemical defences (Campbell et al 2011 Case et al

2011) Such diseases therefore have the capacity to reduce

macroalgal abundance either through increased consump-

tion (due to reduced herbivory defence) or through direct

host mortality (Goecke et al 2010)

With the delivery of warmer water further south the East

Australian Current not only contracts the range of many

macroalgal species but also extends the range of urchin con-

sumers Urchin barrens are now extensive throughout south-

eastern Australia and are continuing to expand at the detri-

ment of macroalgal populations (Johnson et al 2011) Such

altered ecological interactions with herbivores from this tro-

picalisation of high latitudes are therefore causing macroal-

gal populations to decline in Tasmania

While climate change will have detrimental effects on

macroalgal populations especially in temperate Australia

tropical regions may experience increased macroalgal abun-

dance following thermal pulses on coral-dominated reefs If

temperatures on coral reefs exceed summer averages by as

little as 1ndash28C mass coral bleaching events can occur which

can lead to coral mortality (Hoegh-Guldberg et al 2007)

Phase shifts toward macroalgal-dominated reefs can follow

especially if herbivory has been reduced by overfishing

(McManus et al 2000 Bruno et al 2009 Hughes et al

2010) However not all tropical macroalgal species will bene-

fit from climate change with species such as Chnoospora

implexa expected to decrease in abundance (Bender et al

2013)

When considering the donor capacity of macroalgae algal

rafts have the potential to deliver dislodged macroalgae to

receiver habitats that can bury the carbon and thus enhance

the carbon sink (see above) However changes in climate

will affect raft supply and persistence (Macreadie et al

2011) Increased storm intensities (IPCC 2007) will promote

substratum detachment andor fragmentation and hence

increase the abundance of algal fragments and rafts and

may also increase burial of macroalgal material (Macreadie

et al 2011) Elevated temperatures however may counter

this process by reducing raft longevity due to an increase in

herbivore metabolism and consumption (Macreadie et al

2011) In addition changes in ocean surface currents may

affect advection routes and potential endpoints of deposition

into more or less favorable receiver environments for

sequestration

Given the dynamic nature of macroalgal populations and

changes in abundance and productivity especially from

human activities the potential for carbon storage and export

may be highly variable In considering the role macroalgae

may play in climate change mitigation the factors detailed

above should be taken into account as they are likely to

greatly influence the contribution of macroalgae to blue car-

bon storage

Conclusions and research priorities

Although macroalgal communities in Australia and

around the world produce massive quantities of plant bio-

mass with high organic carbon content the presence of a

hard rocky substrate precludes the potential for long-term

storage of carbon within the macroalgal habitat In isolation

we therefore conclude that macroalgae do not contribute to

blue carbon

However a considerable proportion of macroalgal bio-

mass becomes dislodged from the benthos and is exported

beyond macroalgal habitat boundaries This donor carbon

may be received by habitats with long-term sequestration

capacity such as seagrass beds saltmarshes mangroves and

continental shelf regions Within Australia and globally

geographic differences in macroalgal biomass community

composition and productivity will influence the blue carbon

donor capacity of macroalgae with the greatest contribu-

tions likely to be in the temperate (and possibly polar)

regions In addition to a high rate of biomass production to

be a viable carbon donor macroalgae must be transferred to

a receiver habitat undergo burial and avoid microbial remi-

neralization The fate of detached macroalgal biomass is not

entirely clear and whilst limited data on the composition of

macroalgal biomass indicates that macroalgal carbon is

highly labile recent research has highlighted the potentially

significant role of refractory taxon-specific compounds (car-

bonates long-chain lipids alginates xylans and sulphated

polysaccharides) from macroalgae in contributing to long-

term blue carbon stores (Trevathan-Tackett et al in press)

We therefore conclude that macroalgae have the potential

to make ecologically meaningful contributions toward global

blue carbon sequestration as significant carbon donors but

further research is needed to quantify these contributions

Data on the degradability of macroalgal plant material is

limited to only a handful of taxa so there is considerable

need for additional testing on other taxa The capacity for

Hill et al Can macroalgae contribute to blue carbon

12

any incorporation of organic material from macroalgae into

long-term carbon stores is only possible if the material can

avoid decomposition by microbes potentially by entering a

storage habitat that is a rapidly accreting zone Research

therefore needs to focus on determining the burial rates of

macroalgal tissue at receiver sites which of these sites are

the greatest sink of macroalgal fragments understanding the

environmental conditions that maximise the burial process

and assessing whether burial is fast enough to limit micro-

bial remineralization of the organic macroalgal material

This will also need to include further research identifying

interspecies variation in carbon donor capacity due to rate of

lability and rate of transport to accreting zones In existing

blue carbon habitats methods for identifying macroalgal car-

bon in the storage zone also need to be developed to gauge

historical contributions of macroalgae into these zones

Once these unknowns are addressed the potential for mac-

roalgae to contribute to blue carbon as a carbon donor will

become less ambiguous Focusing future research on these

key areas will provide evidence as to whether macroalgae

should be included under the blue carbon umbrella

Macroalgal aquaculture and the harvesting of natural pop-

ulations are growing industries worldwide and are actions

that can greatly increase the carbon sequestration capacity

afforded by macroalgae (Chung et al 2011) Furthermore

the production of macroalgal biochar (a process involving

the pyrolysis of biomass) for addition to soil may represent

a viable long-term CO2 sink although research in this field

is in its infancy (Lehmann et al 2006 Bird et al 2011)

Given that macroalgal populations have the highest abun-

dance biomass and productivity of all coastal habitats they

not only store an immense amount of carbon in their living

biomass but they also have an outstanding potential to act

as significant carbon donors However macroalgae are vul-

nerable to a range of anthropogenic impacts so it is impor-

tant to protect these ecosystems for their climate-change-

mitigation potential as well as their ecosystem services

References

Agawin N S R and G M Duarte 2002 Evidence of direct

particle trapping by a tropical seagrass meadow Estuaries

25 1205ndash1209 doi101007BF02692217

Airoldi L D Balata and M W Beck 2008 The Gray Zone

Relationships between habitat loss and marine diversity

and their applications in conservation J Exp Mar Biol

Ecol 366 8ndash15 doi101016jjembe200807034

Airoldi L and M W Beck 2007 Loss status and trends for

coastal marine habitats of Europe Oceanogr Mar Biol

Ann Rev 45 345ndash405

Ang P O J 1985 Regeneration studies of Sargassum

siliquosum J ag and S paniculatum J Ag (Phaeophyta

Sargassaceae) Botanical Marina 28 231ndash235 doi101515

botm1985286231

Bala G 2013 Digesting 400 ppm for global mean CO2

concentration Curr Sci 104 1471ndash1472

Baring R J P G Fairweather and R E Lester 2014

Storm versus calm Variation in fauna associated with

drifting macrophytes in sandy beach surf zones J Exp

Mar Biol Ecol 461 397ndash406 doi101016jjembe2014

09011

Beer S M Bjeuroork and J Beardall 2014 Photosynthesis in

the marine environment Wiley

Behrenfeld M J E Mara~non D A Siegel and S B Hooker

2002 Photoacclimation and nutrient-based model of

light-saturated photosynthesis for quantifying oceanic pri-

mary production Mar Ecol Prog Ser 228 103ndash117 doi

103354meps228103

Bender D G Diaz-Pulido and S Dove 2013 The impact of

CO2 emission scenarios and nutrient enrichment on a

common coral reef macroalga is modified by temporal

effects J Phycol 50 203ndash215 doi101111jpy12153

Bird M I C M Wurster P H de Paula Silva A M Bass

and D de Nys 2011 Algal biocharmdashproduction and

properties Bioresour Technol 102 1886ndash1891 doi

101111j1757-1707201101109x

Briand X 1991 Seaweed harvesting in Europe p 293ndash308

In M D Guiry and G Blunden [eds] Seaweed resources

in Europe Uses and potential Wiley

Bruno J F H Sweatman W F Precht E R Selig and V

G W Schutte 2009 Assessing evidence of phase shifts

from coral to macroalgal dominance on coral reefs

Ecology 90 1478ndash1484 doi10189008-17811

Cacador I A L Coasta and C Vale 2004 Carbon storage

in Tagus salt marsh sediments Water Air Soil Pollut Focus

4 701ndash714 doi101023BWAFO000002838884544ce

Campbell A H T Harder S Nielsen S Kjelleberg and P D

Steinberg 2011 Climate change and disease Bleaching of

a chemically defended seaweed Glob Chang Biol 17

2958ndash2970 doi101111j1365-2486201102456x

Case R J S R Longford A H Campbell A Low N Tujula

P D Steinberg and S Kjelleberg 2011 Temperature

induced bacterial virulence and bleaching disease in a

chemically defended marine macroalga Environ Microbiol

13 529ndash537 doi101111j1462-2920201002356x

Che Hasan R D Ierodiaconou and J Monk 2012

Evaluation of four supervised learning methods for Benthic

habitat mapping using backscatter from multi-beam sonar

Remote Sens 4 3427ndash3443 doi103390rs4113427

Cheshire A C and N D Hallam 1988 Biomass and

density of native stands of Durvillaea potatorum (southern

bull-kelp) in south eastern Australia Mar Ecol Prog Ser

48 277ndash283 doi103354meps048277

Cheshire A C G Westphalen A Wenden L J Scriven

and B C Rowland 1996 Photosynthesis and respiration

of phaeophycean-dominated macroalgal communities in

summer and winter Aquat Bot 55 159ndash170 doi

101016S0304-3770(96)01071-6

Hill et al Can macroalgae contribute to blue carbon

13

regions (Table 1) and contribute the major part of the cal-

careous sediment found in the sandy beaches of many tropi-

cal shores Halimeda bioherms alone have been estimated to

contribute 400 Tg CaCO3 yr21 to CaCO3 accumulation (Hillis

1997) Rhodolith forming species can produce in the region

of 60ndash1000 g CaCO3 m22 yr21 with CaCO3 deposits off Bra-

zilrsquos coast alone of 2 Pg (Riul et al 2008 Nelson 2009)

Importantly carbonates deposited by oceanic organisms

have not previously been included in blue carbon budgets

This is because the calcification process (Eq 1) results in the

release of 1 CO2 for every CaCO3 formed

2 HCO23 1Ca21 CaCO31CO21H2O (1)

However the CO2 produced in this way can be rapidly

utilised in photosynthesis and even if it is not (during calcifi-

cation in the dark for instance) there is still the net conver-

sion of one soluble HCO23 into one insoluble carbonate

(ie calcification still results in net drawdown of carbon in

the recalcitrant carbonate minerals aragonite or calcite)

Given the significant contribution of macroalgal calcifica-

tion to the global C budget and the persistence of CaCO3 in

sediments we would argue that calcification should be con-

sidered in any calculations of blue carbon into the future If

included this would constitute a further 034 Pg C yr21

sequestered globally

Macroalgae as carbon donors

So far we have established that most macroalgal species

have limited capacity to act as long-term carbon sinks in

their own right (Table 2) largely due to their inability to

accumulate below-ground stores of carbon relative to other

vegetated coastal habitats such as seagrasses saltmarshes

and mangroves However even though macroalgae do not

develop significant carbon deposits themselves there still

exists the possibility that they could make significant contri-

butions to global carbon sequestration by acting as ldquocarbon

donorsrdquo In this section we explore this possibility

What is a ldquocarbon donorrdquo Here we define a carbon donor

as an autotroph that ldquodonatesrdquo carbon to another ldquoreceiverrdquo

habitat that ultimately buries that carbon Therefore carbon

donors make indirect contributions to carbon sequestration

Such movement of carbon from one system to another is

referred to as ldquoleakagerdquo (or ldquospilloverrdquo) A well-recognised

example of leakage can be seen in seagrass ecosystems Sea-

grasses have a high particle-trapping capacity (Agawin and

Duarte 2002 Gruber and Kemp 2010) and due to their

occurrence at the interface between land and sea they cap-

ture large amounts of terrestrial carbon that runs off the

land following rainfall events (Kennedy et al 2010 Macrea-

die et al 2014) This externally derived carbon that leaks

into a receiver habitat is termed ldquoallochthonousrdquo carbon In

seagrasses allochthonous carbon can contribute as much as

half the total organic carbon that is sequestered in a meadow

(Kennedy et al 2010)

From a carbon accounting perspective leakage of carbon

is a complex issue Can habitats take credit for carbon that

they didnrsquot produce What happens if the carbon was

already credited to another system (double-counting) How

can the origin of carbon be determined These questions are

at the forefront of many terrestrial carbon-offset programs

(eg REDD) but have received comparatively little attention

in the aquatic fields The matter of carbon accounting of

leakage will however become increasingly important with

the rising prominence of blue carbon but is beyond the

scope of this review We recommend Murray et al (2007) for

more information on leakage

For a system to be a significant carbon donor there are

three requirements (1) high rates of biomass production (2)

effective transfer of biomass to receiver habitats and (3) the

donor carbon must undergo efficient burial of allochthonous

biomass within receiver habitats such that it evades micro-

bial attack (the latter is a function of several factors includ-

ing the intrinsic stability of the carbon physical

mechanisms of protection and environmental conditions

that dictate microbial activity) All three requirements are

necessary none are redundant or substitutable The first

requirement has already been discussed earlier in this article

and can be summarised as follows macroalgae have excep-

tionally high biomass production their global extent (2ndash68

million km2) and primary production (019ndash064 Pg C yr21)

exceeds that of all the vegetated coastal habitats (seagrass

beds saltmarshes mangroves) combined (Duarte et al

2013) In the following section we will discuss requirements

2 and 3 which concern the export and fate of this biomass

production

Export and fate of macroalgal biomass

to receiver habitats

Most macroalgal species spend their early life history

attached to benthic (hard) substrata (Leurouning 1990) but then

become dislodged or fragmented and can undergo a period

of transport in surface or bottom waters by wind and water

movement (potentially as rafts that travel significant distan-

ces) until eventually sinking disintegrating or becoming

cast upon land (Thiel 2003 Thiel and Gutow 2005 Macrea-

die et al 2011) Detachment of macroalgal tissue can arise

from natural senescence (Ang 1985) dislodgement by herbi-

vores (Kingsford 1992 Tegner et al 1995) and through

hydrodynamic forces such as waves and storms (Duggins

et al 2003) The supply quality persistence and transport

(trajectory and duration) of macroalgal rafts are all influ-

enced by climate (Macreadie et al 2011) particularly tem-

perature (Graiff et al 2013) Thus whilst there is temporal

variation in the extent of macroalgal rafts related to these

processes there is continuous export of macroalgal biomass

throughout the year whereas saltmarsh and seagrass detrital

Hill et al Can macroalgae contribute to blue carbon

9

export tends to be seasonal (Josselyn and Mathieson 1980)

Furthermore acknowledging spatial variation in the export

of macroalgal and vascular plant biomass macroalgae are

often more significant contributors to surf-zone and beach

wrack than seagrasses (Josselyn and Mathieson 1980 Gomez

et al 2013 Baring et al 2014 Ruiz-Delgado et al 2014)

From genetic and tracking studies we know that exported

macroalgal biomass can be transported long distances (Thiel

and Haye 2006 Fraser et al 2009 2010 2011 Nikula et al

2010) but there is limited information on what happens to

carbon bound within macroalgal biomass once rafts or frag-

ments sink and disintegratemdashie the point at which carbon

bound within macroalgal biomass is broken down into dis-

solved and particulate organic carbon Wada et al (2007)

suggested that macroalgae could release 20ndash40 of their pro-

ductivity as dissolved organic matter (DOM) Much of the

macroalgal DOM is likely to be microbially degraded but

estimates of the refractory component of this DOM will be

important for understanding how much could be donated to

other habitats UV is known to degrade DOM this means

that if this matter can be deposited in regions away from

light such as the deep ocean the breakdown will be further

diminished

There is some evidence to suggest that macroalgal carbon

is donated to other receiver habitats that have long-term

sequestration capacity including the deep sea (Wada et al

2008 Dierssen et al 2009) and other vegetated coastal habi-

tats such as mangrove forests seagrass beds and salt

marshes (Hyndes et al 2012 Macreadie et al 2012) In tropi-

cal estuaries and bays it is estimated that about half of the

macroalgal biomass produced is consumed by herbivores and

the other half is exported to other habitats whereas in the

temperate open coast most of the biomass is decomposed by

detritivores with a lesser amount being exported and only

small fractions being consumed or accumulated as detritus

(Hyndes et al 2013) The fate of macroalgal biomass in tem-

perate estuaries and fjords is largely unknown (Hyndes et al

2013) Most export of macroalgal biomass occurs via advec-

tion but there are also complex biotic pathways that trans-

port macroalgal biomass into receiver habitats such as via

ingestion and concomitant faecal deposition of carbon

within receiver habitats by fish which can contribute to car-

bon sequestration by fertilising receiver habitats and thereby

increasing their productivity and sequestration capacity

(Valiela 1995 Hyndes et al 2013) Breakdown of macroalgae

has been shown to be mostly mediated by microbial proc-

esses (Rieper-Kirchner 1990) however protozoans and meio-

fauna also contribute to the decomposition of macroalgal

tissues as well as enhance microbial degradation Microbial

breakdown rate is also dependent upon the sediment com-

position and oxic status of the water Sassi et al (1988)

found that macroalgal decomposition rates over 25 d under

aerobic vs anaerobic conditions were 35 and 24 respec-

tively Therefore if the macroalgal detritus can be advected

to a rapidly sedimenting region where it can be incorporated

into an anaerobic sediment this will slow the microbial

breakdown and maintain the carbon within the sediment

longer More research is needed to understand how long this

carbon actually remains within anaerobic sediment

All macroalgal carbon that enters the sedimentary carbon

pool will eventually be broken down (oxidised and reminer-

alized) by microbes and converted to inorganic forms and

potentially returned to the atmosphere The rate and effi-

ciency of this remineralization process can dictate whether

macroalgal carbon remains bound within sediments for

months or millennia Macroalgal carbon entering the sedi-

mentary pool has three possible fates (1) particulate and dis-

solved organic carbon that is recalcitrant to microbial

degradation is likely to remain stored within the sediment

for prolonged periods while labile carbon will be recycled by

heterotrophic bacteria and is either (2) assimilated into

microbial biomass or (3) respired as CO2 back to the water

column and possibly the atmosphere The proportion of

nonrespired carbon represents the amount of macroalgal car-

bon that is sequestered

It should be recognised that macroalgae lack the struc-

tural polysaccharide complexity of higher plants and conse-

quently their decomposition rates are faster (Sassi et al

1988) To better understand the degradation pathways of

macroalgal plant material within aquatic sediments

researchers have used several techniques Analyses of ele-

mental composition and stable isotope signatures are rou-

tinely used to ldquofingerprintrdquo carbon and determine its origin

although there is difficultly in separating microalgal and

macroalgal organic carbon signatures (Hardison et al 2011)

Furthermore isotopic signatures may also be variable in

space and time during the decomposition process (Fenton

and Ritz 1988) Similarly a problem with identifying sources

of organic carbon based on carbohydrate composition is that

many groups of organisms contain the same carbohydrates

(Vichkovitten and Holmer 2004) Fatty acid signatures have

proven to offer better resolution of the different plant contri-

butions to organic matter (Hardison et al 2013) although

the level of complexity using this technique is much higher

(Graeve et al 2002) Manipulative approaches using isotopic

tracer studies (Hee et al 2001 Hardison et al 2010 2011

Hyndes et al 2012) and radiolabelling (Chidthaisong et al

1999) have proved to be robust for studying the incorpora-

tion of macroalgal carbon into sediments

Reliable data on the fate of decomposed macroalgal

carbon within sediments (eg macroalgal carbon that is

ldquolostrdquo during litter bag mass loss experiments) is scarce

Hardison et al (2010) traced carbon from senescing macroal-

gae (Gracilaria spp) that were pre-labeled with the 13C stable

isotope and found that 2ndash9 of macroalgal carbon was

incorporated into the sediment This percentage of macroal-

gal carbon uptake by sediments is relatively high suggesting

efficient burial however the fate of this buried carbon was

Hill et al Can macroalgae contribute to blue carbon

10

only monitored for 2 weeks so it is not known whether this

carbon stock was sequestered long-term Other studies sug-

gest that macroalgal carbon is not sequestered long-term For

example Garcia-Robledo et al (2008) found that macroalgal

detritus (tubular and planar Ulva spp) that entered sedimen-

tary organic carbon pools vanished within days after its ini-

tial appearance indicating that carbon from such simple and

ephemeral macroalgae is not retained for durations that

would make them an important component of the long-

term carbon pool within a receiver habitat However given

the diversity in the cell walls and carbon chemistry of mac-

roalgae it is difficult to make conclusions on likely persist-

ence of sequestered macroalgae based on only a handful of

studies

Kristensen (1994) compared the decomposition rate of six

different plant materials (two macroalgae two seagrasses

and two tree leaves) using stepwise thermogravimetry and

found that macroalgae (Fucus vesiculosus and Ulva lactuca)

lost 40ndash44 of their carbon within 70 d whereas seagrasses

(Zostera marina and Ruppia maritima) lost 29ndash55 and tree

leaves (Fagus sylvatica and Rhizophora apiculata) lost only 0ndash

8 Similarly Josselyn and Mathieson (1980) found that

macroalgae (Ascophyllum nodosum and Fucus vesiculosus)

decomposed 3ndash10 times faster than a saltmarsh plant (Spar-

tina alterniflora) and seagrass (Zostera marina) Litter bag stud-

ies have reported a lack of change in sediment carbon

following decomposition of buried macroalgae suggesting

that the organic carbon bound within macroalgal structural

material (eg carbohydrates) is highly labile and rapidly

decomposed by microbes (Vichkovitten and Holmer 2004)

Despite this general pattern of high degradability of macroal-

gae compared with aquatic angiosperms (Trevathan-Tackett

et al in press) there is a high degree of diversity in the

structural complexity of macroalgae particularly in cell-wall

structure and carbon chemistry resulting in high variability

in decay rate estimates within the literature (Rice and Han-

son 1984 Twilley et al 1986 Kristensen 1990 Wada et al

2008 Trevathan-Tackett et al in press)

Nedzarek and Rakusa-Suszczewski (2004) examined the

decomposition of 10 Antarctic macroalgal species finding

they released 80 of the nutrients with the first 3 d of a 69

d decomposition experiment these rates occurred at polar

temperatures (48C) so it would be assumed that tropical

decomposition would be more rapid Similar results were

found with North Sea macroalgae where 50ndash80 of the tis-

sue biomass was lost within 14 d at 188C (Rieper-Kirchner

1990) which included the brown leathery kelp Laminaria

saccharina

Factors influencing the future carbon storage anddonor ability of macroalgae

This review presents a static view on the current state of

carbon cycling sequestration and donor capacity of macroal-

gae with an emphasis on Australian coastal systems In real-

ity the distribution biomass and productivity of these

macroalgae are vulnerable to change due to anthropogenic

activities and as such the dynamic nature of these macroal-

gal systems should be taken into consideration Factors such

as climate change (Duarte et al 2013) and urbanisation (Air-

oldi and Beck 2007 Airoldi et al 2008) can greatly alter the

distribution abundance and productivity of these systems

although the rate of change in global macroalgae population

size remains unknown

Climate change can greatly influence the survival photo-

synthetic capacity growth and competitive interactions of

macroalgae in coastal habitats (Wernberg et al 2011b)

Ocean warming on both the east and west coasts of Australia

have caused pole-ward movement of macroalgal species over

the past five decades (Wernberg et al 2011a) Potentially

hundreds of species are expected to be driven beyond the

edge of the Australian continent as warming continues driv-

ing not only local but global extinctions as 62 of macro-

algal species found in southern Australia are endemic to the

region (Phillips 2001) On the east coast of Australia there

has been a southern retreat of three habitat-forming macro-

algal species (Ecklonia radiata Phyllospora comosa and Durvil-

laea potatorum Millar 2007) and in eastern Tasmania the

once common Macrocystis pyrifera has almost completely dis-

appeared with ocean warming (Edyvane 2003 Johnson et al

2011)

In addition to rising temperatures climate change is

expected to influence macroalgal distribution and productiv-

ity through ocean acidification emergence of marine dis-

eases and shifts in the distribution of consumers In

terrestrial ecosystems there have been climate-driven

increases in global net primary production due to the easing

of critical climatic constraints such as increasing solar radia-

tion from reduced cloud cover (Nemani et al 2003) In the

oceans while increased CO2 dissolution is reducing pH and

disrupting carbonate chemistry this inorganic carbon is a

building block for photosynthesis The predicted changes in

CO2 in the atmosphere over the next 100 yr will translate to

a 25- to 3-fold increase in dissolved CO2 in seawater

although the subsequent drop in pH will cause shifts in the

equilibria between inorganic carbon forms HCO23 concentra-

tions will only rise by 10 and total Ci available for pho-

tosynthesis (HCO23 1 CO2) will thus rise bylt15 However

if CO2 availability is a constraint to the rate of photosynthe-

sis could the more abundant CO2 result in faster macroalgal

growth Most macroalgae have the capacity to use the

HCO23 ion that is dominant in seawater and given that the

HCO23 concentrations will not change much in future an

impact on photosynthesis is unlikely Furthermore most

macroalgae and seagrasses (Beer et al 2014) possess carbon

concentrating mechanisms (CCMs Giordano et al 2005)

which actively take up inorganic carbon (as HCO23 andor

CO2) and thereby accumulate CO2 at the active site of the

Hill et al Can macroalgae contribute to blue carbon

11

CO2-fixing enzyme Rubisco This effectively saturates

Rubisco for CO2 and limits any increased productivity of

macroalgae from elevated atmospheric CO2 and ocean acidi-

fication There are few exceptions mostly subtidal rhodo-

phytes to the rule that macroalgae possess CCMs so

increased CO2 per se is unlikely to increase CO2 drawdown

by coastal primary producers However there are suggestions

that higher CO2 may increase carbon allocation to seagrass

rhizomes under high light (ie in shallow water) and

thereby enhance burial rates (Jiang et al 2010)

Anthropogenic activities such as climate-change-

associated rising sea temperatures are expected to increase

the occurrence of macroalgal diseases through an increased

virulence of opportunistic pathogens as well as reduced

resistance to disease in thermally stressed hosts (Egan et al

2013) For example in the chemically defended macroalgae

Delisea pulchra bacterial bleaching of the thallus occurs in

response to elevated temperatures due to reduced antibacte-

rial chemical defences (Campbell et al 2011 Case et al

2011) Such diseases therefore have the capacity to reduce

macroalgal abundance either through increased consump-

tion (due to reduced herbivory defence) or through direct

host mortality (Goecke et al 2010)

With the delivery of warmer water further south the East

Australian Current not only contracts the range of many

macroalgal species but also extends the range of urchin con-

sumers Urchin barrens are now extensive throughout south-

eastern Australia and are continuing to expand at the detri-

ment of macroalgal populations (Johnson et al 2011) Such

altered ecological interactions with herbivores from this tro-

picalisation of high latitudes are therefore causing macroal-

gal populations to decline in Tasmania

While climate change will have detrimental effects on

macroalgal populations especially in temperate Australia

tropical regions may experience increased macroalgal abun-

dance following thermal pulses on coral-dominated reefs If

temperatures on coral reefs exceed summer averages by as

little as 1ndash28C mass coral bleaching events can occur which

can lead to coral mortality (Hoegh-Guldberg et al 2007)

Phase shifts toward macroalgal-dominated reefs can follow

especially if herbivory has been reduced by overfishing

(McManus et al 2000 Bruno et al 2009 Hughes et al

2010) However not all tropical macroalgal species will bene-

fit from climate change with species such as Chnoospora

implexa expected to decrease in abundance (Bender et al

2013)

When considering the donor capacity of macroalgae algal

rafts have the potential to deliver dislodged macroalgae to

receiver habitats that can bury the carbon and thus enhance

the carbon sink (see above) However changes in climate

will affect raft supply and persistence (Macreadie et al

2011) Increased storm intensities (IPCC 2007) will promote

substratum detachment andor fragmentation and hence

increase the abundance of algal fragments and rafts and

may also increase burial of macroalgal material (Macreadie

et al 2011) Elevated temperatures however may counter

this process by reducing raft longevity due to an increase in

herbivore metabolism and consumption (Macreadie et al

2011) In addition changes in ocean surface currents may

affect advection routes and potential endpoints of deposition

into more or less favorable receiver environments for

sequestration

Given the dynamic nature of macroalgal populations and

changes in abundance and productivity especially from

human activities the potential for carbon storage and export

may be highly variable In considering the role macroalgae

may play in climate change mitigation the factors detailed

above should be taken into account as they are likely to

greatly influence the contribution of macroalgae to blue car-

bon storage

Conclusions and research priorities

Although macroalgal communities in Australia and

around the world produce massive quantities of plant bio-

mass with high organic carbon content the presence of a

hard rocky substrate precludes the potential for long-term

storage of carbon within the macroalgal habitat In isolation

we therefore conclude that macroalgae do not contribute to

blue carbon

However a considerable proportion of macroalgal bio-

mass becomes dislodged from the benthos and is exported

beyond macroalgal habitat boundaries This donor carbon

may be received by habitats with long-term sequestration

capacity such as seagrass beds saltmarshes mangroves and

continental shelf regions Within Australia and globally

geographic differences in macroalgal biomass community

composition and productivity will influence the blue carbon

donor capacity of macroalgae with the greatest contribu-

tions likely to be in the temperate (and possibly polar)

regions In addition to a high rate of biomass production to

be a viable carbon donor macroalgae must be transferred to

a receiver habitat undergo burial and avoid microbial remi-

neralization The fate of detached macroalgal biomass is not

entirely clear and whilst limited data on the composition of

macroalgal biomass indicates that macroalgal carbon is

highly labile recent research has highlighted the potentially

significant role of refractory taxon-specific compounds (car-

bonates long-chain lipids alginates xylans and sulphated

polysaccharides) from macroalgae in contributing to long-

term blue carbon stores (Trevathan-Tackett et al in press)

We therefore conclude that macroalgae have the potential

to make ecologically meaningful contributions toward global

blue carbon sequestration as significant carbon donors but

further research is needed to quantify these contributions

Data on the degradability of macroalgal plant material is

limited to only a handful of taxa so there is considerable

need for additional testing on other taxa The capacity for

Hill et al Can macroalgae contribute to blue carbon

12

any incorporation of organic material from macroalgae into

long-term carbon stores is only possible if the material can

avoid decomposition by microbes potentially by entering a

storage habitat that is a rapidly accreting zone Research

therefore needs to focus on determining the burial rates of

macroalgal tissue at receiver sites which of these sites are

the greatest sink of macroalgal fragments understanding the

environmental conditions that maximise the burial process

and assessing whether burial is fast enough to limit micro-

bial remineralization of the organic macroalgal material

This will also need to include further research identifying

interspecies variation in carbon donor capacity due to rate of

lability and rate of transport to accreting zones In existing

blue carbon habitats methods for identifying macroalgal car-

bon in the storage zone also need to be developed to gauge

historical contributions of macroalgae into these zones

Once these unknowns are addressed the potential for mac-

roalgae to contribute to blue carbon as a carbon donor will

become less ambiguous Focusing future research on these

key areas will provide evidence as to whether macroalgae

should be included under the blue carbon umbrella

Macroalgal aquaculture and the harvesting of natural pop-

ulations are growing industries worldwide and are actions

that can greatly increase the carbon sequestration capacity

afforded by macroalgae (Chung et al 2011) Furthermore

the production of macroalgal biochar (a process involving

the pyrolysis of biomass) for addition to soil may represent

a viable long-term CO2 sink although research in this field

is in its infancy (Lehmann et al 2006 Bird et al 2011)

Given that macroalgal populations have the highest abun-

dance biomass and productivity of all coastal habitats they

not only store an immense amount of carbon in their living

biomass but they also have an outstanding potential to act

as significant carbon donors However macroalgae are vul-

nerable to a range of anthropogenic impacts so it is impor-

tant to protect these ecosystems for their climate-change-

mitigation potential as well as their ecosystem services

References

Agawin N S R and G M Duarte 2002 Evidence of direct

particle trapping by a tropical seagrass meadow Estuaries

25 1205ndash1209 doi101007BF02692217

Airoldi L D Balata and M W Beck 2008 The Gray Zone

Relationships between habitat loss and marine diversity

and their applications in conservation J Exp Mar Biol

Ecol 366 8ndash15 doi101016jjembe200807034

Airoldi L and M W Beck 2007 Loss status and trends for

coastal marine habitats of Europe Oceanogr Mar Biol

Ann Rev 45 345ndash405

Ang P O J 1985 Regeneration studies of Sargassum

siliquosum J ag and S paniculatum J Ag (Phaeophyta

Sargassaceae) Botanical Marina 28 231ndash235 doi101515

botm1985286231

Bala G 2013 Digesting 400 ppm for global mean CO2

concentration Curr Sci 104 1471ndash1472

Baring R J P G Fairweather and R E Lester 2014

Storm versus calm Variation in fauna associated with

drifting macrophytes in sandy beach surf zones J Exp

Mar Biol Ecol 461 397ndash406 doi101016jjembe2014

09011

Beer S M Bjeuroork and J Beardall 2014 Photosynthesis in

the marine environment Wiley

Behrenfeld M J E Mara~non D A Siegel and S B Hooker

2002 Photoacclimation and nutrient-based model of

light-saturated photosynthesis for quantifying oceanic pri-

mary production Mar Ecol Prog Ser 228 103ndash117 doi

103354meps228103

Bender D G Diaz-Pulido and S Dove 2013 The impact of

CO2 emission scenarios and nutrient enrichment on a

common coral reef macroalga is modified by temporal

effects J Phycol 50 203ndash215 doi101111jpy12153

Bird M I C M Wurster P H de Paula Silva A M Bass

and D de Nys 2011 Algal biocharmdashproduction and

properties Bioresour Technol 102 1886ndash1891 doi

101111j1757-1707201101109x

Briand X 1991 Seaweed harvesting in Europe p 293ndash308

In M D Guiry and G Blunden [eds] Seaweed resources

in Europe Uses and potential Wiley

Bruno J F H Sweatman W F Precht E R Selig and V

G W Schutte 2009 Assessing evidence of phase shifts

from coral to macroalgal dominance on coral reefs

Ecology 90 1478ndash1484 doi10189008-17811

Cacador I A L Coasta and C Vale 2004 Carbon storage

in Tagus salt marsh sediments Water Air Soil Pollut Focus

4 701ndash714 doi101023BWAFO000002838884544ce

Campbell A H T Harder S Nielsen S Kjelleberg and P D

Steinberg 2011 Climate change and disease Bleaching of

a chemically defended seaweed Glob Chang Biol 17

2958ndash2970 doi101111j1365-2486201102456x

Case R J S R Longford A H Campbell A Low N Tujula

P D Steinberg and S Kjelleberg 2011 Temperature

induced bacterial virulence and bleaching disease in a

chemically defended marine macroalga Environ Microbiol

13 529ndash537 doi101111j1462-2920201002356x

Che Hasan R D Ierodiaconou and J Monk 2012

Evaluation of four supervised learning methods for Benthic

habitat mapping using backscatter from multi-beam sonar

Remote Sens 4 3427ndash3443 doi103390rs4113427

Cheshire A C and N D Hallam 1988 Biomass and

density of native stands of Durvillaea potatorum (southern

bull-kelp) in south eastern Australia Mar Ecol Prog Ser

48 277ndash283 doi103354meps048277

Cheshire A C G Westphalen A Wenden L J Scriven

and B C Rowland 1996 Photosynthesis and respiration

of phaeophycean-dominated macroalgal communities in

summer and winter Aquat Bot 55 159ndash170 doi

101016S0304-3770(96)01071-6

Hill et al Can macroalgae contribute to blue carbon

13

export tends to be seasonal (Josselyn and Mathieson 1980)

Furthermore acknowledging spatial variation in the export

of macroalgal and vascular plant biomass macroalgae are

often more significant contributors to surf-zone and beach

wrack than seagrasses (Josselyn and Mathieson 1980 Gomez

et al 2013 Baring et al 2014 Ruiz-Delgado et al 2014)

From genetic and tracking studies we know that exported

macroalgal biomass can be transported long distances (Thiel

and Haye 2006 Fraser et al 2009 2010 2011 Nikula et al

2010) but there is limited information on what happens to

carbon bound within macroalgal biomass once rafts or frag-

ments sink and disintegratemdashie the point at which carbon

bound within macroalgal biomass is broken down into dis-

solved and particulate organic carbon Wada et al (2007)

suggested that macroalgae could release 20ndash40 of their pro-

ductivity as dissolved organic matter (DOM) Much of the

macroalgal DOM is likely to be microbially degraded but

estimates of the refractory component of this DOM will be

important for understanding how much could be donated to

other habitats UV is known to degrade DOM this means

that if this matter can be deposited in regions away from

light such as the deep ocean the breakdown will be further

diminished

There is some evidence to suggest that macroalgal carbon

is donated to other receiver habitats that have long-term

sequestration capacity including the deep sea (Wada et al

2008 Dierssen et al 2009) and other vegetated coastal habi-

tats such as mangrove forests seagrass beds and salt

marshes (Hyndes et al 2012 Macreadie et al 2012) In tropi-

cal estuaries and bays it is estimated that about half of the

macroalgal biomass produced is consumed by herbivores and

the other half is exported to other habitats whereas in the

temperate open coast most of the biomass is decomposed by

detritivores with a lesser amount being exported and only

small fractions being consumed or accumulated as detritus

(Hyndes et al 2013) The fate of macroalgal biomass in tem-

perate estuaries and fjords is largely unknown (Hyndes et al

2013) Most export of macroalgal biomass occurs via advec-

tion but there are also complex biotic pathways that trans-

port macroalgal biomass into receiver habitats such as via

ingestion and concomitant faecal deposition of carbon

within receiver habitats by fish which can contribute to car-

bon sequestration by fertilising receiver habitats and thereby

increasing their productivity and sequestration capacity

(Valiela 1995 Hyndes et al 2013) Breakdown of macroalgae

has been shown to be mostly mediated by microbial proc-

esses (Rieper-Kirchner 1990) however protozoans and meio-

fauna also contribute to the decomposition of macroalgal

tissues as well as enhance microbial degradation Microbial

breakdown rate is also dependent upon the sediment com-

position and oxic status of the water Sassi et al (1988)

found that macroalgal decomposition rates over 25 d under

aerobic vs anaerobic conditions were 35 and 24 respec-

tively Therefore if the macroalgal detritus can be advected

to a rapidly sedimenting region where it can be incorporated

into an anaerobic sediment this will slow the microbial

breakdown and maintain the carbon within the sediment

longer More research is needed to understand how long this

carbon actually remains within anaerobic sediment

All macroalgal carbon that enters the sedimentary carbon

pool will eventually be broken down (oxidised and reminer-

alized) by microbes and converted to inorganic forms and

potentially returned to the atmosphere The rate and effi-

ciency of this remineralization process can dictate whether

macroalgal carbon remains bound within sediments for

months or millennia Macroalgal carbon entering the sedi-

mentary pool has three possible fates (1) particulate and dis-

solved organic carbon that is recalcitrant to microbial

degradation is likely to remain stored within the sediment

for prolonged periods while labile carbon will be recycled by

heterotrophic bacteria and is either (2) assimilated into

microbial biomass or (3) respired as CO2 back to the water

column and possibly the atmosphere The proportion of

nonrespired carbon represents the amount of macroalgal car-

bon that is sequestered

It should be recognised that macroalgae lack the struc-

tural polysaccharide complexity of higher plants and conse-

quently their decomposition rates are faster (Sassi et al

1988) To better understand the degradation pathways of

macroalgal plant material within aquatic sediments

researchers have used several techniques Analyses of ele-

mental composition and stable isotope signatures are rou-

tinely used to ldquofingerprintrdquo carbon and determine its origin

although there is difficultly in separating microalgal and

macroalgal organic carbon signatures (Hardison et al 2011)

Furthermore isotopic signatures may also be variable in

space and time during the decomposition process (Fenton

and Ritz 1988) Similarly a problem with identifying sources

of organic carbon based on carbohydrate composition is that

many groups of organisms contain the same carbohydrates

(Vichkovitten and Holmer 2004) Fatty acid signatures have

proven to offer better resolution of the different plant contri-

butions to organic matter (Hardison et al 2013) although

the level of complexity using this technique is much higher

(Graeve et al 2002) Manipulative approaches using isotopic

tracer studies (Hee et al 2001 Hardison et al 2010 2011

Hyndes et al 2012) and radiolabelling (Chidthaisong et al

1999) have proved to be robust for studying the incorpora-

tion of macroalgal carbon into sediments

Reliable data on the fate of decomposed macroalgal

carbon within sediments (eg macroalgal carbon that is

ldquolostrdquo during litter bag mass loss experiments) is scarce

Hardison et al (2010) traced carbon from senescing macroal-

gae (Gracilaria spp) that were pre-labeled with the 13C stable

isotope and found that 2ndash9 of macroalgal carbon was

incorporated into the sediment This percentage of macroal-

gal carbon uptake by sediments is relatively high suggesting

efficient burial however the fate of this buried carbon was

Hill et al Can macroalgae contribute to blue carbon

10

only monitored for 2 weeks so it is not known whether this

carbon stock was sequestered long-term Other studies sug-

gest that macroalgal carbon is not sequestered long-term For

example Garcia-Robledo et al (2008) found that macroalgal

detritus (tubular and planar Ulva spp) that entered sedimen-

tary organic carbon pools vanished within days after its ini-

tial appearance indicating that carbon from such simple and

ephemeral macroalgae is not retained for durations that

would make them an important component of the long-

term carbon pool within a receiver habitat However given

the diversity in the cell walls and carbon chemistry of mac-

roalgae it is difficult to make conclusions on likely persist-

ence of sequestered macroalgae based on only a handful of

studies

Kristensen (1994) compared the decomposition rate of six

different plant materials (two macroalgae two seagrasses

and two tree leaves) using stepwise thermogravimetry and

found that macroalgae (Fucus vesiculosus and Ulva lactuca)

lost 40ndash44 of their carbon within 70 d whereas seagrasses

(Zostera marina and Ruppia maritima) lost 29ndash55 and tree

leaves (Fagus sylvatica and Rhizophora apiculata) lost only 0ndash

8 Similarly Josselyn and Mathieson (1980) found that

macroalgae (Ascophyllum nodosum and Fucus vesiculosus)

decomposed 3ndash10 times faster than a saltmarsh plant (Spar-

tina alterniflora) and seagrass (Zostera marina) Litter bag stud-

ies have reported a lack of change in sediment carbon

following decomposition of buried macroalgae suggesting

that the organic carbon bound within macroalgal structural

material (eg carbohydrates) is highly labile and rapidly

decomposed by microbes (Vichkovitten and Holmer 2004)

Despite this general pattern of high degradability of macroal-

gae compared with aquatic angiosperms (Trevathan-Tackett

et al in press) there is a high degree of diversity in the

structural complexity of macroalgae particularly in cell-wall

structure and carbon chemistry resulting in high variability

in decay rate estimates within the literature (Rice and Han-

son 1984 Twilley et al 1986 Kristensen 1990 Wada et al

2008 Trevathan-Tackett et al in press)

Nedzarek and Rakusa-Suszczewski (2004) examined the

decomposition of 10 Antarctic macroalgal species finding

they released 80 of the nutrients with the first 3 d of a 69

d decomposition experiment these rates occurred at polar

temperatures (48C) so it would be assumed that tropical

decomposition would be more rapid Similar results were

found with North Sea macroalgae where 50ndash80 of the tis-

sue biomass was lost within 14 d at 188C (Rieper-Kirchner

1990) which included the brown leathery kelp Laminaria

saccharina

Factors influencing the future carbon storage anddonor ability of macroalgae

This review presents a static view on the current state of

carbon cycling sequestration and donor capacity of macroal-

gae with an emphasis on Australian coastal systems In real-

ity the distribution biomass and productivity of these

macroalgae are vulnerable to change due to anthropogenic

activities and as such the dynamic nature of these macroal-

gal systems should be taken into consideration Factors such

as climate change (Duarte et al 2013) and urbanisation (Air-

oldi and Beck 2007 Airoldi et al 2008) can greatly alter the

distribution abundance and productivity of these systems

although the rate of change in global macroalgae population

size remains unknown

Climate change can greatly influence the survival photo-

synthetic capacity growth and competitive interactions of

macroalgae in coastal habitats (Wernberg et al 2011b)

Ocean warming on both the east and west coasts of Australia

have caused pole-ward movement of macroalgal species over

the past five decades (Wernberg et al 2011a) Potentially

hundreds of species are expected to be driven beyond the

edge of the Australian continent as warming continues driv-

ing not only local but global extinctions as 62 of macro-

algal species found in southern Australia are endemic to the

region (Phillips 2001) On the east coast of Australia there

has been a southern retreat of three habitat-forming macro-

algal species (Ecklonia radiata Phyllospora comosa and Durvil-

laea potatorum Millar 2007) and in eastern Tasmania the

once common Macrocystis pyrifera has almost completely dis-

appeared with ocean warming (Edyvane 2003 Johnson et al

2011)

In addition to rising temperatures climate change is

expected to influence macroalgal distribution and productiv-

ity through ocean acidification emergence of marine dis-

eases and shifts in the distribution of consumers In

terrestrial ecosystems there have been climate-driven

increases in global net primary production due to the easing

of critical climatic constraints such as increasing solar radia-

tion from reduced cloud cover (Nemani et al 2003) In the

oceans while increased CO2 dissolution is reducing pH and

disrupting carbonate chemistry this inorganic carbon is a

building block for photosynthesis The predicted changes in

CO2 in the atmosphere over the next 100 yr will translate to

a 25- to 3-fold increase in dissolved CO2 in seawater

although the subsequent drop in pH will cause shifts in the

equilibria between inorganic carbon forms HCO23 concentra-

tions will only rise by 10 and total Ci available for pho-

tosynthesis (HCO23 1 CO2) will thus rise bylt15 However

if CO2 availability is a constraint to the rate of photosynthe-

sis could the more abundant CO2 result in faster macroalgal

growth Most macroalgae have the capacity to use the

HCO23 ion that is dominant in seawater and given that the

HCO23 concentrations will not change much in future an

impact on photosynthesis is unlikely Furthermore most

macroalgae and seagrasses (Beer et al 2014) possess carbon

concentrating mechanisms (CCMs Giordano et al 2005)

which actively take up inorganic carbon (as HCO23 andor

CO2) and thereby accumulate CO2 at the active site of the

Hill et al Can macroalgae contribute to blue carbon

11

CO2-fixing enzyme Rubisco This effectively saturates

Rubisco for CO2 and limits any increased productivity of

macroalgae from elevated atmospheric CO2 and ocean acidi-

fication There are few exceptions mostly subtidal rhodo-

phytes to the rule that macroalgae possess CCMs so

increased CO2 per se is unlikely to increase CO2 drawdown

by coastal primary producers However there are suggestions

that higher CO2 may increase carbon allocation to seagrass

rhizomes under high light (ie in shallow water) and

thereby enhance burial rates (Jiang et al 2010)

Anthropogenic activities such as climate-change-

associated rising sea temperatures are expected to increase

the occurrence of macroalgal diseases through an increased

virulence of opportunistic pathogens as well as reduced

resistance to disease in thermally stressed hosts (Egan et al

2013) For example in the chemically defended macroalgae

Delisea pulchra bacterial bleaching of the thallus occurs in

response to elevated temperatures due to reduced antibacte-

rial chemical defences (Campbell et al 2011 Case et al

2011) Such diseases therefore have the capacity to reduce

macroalgal abundance either through increased consump-

tion (due to reduced herbivory defence) or through direct

host mortality (Goecke et al 2010)

With the delivery of warmer water further south the East

Australian Current not only contracts the range of many

macroalgal species but also extends the range of urchin con-

sumers Urchin barrens are now extensive throughout south-

eastern Australia and are continuing to expand at the detri-

ment of macroalgal populations (Johnson et al 2011) Such

altered ecological interactions with herbivores from this tro-

picalisation of high latitudes are therefore causing macroal-

gal populations to decline in Tasmania

While climate change will have detrimental effects on

macroalgal populations especially in temperate Australia

tropical regions may experience increased macroalgal abun-

dance following thermal pulses on coral-dominated reefs If

temperatures on coral reefs exceed summer averages by as

little as 1ndash28C mass coral bleaching events can occur which

can lead to coral mortality (Hoegh-Guldberg et al 2007)

Phase shifts toward macroalgal-dominated reefs can follow

especially if herbivory has been reduced by overfishing

(McManus et al 2000 Bruno et al 2009 Hughes et al

2010) However not all tropical macroalgal species will bene-

fit from climate change with species such as Chnoospora

implexa expected to decrease in abundance (Bender et al

2013)

When considering the donor capacity of macroalgae algal

rafts have the potential to deliver dislodged macroalgae to

receiver habitats that can bury the carbon and thus enhance

the carbon sink (see above) However changes in climate

will affect raft supply and persistence (Macreadie et al

2011) Increased storm intensities (IPCC 2007) will promote

substratum detachment andor fragmentation and hence

increase the abundance of algal fragments and rafts and

may also increase burial of macroalgal material (Macreadie

et al 2011) Elevated temperatures however may counter

this process by reducing raft longevity due to an increase in

herbivore metabolism and consumption (Macreadie et al

2011) In addition changes in ocean surface currents may

affect advection routes and potential endpoints of deposition

into more or less favorable receiver environments for

sequestration

Given the dynamic nature of macroalgal populations and

changes in abundance and productivity especially from

human activities the potential for carbon storage and export

may be highly variable In considering the role macroalgae

may play in climate change mitigation the factors detailed

above should be taken into account as they are likely to

greatly influence the contribution of macroalgae to blue car-

bon storage

Conclusions and research priorities

Although macroalgal communities in Australia and

around the world produce massive quantities of plant bio-

mass with high organic carbon content the presence of a

hard rocky substrate precludes the potential for long-term

storage of carbon within the macroalgal habitat In isolation

we therefore conclude that macroalgae do not contribute to

blue carbon

However a considerable proportion of macroalgal bio-

mass becomes dislodged from the benthos and is exported

beyond macroalgal habitat boundaries This donor carbon

may be received by habitats with long-term sequestration

capacity such as seagrass beds saltmarshes mangroves and

continental shelf regions Within Australia and globally

geographic differences in macroalgal biomass community

composition and productivity will influence the blue carbon

donor capacity of macroalgae with the greatest contribu-

tions likely to be in the temperate (and possibly polar)

regions In addition to a high rate of biomass production to

be a viable carbon donor macroalgae must be transferred to

a receiver habitat undergo burial and avoid microbial remi-

neralization The fate of detached macroalgal biomass is not

entirely clear and whilst limited data on the composition of

macroalgal biomass indicates that macroalgal carbon is

highly labile recent research has highlighted the potentially

significant role of refractory taxon-specific compounds (car-

bonates long-chain lipids alginates xylans and sulphated

polysaccharides) from macroalgae in contributing to long-

term blue carbon stores (Trevathan-Tackett et al in press)

We therefore conclude that macroalgae have the potential

to make ecologically meaningful contributions toward global

blue carbon sequestration as significant carbon donors but

further research is needed to quantify these contributions

Data on the degradability of macroalgal plant material is

limited to only a handful of taxa so there is considerable

need for additional testing on other taxa The capacity for

Hill et al Can macroalgae contribute to blue carbon

12

any incorporation of organic material from macroalgae into

long-term carbon stores is only possible if the material can

avoid decomposition by microbes potentially by entering a

storage habitat that is a rapidly accreting zone Research

therefore needs to focus on determining the burial rates of

macroalgal tissue at receiver sites which of these sites are

the greatest sink of macroalgal fragments understanding the

environmental conditions that maximise the burial process

and assessing whether burial is fast enough to limit micro-

bial remineralization of the organic macroalgal material

This will also need to include further research identifying

interspecies variation in carbon donor capacity due to rate of

lability and rate of transport to accreting zones In existing

blue carbon habitats methods for identifying macroalgal car-

bon in the storage zone also need to be developed to gauge

historical contributions of macroalgae into these zones

Once these unknowns are addressed the potential for mac-

roalgae to contribute to blue carbon as a carbon donor will

become less ambiguous Focusing future research on these

key areas will provide evidence as to whether macroalgae

should be included under the blue carbon umbrella

Macroalgal aquaculture and the harvesting of natural pop-

ulations are growing industries worldwide and are actions

that can greatly increase the carbon sequestration capacity

afforded by macroalgae (Chung et al 2011) Furthermore

the production of macroalgal biochar (a process involving

the pyrolysis of biomass) for addition to soil may represent

a viable long-term CO2 sink although research in this field

is in its infancy (Lehmann et al 2006 Bird et al 2011)

Given that macroalgal populations have the highest abun-

dance biomass and productivity of all coastal habitats they

not only store an immense amount of carbon in their living

biomass but they also have an outstanding potential to act

as significant carbon donors However macroalgae are vul-

nerable to a range of anthropogenic impacts so it is impor-

tant to protect these ecosystems for their climate-change-

mitigation potential as well as their ecosystem services

References

Agawin N S R and G M Duarte 2002 Evidence of direct

particle trapping by a tropical seagrass meadow Estuaries

25 1205ndash1209 doi101007BF02692217

Airoldi L D Balata and M W Beck 2008 The Gray Zone

Relationships between habitat loss and marine diversity

and their applications in conservation J Exp Mar Biol

Ecol 366 8ndash15 doi101016jjembe200807034

Airoldi L and M W Beck 2007 Loss status and trends for

coastal marine habitats of Europe Oceanogr Mar Biol

Ann Rev 45 345ndash405

Ang P O J 1985 Regeneration studies of Sargassum

siliquosum J ag and S paniculatum J Ag (Phaeophyta

Sargassaceae) Botanical Marina 28 231ndash235 doi101515

botm1985286231

Bala G 2013 Digesting 400 ppm for global mean CO2

concentration Curr Sci 104 1471ndash1472

Baring R J P G Fairweather and R E Lester 2014

Storm versus calm Variation in fauna associated with

drifting macrophytes in sandy beach surf zones J Exp

Mar Biol Ecol 461 397ndash406 doi101016jjembe2014

09011

Beer S M Bjeuroork and J Beardall 2014 Photosynthesis in

the marine environment Wiley

Behrenfeld M J E Mara~non D A Siegel and S B Hooker

2002 Photoacclimation and nutrient-based model of

light-saturated photosynthesis for quantifying oceanic pri-

mary production Mar Ecol Prog Ser 228 103ndash117 doi

103354meps228103

Bender D G Diaz-Pulido and S Dove 2013 The impact of

CO2 emission scenarios and nutrient enrichment on a

common coral reef macroalga is modified by temporal

effects J Phycol 50 203ndash215 doi101111jpy12153

Bird M I C M Wurster P H de Paula Silva A M Bass

and D de Nys 2011 Algal biocharmdashproduction and

properties Bioresour Technol 102 1886ndash1891 doi

101111j1757-1707201101109x

Briand X 1991 Seaweed harvesting in Europe p 293ndash308

In M D Guiry and G Blunden [eds] Seaweed resources

in Europe Uses and potential Wiley

Bruno J F H Sweatman W F Precht E R Selig and V

G W Schutte 2009 Assessing evidence of phase shifts

from coral to macroalgal dominance on coral reefs

Ecology 90 1478ndash1484 doi10189008-17811

Cacador I A L Coasta and C Vale 2004 Carbon storage

in Tagus salt marsh sediments Water Air Soil Pollut Focus

4 701ndash714 doi101023BWAFO000002838884544ce

Campbell A H T Harder S Nielsen S Kjelleberg and P D

Steinberg 2011 Climate change and disease Bleaching of

a chemically defended seaweed Glob Chang Biol 17

2958ndash2970 doi101111j1365-2486201102456x

Case R J S R Longford A H Campbell A Low N Tujula

P D Steinberg and S Kjelleberg 2011 Temperature

induced bacterial virulence and bleaching disease in a

chemically defended marine macroalga Environ Microbiol

13 529ndash537 doi101111j1462-2920201002356x

Che Hasan R D Ierodiaconou and J Monk 2012

Evaluation of four supervised learning methods for Benthic

habitat mapping using backscatter from multi-beam sonar

Remote Sens 4 3427ndash3443 doi103390rs4113427

Cheshire A C and N D Hallam 1988 Biomass and

density of native stands of Durvillaea potatorum (southern

bull-kelp) in south eastern Australia Mar Ecol Prog Ser

48 277ndash283 doi103354meps048277

Cheshire A C G Westphalen A Wenden L J Scriven

and B C Rowland 1996 Photosynthesis and respiration

of phaeophycean-dominated macroalgal communities in

summer and winter Aquat Bot 55 159ndash170 doi

101016S0304-3770(96)01071-6

Hill et al Can macroalgae contribute to blue carbon

13

only monitored for 2 weeks so it is not known whether this

carbon stock was sequestered long-term Other studies sug-

gest that macroalgal carbon is not sequestered long-term For

example Garcia-Robledo et al (2008) found that macroalgal

detritus (tubular and planar Ulva spp) that entered sedimen-

tary organic carbon pools vanished within days after its ini-

tial appearance indicating that carbon from such simple and

ephemeral macroalgae is not retained for durations that

would make them an important component of the long-

term carbon pool within a receiver habitat However given

the diversity in the cell walls and carbon chemistry of mac-

roalgae it is difficult to make conclusions on likely persist-

ence of sequestered macroalgae based on only a handful of

studies

Kristensen (1994) compared the decomposition rate of six

different plant materials (two macroalgae two seagrasses

and two tree leaves) using stepwise thermogravimetry and

found that macroalgae (Fucus vesiculosus and Ulva lactuca)

lost 40ndash44 of their carbon within 70 d whereas seagrasses

(Zostera marina and Ruppia maritima) lost 29ndash55 and tree

leaves (Fagus sylvatica and Rhizophora apiculata) lost only 0ndash

8 Similarly Josselyn and Mathieson (1980) found that

macroalgae (Ascophyllum nodosum and Fucus vesiculosus)

decomposed 3ndash10 times faster than a saltmarsh plant (Spar-

tina alterniflora) and seagrass (Zostera marina) Litter bag stud-

ies have reported a lack of change in sediment carbon

following decomposition of buried macroalgae suggesting

that the organic carbon bound within macroalgal structural

material (eg carbohydrates) is highly labile and rapidly

decomposed by microbes (Vichkovitten and Holmer 2004)

Despite this general pattern of high degradability of macroal-

gae compared with aquatic angiosperms (Trevathan-Tackett

et al in press) there is a high degree of diversity in the

structural complexity of macroalgae particularly in cell-wall

structure and carbon chemistry resulting in high variability

in decay rate estimates within the literature (Rice and Han-

son 1984 Twilley et al 1986 Kristensen 1990 Wada et al

2008 Trevathan-Tackett et al in press)

Nedzarek and Rakusa-Suszczewski (2004) examined the

decomposition of 10 Antarctic macroalgal species finding

they released 80 of the nutrients with the first 3 d of a 69

d decomposition experiment these rates occurred at polar

temperatures (48C) so it would be assumed that tropical

decomposition would be more rapid Similar results were

found with North Sea macroalgae where 50ndash80 of the tis-

sue biomass was lost within 14 d at 188C (Rieper-Kirchner

1990) which included the brown leathery kelp Laminaria

saccharina

Factors influencing the future carbon storage anddonor ability of macroalgae

This review presents a static view on the current state of

carbon cycling sequestration and donor capacity of macroal-

gae with an emphasis on Australian coastal systems In real-

ity the distribution biomass and productivity of these

macroalgae are vulnerable to change due to anthropogenic

activities and as such the dynamic nature of these macroal-

gal systems should be taken into consideration Factors such

as climate change (Duarte et al 2013) and urbanisation (Air-

oldi and Beck 2007 Airoldi et al 2008) can greatly alter the

distribution abundance and productivity of these systems

although the rate of change in global macroalgae population

size remains unknown

Climate change can greatly influence the survival photo-

synthetic capacity growth and competitive interactions of

macroalgae in coastal habitats (Wernberg et al 2011b)

Ocean warming on both the east and west coasts of Australia

have caused pole-ward movement of macroalgal species over

the past five decades (Wernberg et al 2011a) Potentially

hundreds of species are expected to be driven beyond the

edge of the Australian continent as warming continues driv-

ing not only local but global extinctions as 62 of macro-

algal species found in southern Australia are endemic to the

region (Phillips 2001) On the east coast of Australia there

has been a southern retreat of three habitat-forming macro-

algal species (Ecklonia radiata Phyllospora comosa and Durvil-

laea potatorum Millar 2007) and in eastern Tasmania the

once common Macrocystis pyrifera has almost completely dis-

appeared with ocean warming (Edyvane 2003 Johnson et al

2011)

In addition to rising temperatures climate change is

expected to influence macroalgal distribution and productiv-

ity through ocean acidification emergence of marine dis-

eases and shifts in the distribution of consumers In

terrestrial ecosystems there have been climate-driven

increases in global net primary production due to the easing

of critical climatic constraints such as increasing solar radia-

tion from reduced cloud cover (Nemani et al 2003) In the

oceans while increased CO2 dissolution is reducing pH and

disrupting carbonate chemistry this inorganic carbon is a

building block for photosynthesis The predicted changes in

CO2 in the atmosphere over the next 100 yr will translate to

a 25- to 3-fold increase in dissolved CO2 in seawater

although the subsequent drop in pH will cause shifts in the

equilibria between inorganic carbon forms HCO23 concentra-

tions will only rise by 10 and total Ci available for pho-

tosynthesis (HCO23 1 CO2) will thus rise bylt15 However

if CO2 availability is a constraint to the rate of photosynthe-

sis could the more abundant CO2 result in faster macroalgal

growth Most macroalgae have the capacity to use the

HCO23 ion that is dominant in seawater and given that the

HCO23 concentrations will not change much in future an

impact on photosynthesis is unlikely Furthermore most

macroalgae and seagrasses (Beer et al 2014) possess carbon

concentrating mechanisms (CCMs Giordano et al 2005)

which actively take up inorganic carbon (as HCO23 andor

CO2) and thereby accumulate CO2 at the active site of the

Hill et al Can macroalgae contribute to blue carbon

11

CO2-fixing enzyme Rubisco This effectively saturates

Rubisco for CO2 and limits any increased productivity of

macroalgae from elevated atmospheric CO2 and ocean acidi-

fication There are few exceptions mostly subtidal rhodo-

phytes to the rule that macroalgae possess CCMs so

increased CO2 per se is unlikely to increase CO2 drawdown

by coastal primary producers However there are suggestions

that higher CO2 may increase carbon allocation to seagrass

rhizomes under high light (ie in shallow water) and

thereby enhance burial rates (Jiang et al 2010)

Anthropogenic activities such as climate-change-

associated rising sea temperatures are expected to increase

the occurrence of macroalgal diseases through an increased

virulence of opportunistic pathogens as well as reduced

resistance to disease in thermally stressed hosts (Egan et al

2013) For example in the chemically defended macroalgae

Delisea pulchra bacterial bleaching of the thallus occurs in

response to elevated temperatures due to reduced antibacte-

rial chemical defences (Campbell et al 2011 Case et al

2011) Such diseases therefore have the capacity to reduce

macroalgal abundance either through increased consump-

tion (due to reduced herbivory defence) or through direct

host mortality (Goecke et al 2010)

With the delivery of warmer water further south the East

Australian Current not only contracts the range of many

macroalgal species but also extends the range of urchin con-

sumers Urchin barrens are now extensive throughout south-

eastern Australia and are continuing to expand at the detri-

ment of macroalgal populations (Johnson et al 2011) Such

altered ecological interactions with herbivores from this tro-

picalisation of high latitudes are therefore causing macroal-

gal populations to decline in Tasmania

While climate change will have detrimental effects on

macroalgal populations especially in temperate Australia

tropical regions may experience increased macroalgal abun-

dance following thermal pulses on coral-dominated reefs If

temperatures on coral reefs exceed summer averages by as

little as 1ndash28C mass coral bleaching events can occur which

can lead to coral mortality (Hoegh-Guldberg et al 2007)

Phase shifts toward macroalgal-dominated reefs can follow

especially if herbivory has been reduced by overfishing

(McManus et al 2000 Bruno et al 2009 Hughes et al

2010) However not all tropical macroalgal species will bene-

fit from climate change with species such as Chnoospora

implexa expected to decrease in abundance (Bender et al

2013)

When considering the donor capacity of macroalgae algal

rafts have the potential to deliver dislodged macroalgae to

receiver habitats that can bury the carbon and thus enhance

the carbon sink (see above) However changes in climate

will affect raft supply and persistence (Macreadie et al

2011) Increased storm intensities (IPCC 2007) will promote

substratum detachment andor fragmentation and hence

increase the abundance of algal fragments and rafts and

may also increase burial of macroalgal material (Macreadie

et al 2011) Elevated temperatures however may counter

this process by reducing raft longevity due to an increase in

herbivore metabolism and consumption (Macreadie et al

2011) In addition changes in ocean surface currents may

affect advection routes and potential endpoints of deposition

into more or less favorable receiver environments for

sequestration

Given the dynamic nature of macroalgal populations and

changes in abundance and productivity especially from

human activities the potential for carbon storage and export

may be highly variable In considering the role macroalgae

may play in climate change mitigation the factors detailed

above should be taken into account as they are likely to

greatly influence the contribution of macroalgae to blue car-

bon storage

Conclusions and research priorities

Although macroalgal communities in Australia and

around the world produce massive quantities of plant bio-

mass with high organic carbon content the presence of a

hard rocky substrate precludes the potential for long-term

storage of carbon within the macroalgal habitat In isolation

we therefore conclude that macroalgae do not contribute to

blue carbon

However a considerable proportion of macroalgal bio-

mass becomes dislodged from the benthos and is exported

beyond macroalgal habitat boundaries This donor carbon

may be received by habitats with long-term sequestration

capacity such as seagrass beds saltmarshes mangroves and

continental shelf regions Within Australia and globally

geographic differences in macroalgal biomass community

composition and productivity will influence the blue carbon

donor capacity of macroalgae with the greatest contribu-

tions likely to be in the temperate (and possibly polar)

regions In addition to a high rate of biomass production to

be a viable carbon donor macroalgae must be transferred to

a receiver habitat undergo burial and avoid microbial remi-

neralization The fate of detached macroalgal biomass is not

entirely clear and whilst limited data on the composition of

macroalgal biomass indicates that macroalgal carbon is

highly labile recent research has highlighted the potentially

significant role of refractory taxon-specific compounds (car-

bonates long-chain lipids alginates xylans and sulphated

polysaccharides) from macroalgae in contributing to long-

term blue carbon stores (Trevathan-Tackett et al in press)

We therefore conclude that macroalgae have the potential

to make ecologically meaningful contributions toward global

blue carbon sequestration as significant carbon donors but

further research is needed to quantify these contributions

Data on the degradability of macroalgal plant material is

limited to only a handful of taxa so there is considerable

need for additional testing on other taxa The capacity for

Hill et al Can macroalgae contribute to blue carbon

12

any incorporation of organic material from macroalgae into

long-term carbon stores is only possible if the material can

avoid decomposition by microbes potentially by entering a

storage habitat that is a rapidly accreting zone Research

therefore needs to focus on determining the burial rates of

macroalgal tissue at receiver sites which of these sites are

the greatest sink of macroalgal fragments understanding the

environmental conditions that maximise the burial process

and assessing whether burial is fast enough to limit micro-

bial remineralization of the organic macroalgal material

This will also need to include further research identifying

interspecies variation in carbon donor capacity due to rate of

lability and rate of transport to accreting zones In existing

blue carbon habitats methods for identifying macroalgal car-

bon in the storage zone also need to be developed to gauge

historical contributions of macroalgae into these zones

Once these unknowns are addressed the potential for mac-

roalgae to contribute to blue carbon as a carbon donor will

become less ambiguous Focusing future research on these

key areas will provide evidence as to whether macroalgae

should be included under the blue carbon umbrella

Macroalgal aquaculture and the harvesting of natural pop-

ulations are growing industries worldwide and are actions

that can greatly increase the carbon sequestration capacity

afforded by macroalgae (Chung et al 2011) Furthermore

the production of macroalgal biochar (a process involving

the pyrolysis of biomass) for addition to soil may represent

a viable long-term CO2 sink although research in this field

is in its infancy (Lehmann et al 2006 Bird et al 2011)

Given that macroalgal populations have the highest abun-

dance biomass and productivity of all coastal habitats they

not only store an immense amount of carbon in their living

biomass but they also have an outstanding potential to act

as significant carbon donors However macroalgae are vul-

nerable to a range of anthropogenic impacts so it is impor-

tant to protect these ecosystems for their climate-change-

mitigation potential as well as their ecosystem services

References

Agawin N S R and G M Duarte 2002 Evidence of direct

particle trapping by a tropical seagrass meadow Estuaries

25 1205ndash1209 doi101007BF02692217

Airoldi L D Balata and M W Beck 2008 The Gray Zone

Relationships between habitat loss and marine diversity

and their applications in conservation J Exp Mar Biol

Ecol 366 8ndash15 doi101016jjembe200807034

Airoldi L and M W Beck 2007 Loss status and trends for

coastal marine habitats of Europe Oceanogr Mar Biol

Ann Rev 45 345ndash405

Ang P O J 1985 Regeneration studies of Sargassum

siliquosum J ag and S paniculatum J Ag (Phaeophyta

Sargassaceae) Botanical Marina 28 231ndash235 doi101515

botm1985286231

Bala G 2013 Digesting 400 ppm for global mean CO2

concentration Curr Sci 104 1471ndash1472

Baring R J P G Fairweather and R E Lester 2014

Storm versus calm Variation in fauna associated with

drifting macrophytes in sandy beach surf zones J Exp

Mar Biol Ecol 461 397ndash406 doi101016jjembe2014

09011

Beer S M Bjeuroork and J Beardall 2014 Photosynthesis in

the marine environment Wiley

Behrenfeld M J E Mara~non D A Siegel and S B Hooker

2002 Photoacclimation and nutrient-based model of

light-saturated photosynthesis for quantifying oceanic pri-

mary production Mar Ecol Prog Ser 228 103ndash117 doi

103354meps228103

Bender D G Diaz-Pulido and S Dove 2013 The impact of

CO2 emission scenarios and nutrient enrichment on a

common coral reef macroalga is modified by temporal

effects J Phycol 50 203ndash215 doi101111jpy12153

Bird M I C M Wurster P H de Paula Silva A M Bass

and D de Nys 2011 Algal biocharmdashproduction and

properties Bioresour Technol 102 1886ndash1891 doi

101111j1757-1707201101109x

Briand X 1991 Seaweed harvesting in Europe p 293ndash308

In M D Guiry and G Blunden [eds] Seaweed resources

in Europe Uses and potential Wiley

Bruno J F H Sweatman W F Precht E R Selig and V

G W Schutte 2009 Assessing evidence of phase shifts

from coral to macroalgal dominance on coral reefs

Ecology 90 1478ndash1484 doi10189008-17811

Cacador I A L Coasta and C Vale 2004 Carbon storage

in Tagus salt marsh sediments Water Air Soil Pollut Focus

4 701ndash714 doi101023BWAFO000002838884544ce

Campbell A H T Harder S Nielsen S Kjelleberg and P D

Steinberg 2011 Climate change and disease Bleaching of

a chemically defended seaweed Glob Chang Biol 17

2958ndash2970 doi101111j1365-2486201102456x

Case R J S R Longford A H Campbell A Low N Tujula

P D Steinberg and S Kjelleberg 2011 Temperature

induced bacterial virulence and bleaching disease in a

chemically defended marine macroalga Environ Microbiol

13 529ndash537 doi101111j1462-2920201002356x

Che Hasan R D Ierodiaconou and J Monk 2012

Evaluation of four supervised learning methods for Benthic

habitat mapping using backscatter from multi-beam sonar

Remote Sens 4 3427ndash3443 doi103390rs4113427

Cheshire A C and N D Hallam 1988 Biomass and

density of native stands of Durvillaea potatorum (southern

bull-kelp) in south eastern Australia Mar Ecol Prog Ser

48 277ndash283 doi103354meps048277

Cheshire A C G Westphalen A Wenden L J Scriven

and B C Rowland 1996 Photosynthesis and respiration

of phaeophycean-dominated macroalgal communities in

summer and winter Aquat Bot 55 159ndash170 doi

101016S0304-3770(96)01071-6

Hill et al Can macroalgae contribute to blue carbon

13

CO2-fixing enzyme Rubisco This effectively saturates

Rubisco for CO2 and limits any increased productivity of

macroalgae from elevated atmospheric CO2 and ocean acidi-

fication There are few exceptions mostly subtidal rhodo-

phytes to the rule that macroalgae possess CCMs so

increased CO2 per se is unlikely to increase CO2 drawdown

by coastal primary producers However there are suggestions

that higher CO2 may increase carbon allocation to seagrass

rhizomes under high light (ie in shallow water) and

thereby enhance burial rates (Jiang et al 2010)

Anthropogenic activities such as climate-change-

associated rising sea temperatures are expected to increase

the occurrence of macroalgal diseases through an increased

virulence of opportunistic pathogens as well as reduced

resistance to disease in thermally stressed hosts (Egan et al

2013) For example in the chemically defended macroalgae

Delisea pulchra bacterial bleaching of the thallus occurs in

response to elevated temperatures due to reduced antibacte-

rial chemical defences (Campbell et al 2011 Case et al

2011) Such diseases therefore have the capacity to reduce

macroalgal abundance either through increased consump-

tion (due to reduced herbivory defence) or through direct

host mortality (Goecke et al 2010)

With the delivery of warmer water further south the East

Australian Current not only contracts the range of many

macroalgal species but also extends the range of urchin con-

sumers Urchin barrens are now extensive throughout south-

eastern Australia and are continuing to expand at the detri-

ment of macroalgal populations (Johnson et al 2011) Such

altered ecological interactions with herbivores from this tro-

picalisation of high latitudes are therefore causing macroal-

gal populations to decline in Tasmania

While climate change will have detrimental effects on

macroalgal populations especially in temperate Australia

tropical regions may experience increased macroalgal abun-

dance following thermal pulses on coral-dominated reefs If

temperatures on coral reefs exceed summer averages by as

little as 1ndash28C mass coral bleaching events can occur which

can lead to coral mortality (Hoegh-Guldberg et al 2007)

Phase shifts toward macroalgal-dominated reefs can follow

especially if herbivory has been reduced by overfishing

(McManus et al 2000 Bruno et al 2009 Hughes et al

2010) However not all tropical macroalgal species will bene-

fit from climate change with species such as Chnoospora

implexa expected to decrease in abundance (Bender et al

2013)

When considering the donor capacity of macroalgae algal

rafts have the potential to deliver dislodged macroalgae to

receiver habitats that can bury the carbon and thus enhance

the carbon sink (see above) However changes in climate

will affect raft supply and persistence (Macreadie et al

2011) Increased storm intensities (IPCC 2007) will promote

substratum detachment andor fragmentation and hence

increase the abundance of algal fragments and rafts and

may also increase burial of macroalgal material (Macreadie

et al 2011) Elevated temperatures however may counter

this process by reducing raft longevity due to an increase in

herbivore metabolism and consumption (Macreadie et al

2011) In addition changes in ocean surface currents may

affect advection routes and potential endpoints of deposition

into more or less favorable receiver environments for

sequestration

Given the dynamic nature of macroalgal populations and

changes in abundance and productivity especially from

human activities the potential for carbon storage and export

may be highly variable In considering the role macroalgae

may play in climate change mitigation the factors detailed

above should be taken into account as they are likely to

greatly influence the contribution of macroalgae to blue car-

bon storage

Conclusions and research priorities

Although macroalgal communities in Australia and

around the world produce massive quantities of plant bio-

mass with high organic carbon content the presence of a

hard rocky substrate precludes the potential for long-term

storage of carbon within the macroalgal habitat In isolation

we therefore conclude that macroalgae do not contribute to

blue carbon

However a considerable proportion of macroalgal bio-

mass becomes dislodged from the benthos and is exported

beyond macroalgal habitat boundaries This donor carbon

may be received by habitats with long-term sequestration

capacity such as seagrass beds saltmarshes mangroves and

continental shelf regions Within Australia and globally

geographic differences in macroalgal biomass community

composition and productivity will influence the blue carbon

donor capacity of macroalgae with the greatest contribu-

tions likely to be in the temperate (and possibly polar)

regions In addition to a high rate of biomass production to

be a viable carbon donor macroalgae must be transferred to

a receiver habitat undergo burial and avoid microbial remi-

neralization The fate of detached macroalgal biomass is not

entirely clear and whilst limited data on the composition of

macroalgal biomass indicates that macroalgal carbon is

highly labile recent research has highlighted the potentially

significant role of refractory taxon-specific compounds (car-

bonates long-chain lipids alginates xylans and sulphated

polysaccharides) from macroalgae in contributing to long-

term blue carbon stores (Trevathan-Tackett et al in press)

We therefore conclude that macroalgae have the potential

to make ecologically meaningful contributions toward global

blue carbon sequestration as significant carbon donors but

further research is needed to quantify these contributions

Data on the degradability of macroalgal plant material is

limited to only a handful of taxa so there is considerable

need for additional testing on other taxa The capacity for

Hill et al Can macroalgae contribute to blue carbon

12

any incorporation of organic material from macroalgae into

long-term carbon stores is only possible if the material can

avoid decomposition by microbes potentially by entering a

storage habitat that is a rapidly accreting zone Research

therefore needs to focus on determining the burial rates of

macroalgal tissue at receiver sites which of these sites are

the greatest sink of macroalgal fragments understanding the

environmental conditions that maximise the burial process

and assessing whether burial is fast enough to limit micro-

bial remineralization of the organic macroalgal material

This will also need to include further research identifying

interspecies variation in carbon donor capacity due to rate of

lability and rate of transport to accreting zones In existing

blue carbon habitats methods for identifying macroalgal car-

bon in the storage zone also need to be developed to gauge

historical contributions of macroalgae into these zones

Once these unknowns are addressed the potential for mac-

roalgae to contribute to blue carbon as a carbon donor will

become less ambiguous Focusing future research on these

key areas will provide evidence as to whether macroalgae

should be included under the blue carbon umbrella

Macroalgal aquaculture and the harvesting of natural pop-

ulations are growing industries worldwide and are actions

that can greatly increase the carbon sequestration capacity

afforded by macroalgae (Chung et al 2011) Furthermore

the production of macroalgal biochar (a process involving

the pyrolysis of biomass) for addition to soil may represent

a viable long-term CO2 sink although research in this field

is in its infancy (Lehmann et al 2006 Bird et al 2011)

Given that macroalgal populations have the highest abun-

dance biomass and productivity of all coastal habitats they

not only store an immense amount of carbon in their living

biomass but they also have an outstanding potential to act

as significant carbon donors However macroalgae are vul-

nerable to a range of anthropogenic impacts so it is impor-

tant to protect these ecosystems for their climate-change-

mitigation potential as well as their ecosystem services

References

Agawin N S R and G M Duarte 2002 Evidence of direct

particle trapping by a tropical seagrass meadow Estuaries

25 1205ndash1209 doi101007BF02692217

Airoldi L D Balata and M W Beck 2008 The Gray Zone

Relationships between habitat loss and marine diversity

and their applications in conservation J Exp Mar Biol

Ecol 366 8ndash15 doi101016jjembe200807034

Airoldi L and M W Beck 2007 Loss status and trends for

coastal marine habitats of Europe Oceanogr Mar Biol

Ann Rev 45 345ndash405

Ang P O J 1985 Regeneration studies of Sargassum

siliquosum J ag and S paniculatum J Ag (Phaeophyta

Sargassaceae) Botanical Marina 28 231ndash235 doi101515

botm1985286231

Bala G 2013 Digesting 400 ppm for global mean CO2

concentration Curr Sci 104 1471ndash1472

Baring R J P G Fairweather and R E Lester 2014

Storm versus calm Variation in fauna associated with

drifting macrophytes in sandy beach surf zones J Exp

Mar Biol Ecol 461 397ndash406 doi101016jjembe2014

09011

Beer S M Bjeuroork and J Beardall 2014 Photosynthesis in

the marine environment Wiley

Behrenfeld M J E Mara~non D A Siegel and S B Hooker

2002 Photoacclimation and nutrient-based model of

light-saturated photosynthesis for quantifying oceanic pri-

mary production Mar Ecol Prog Ser 228 103ndash117 doi

103354meps228103

Bender D G Diaz-Pulido and S Dove 2013 The impact of

CO2 emission scenarios and nutrient enrichment on a

common coral reef macroalga is modified by temporal

effects J Phycol 50 203ndash215 doi101111jpy12153

Bird M I C M Wurster P H de Paula Silva A M Bass

and D de Nys 2011 Algal biocharmdashproduction and

properties Bioresour Technol 102 1886ndash1891 doi

101111j1757-1707201101109x

Briand X 1991 Seaweed harvesting in Europe p 293ndash308

In M D Guiry and G Blunden [eds] Seaweed resources

in Europe Uses and potential Wiley

Bruno J F H Sweatman W F Precht E R Selig and V

G W Schutte 2009 Assessing evidence of phase shifts

from coral to macroalgal dominance on coral reefs

Ecology 90 1478ndash1484 doi10189008-17811

Cacador I A L Coasta and C Vale 2004 Carbon storage

in Tagus salt marsh sediments Water Air Soil Pollut Focus

4 701ndash714 doi101023BWAFO000002838884544ce

Campbell A H T Harder S Nielsen S Kjelleberg and P D

Steinberg 2011 Climate change and disease Bleaching of

a chemically defended seaweed Glob Chang Biol 17

2958ndash2970 doi101111j1365-2486201102456x

Case R J S R Longford A H Campbell A Low N Tujula

P D Steinberg and S Kjelleberg 2011 Temperature

induced bacterial virulence and bleaching disease in a

chemically defended marine macroalga Environ Microbiol

13 529ndash537 doi101111j1462-2920201002356x

Che Hasan R D Ierodiaconou and J Monk 2012

Evaluation of four supervised learning methods for Benthic

habitat mapping using backscatter from multi-beam sonar

Remote Sens 4 3427ndash3443 doi103390rs4113427

Cheshire A C and N D Hallam 1988 Biomass and

density of native stands of Durvillaea potatorum (southern

bull-kelp) in south eastern Australia Mar Ecol Prog Ser

48 277ndash283 doi103354meps048277

Cheshire A C G Westphalen A Wenden L J Scriven

and B C Rowland 1996 Photosynthesis and respiration

of phaeophycean-dominated macroalgal communities in

summer and winter Aquat Bot 55 159ndash170 doi

101016S0304-3770(96)01071-6

Hill et al Can macroalgae contribute to blue carbon

13

any incorporation of organic material from macroalgae into

long-term carbon stores is only possible if the material can

avoid decomposition by microbes potentially by entering a

storage habitat that is a rapidly accreting zone Research

therefore needs to focus on determining the burial rates of

macroalgal tissue at receiver sites which of these sites are

the greatest sink of macroalgal fragments understanding the

environmental conditions that maximise the burial process

and assessing whether burial is fast enough to limit micro-

bial remineralization of the organic macroalgal material

This will also need to include further research identifying

interspecies variation in carbon donor capacity due to rate of

lability and rate of transport to accreting zones In existing

blue carbon habitats methods for identifying macroalgal car-

bon in the storage zone also need to be developed to gauge

historical contributions of macroalgae into these zones

Once these unknowns are addressed the potential for mac-

roalgae to contribute to blue carbon as a carbon donor will

become less ambiguous Focusing future research on these

key areas will provide evidence as to whether macroalgae

should be included under the blue carbon umbrella

Macroalgal aquaculture and the harvesting of natural pop-

ulations are growing industries worldwide and are actions

that can greatly increase the carbon sequestration capacity

afforded by macroalgae (Chung et al 2011) Furthermore

the production of macroalgal biochar (a process involving

the pyrolysis of biomass) for addition to soil may represent

a viable long-term CO2 sink although research in this field

is in its infancy (Lehmann et al 2006 Bird et al 2011)

Given that macroalgal populations have the highest abun-

dance biomass and productivity of all coastal habitats they

not only store an immense amount of carbon in their living

biomass but they also have an outstanding potential to act

as significant carbon donors However macroalgae are vul-

nerable to a range of anthropogenic impacts so it is impor-

tant to protect these ecosystems for their climate-change-

mitigation potential as well as their ecosystem services

References

Agawin N S R and G M Duarte 2002 Evidence of direct

particle trapping by a tropical seagrass meadow Estuaries

25 1205ndash1209 doi101007BF02692217

Airoldi L D Balata and M W Beck 2008 The Gray Zone

Relationships between habitat loss and marine diversity

and their applications in conservation J Exp Mar Biol

Ecol 366 8ndash15 doi101016jjembe200807034

Airoldi L and M W Beck 2007 Loss status and trends for

coastal marine habitats of Europe Oceanogr Mar Biol

Ann Rev 45 345ndash405

Ang P O J 1985 Regeneration studies of Sargassum

siliquosum J ag and S paniculatum J Ag (Phaeophyta

Sargassaceae) Botanical Marina 28 231ndash235 doi101515

botm1985286231

Bala G 2013 Digesting 400 ppm for global mean CO2

concentration Curr Sci 104 1471ndash1472

Baring R J P G Fairweather and R E Lester 2014

Storm versus calm Variation in fauna associated with

drifting macrophytes in sandy beach surf zones J Exp

Mar Biol Ecol 461 397ndash406 doi101016jjembe2014

09011

Beer S M Bjeuroork and J Beardall 2014 Photosynthesis in

the marine environment Wiley

Behrenfeld M J E Mara~non D A Siegel and S B Hooker

2002 Photoacclimation and nutrient-based model of

light-saturated photosynthesis for quantifying oceanic pri-

mary production Mar Ecol Prog Ser 228 103ndash117 doi

103354meps228103

Bender D G Diaz-Pulido and S Dove 2013 The impact of

CO2 emission scenarios and nutrient enrichment on a

common coral reef macroalga is modified by temporal

effects J Phycol 50 203ndash215 doi101111jpy12153

Bird M I C M Wurster P H de Paula Silva A M Bass

and D de Nys 2011 Algal biocharmdashproduction and

properties Bioresour Technol 102 1886ndash1891 doi

101111j1757-1707201101109x

Briand X 1991 Seaweed harvesting in Europe p 293ndash308

In M D Guiry and G Blunden [eds] Seaweed resources

in Europe Uses and potential Wiley

Bruno J F H Sweatman W F Precht E R Selig and V

G W Schutte 2009 Assessing evidence of phase shifts

from coral to macroalgal dominance on coral reefs

Ecology 90 1478ndash1484 doi10189008-17811

Cacador I A L Coasta and C Vale 2004 Carbon storage

in Tagus salt marsh sediments Water Air Soil Pollut Focus

4 701ndash714 doi101023BWAFO000002838884544ce

Campbell A H T Harder S Nielsen S Kjelleberg and P D

Steinberg 2011 Climate change and disease Bleaching of

a chemically defended seaweed Glob Chang Biol 17

2958ndash2970 doi101111j1365-2486201102456x

Case R J S R Longford A H Campbell A Low N Tujula

P D Steinberg and S Kjelleberg 2011 Temperature

induced bacterial virulence and bleaching disease in a

chemically defended marine macroalga Environ Microbiol

13 529ndash537 doi101111j1462-2920201002356x

Che Hasan R D Ierodiaconou and J Monk 2012

Evaluation of four supervised learning methods for Benthic

habitat mapping using backscatter from multi-beam sonar

Remote Sens 4 3427ndash3443 doi103390rs4113427

Cheshire A C and N D Hallam 1988 Biomass and

density of native stands of Durvillaea potatorum (southern

bull-kelp) in south eastern Australia Mar Ecol Prog Ser

48 277ndash283 doi103354meps048277

Cheshire A C G Westphalen A Wenden L J Scriven

and B C Rowland 1996 Photosynthesis and respiration

of phaeophycean-dominated macroalgal communities in

summer and winter Aquat Bot 55 159ndash170 doi

101016S0304-3770(96)01071-6

Hill et al Can macroalgae contribute to blue carbon

13

Chidthaisong A B Rosenstock and R Conrad 1999

Measurement of monosaccharides and conversion of

glucose to acetate in anoxic rice field soil Appl Environ

Microbiol 65 2350ndash2355

Chung I K J Beardall S Mehta D Sahoo and S

Stojkovic 2011 Using marine macroalgae for carbon

sequestration A critical appraisal J Appl Phycol 23

877ndash886 doi101007s10811-010-9604-9

Connell S D and A D Irving 2008 Integrating ecology with

biogeography using landscape characteristics A case study of

subtidal habitat across continental Australia J Biogeogr 35

1608ndash1621 doi101111j1365-2699200801903x

Copertino M S D Connell and A Cheshire 2005 The

prevalence and production of turf-forming algae on a

temperate subtidal coast Phycologia 44 241ndash248 doi

1022160031-8884(2005)44[241TPAPOT]20CO2

Cornwall C E C D Hepburn D Pritchard K I Currie C M

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pH and implications for ocean acidification J Phycol 48

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Department of Agriculture 2013 Australiarsquos Forests Austra-

lian Government Available from httpwwwdaffgovau

forestryaustralias-forests Date accessed 16 June 2015

Dierssen H M R C Zimmerman L A Drake and D J

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macroalgae to the deep sea through wind-driven Lang-

muir circulation Geophys Res Lett 36 L04602 doi

1010292008GL036188

Doney S C V J Fabry R A Feely and J A Kleypas 2009

Ocean acidification The other CO2 problem Ann Rev Mar

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Drew E A and K M Abel 1988 Studies on Halimeda 1

The distribution and species composition of Halimeda

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Coral Reefs 6 195ndash205 doi101007BF00302016

Duarte C M I J Losada I E Hendriks I Mazarrasa and

N Marba 2013 The role of coastal plant communities for

climate change mitigation and adaptation Nat Clim

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2003 Population morphometric and biomechanical

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gradient Mar Ecol Prog Ser 265 57ndash76 doi103354

meps265057

Edyvane K 2003 Conservation monitoring and recovery of

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Industries Water and Environment Tasmania

Egan S N D Fernandes V Kumar M Gardiner and T

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and host defence in marine macroalgae Environ

Microbiol 16 925ndash938 doi1011111462-292012288

Farrelly D C D Everard C C Fagan and K P McDonnell

2013 Carbon sequestration and the role of biological

carbon mitigation A review Renewable Sustainable Energy

Rev 21 712ndash727 doi101016jrser201212038

Fenton G E and D A Ritz 1988 Changes in carbon and

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Fourqurean J W and others 2012 Seagrass ecosystems as a

globally significant carbon stock Nat Geosci 5 505ndash509

doi101038ngeo1477

Fraser C I R Nikula H G Spencer and J M Waters

2009 Kelp genes reveal effects of subantarctic sea ice

during the Last Glacial Maximum Proc Natl Acad Sci U

S A 106 3249ndash3253 doi101073pnas0810635106

Fraser C I R Nikula and J M Waters 2011 Oceanic

rafting by a coastal community Proc R Soc B Biol Sci

278 649ndash655 doi101098rspb20101117

Fraser C I M Thiel H G Spencer and J M Waters 2010

Contemporary habitat discontinuity and historic glacial

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Biol 10 203 doi1011861471-2148-10-203

Garcia-Robledo E A Corzo J G de Lomas and S A van

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experiment Mar Ecol Prog Ser 356 139ndash151 doi

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Geoscience Australia 2010 Coastline lengths Australian Gov-

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Date accessed 16 June 2015

Giordano M J Beardall and J A Raven 2005 CO2

concentrating mechanisms in algae Mechanisms

environmental modulation and evolution Annu Rev

Plant Biol 55 99ndash131 doi101146annurevarplant56

032604144052

Goecke F A Labes J Wiese and J E Imhoff 2010

Chemical interactions between marine macroalgae and

bacteria Mar Ecol Prog Ser 409 267ndash300 doi103354

meps08607

Gomez M F Barreiro J Lopez M Lastra and R De La

Huz 2013 Deposition patterns of algal wrack species on

estuarine beaches Aquat Bot 105 25ndash33 doi101016

jaquabot201212001

Gough C 2008 State of the art in carbon dioxide capture

and storage in the UK An expertsrsquo review Int J

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5836(07)00073-4

Grace J 2004 Understanding and managing the global

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0477200400874x

Graeve M G Kattner C Wiencke and U Karsten 2002

Fatty acid composition of Arctic and Antarctic macroalgae

Hill et al Can macroalgae contribute to blue carbon

14

Indicator of phylogenetic and trophic relationships Mar

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Graiff A U Karsten S Meyer D Pfender F Tala and M

Thiel 2013 Seasonal variation in floating persistence of

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Botanica Marina 56 3ndash14 doi101515bot-2012-0193

Grall J and J M Hall-Spencer 2003 Problems facing maeuroerl

conservation in Brittany Aquat Conserv Mar Freshw

Ecosyst 13 S55ndash64 doi101002aqc568

Gruber R K and W M Kemp 2010 Feedback effects in a

coastal canopy-forming submersed plant bed Limnol

Oceanogr 55 2285ndash2298 doi104319lo20105562285

Guinotte J M and V J Fabry 2008 Ocean acidification

and its potential effects on marine ecosystems Ann N Y

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Hardison A K I C Anderson E A Canuel C R Tobias

and B Veuger 2011 Carbon and nitrogen dynamics in

shallow photic systems Interactions between macroalgae

microalgae and bacteria Limnol Oceanogr 56 1489ndash

1503 doi104319lo20115641489

Hardison A K E A Canuel I C Anderson C R Tobias B

Veuger and M N Waters 2013 Microphytobenthos and

benthic macroalgae determine sediment organic matter

composition in shallow photic sediments Biogeosciences

10 5571ndash5588 doi105194bg-10-5571-2013

Hardison A K E A Canuel I C Anderson and B Veuger

2010 Fate of macroalgae in benthic systems Carbon and

nitrogen cycling within the microbial community Mar

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1998 Influence of oxygen exposure time on organic

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of the kelp Ecklonia radiata near the northern limit of its

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Hee C A T K Pease M J Alperin and C S Martens

2001 Dissolved organic carbon production and

consumption in anoxic marine sediments A pulsed-tracer

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perspective and a first carbonate budget Proceedings of

the 8th International Coral Reef Symposium 1761ndash766

Hilmi N and others 2013 Towards improved socio-

economic assessments of ocean acidificationrsquos impacts

Mar Biol 160 1773ndash1787 doi101007s00227-012-2031-5

Hoegh-Guldberg O and J F Bruno 2010 The impact of

climate change on the worldrsquos marine ecosystems Science

328 1523ndash1528 doi101126science1189930

Hoegh-Guldberg O and others 2007 Coral reefs under

rapid climate change and ocean acidification Science

318 1737ndash1742 doi101126science1152509

Heuroonisch B and others 2012 The geological record of

ocean acidification Science 335 1058ndash1063 doi101126

science1208277

Howe A J J F Rodrıguez and P M Saco 2009 Surface

evolution and carbon sequestration in disturbed and

undisturbed wetland soils of the Hunter estuary

southeast Australia Estuar Coast Shelf Sci 84 75ndash83

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Hughes T N J A Graham J B C Jackson P J Mumby

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sustaining coral reef resilience Trends Ecol Evol 25

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nutrients from reef-derived kelp into a seagrass ecosys-

tem Mar Ecol Prog Ser 445 97ndash107 doi103354

meps09367

Hyndes G A I Nagelkerken R J McLeod R M Connolly

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Ierodiaconou D S Burq M Reston and L Laurenson

2007 Marine benthic habitat mapping using multibeam

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Ierodiaconou D J Monk A Rattray L Laurenson and V

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study of oceanrsquos calcium carbonate budget EOS Trans

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IPCC 2007 Climate change 2007 The physical science

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Johnson C R and others 2011 Climate change cascades

Shifts in oceanography speciesrsquo ranges and subtidal

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032

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Contrasting effects of ocean acidification on tropical

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Benthic macroalgae of Shark Bay Western Australia

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Kennedy H J Beggins C M Duarte J W Fourqurean M

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Koch M G Bowes C Ross and X-H Zhang 2013

Climate change and ocean acidification effects on seagrass

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Krumhansl K A J M Lee and R E Scheibling 2011

Grazing damage and encrustation by an invasive

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Lal R 2005 Forest soils and carbon sequestration For Ecol

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Lehmann J J Gaunt and M Rondon 2006 Bio-char

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Mitigation Adaptation Strateg Glob Chang 11 403ndash427

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Long S P E A Ainsworth A Rogers and D R Ort 2004

Rising atmospheric carbon dioxide Plants FACE the

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Mapping of inshore marine habitats from Schouten Island

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Mapping of inshore marine habitats in the Cradle Coast

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Macreadie P I M E Baird S M Trevathan-Tackett A W

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modelling the carbon sequestration capacity of seagrass

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Macreadie P I M J Bishop and D J Booth 2011

Implications of climate change for macrophytic rafts and

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Malhi Y D D Baldocchi and P G Jarvis 1999 The

carbon balance of tropical temperate and boreal forest

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Markewitz P and others 2012 Worldwide innovations in

the development of carbon capture technologies and the

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Hill et al Can macroalgae contribute to blue carbon

16

Marshall J F and P J Davies 1988 Halimeda bioherms of

the northern Great Barrier Reef Coral Reefs 6 139ndash148

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McKenzie P F and A Bellgrove 2009 Dislodgment and

attachment strength of the intertidal macroalga

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Mcleod E and others 2011 A blueprint for blue carbon

Toward an improved understanding of the role of

vegetated coastal habitats in sequestering CO2 Front

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coral-algal phase shifts Implications for global reef status

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Millar A J K 2007 The Flindersian and Peronian Provinces

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consequences of consideration of permanence leakage and

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Nedzarek A and S Rakusa-Suszczewski 2004 Decomposition

of macroalgae and the release of nutrient in Admiralty Bay

King George Island Antarctica Polar BioSci 17 26ndash35

Nellemann C E Corcoran C M Duarte L Valdes C De

Young L Fonseca and G Grimsditch 2009 A rapid

response assessment United Nations Environment

Programme GRID-Arendal

Nelson W A 2009 Calcified macroalgaemdashcritical to coastal

ecosystems and vulnerable to change A review Mar

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Nemani R R and others 2003 Climate-driven increases in

global terrestrial net primary production from 1982 to 1999

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Nikula R C I Fraser H G Spencer and J M Waters

2010 Circumpolar dispersal by rafting in two subantarctic

kelp-dwelling crustaceans Mar Ecol Prog Ser 405 221ndash

230 doi103354meps08523

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Geoscience Australia Available from httpwwwozcoasts

govaunrm_rpthabitat_extentjsp

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carbonrdquo emissions from conversion and degradation of

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hotspots Why is there high species richness and

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1011813627613

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biological communities on the shallow South East

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237ndash245 doi101016jecss200906023

Rattray A D Ierodiaconou J Monk V L Versace and L J

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(Rhodophyta) primary production due to the deposition

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Rubin E S H Mantripragada A Marks P Versteeg and J

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Sabine C L and others 2004 The oceanic sink for

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Acknowledgments

This research is undertaken by the CSIRO Flagship Marine amp Coastal

Carbon Biogeochemical Cluster (Coastal Carbon Cluster) with fundingfrom the CSIRO Flagship Collaboration Fund The Coastal Carbon Clus-ter is an Australian research program designed to foster vital scientific

research to strengthen our low carbon economy and prevent futureexcessive greenhouse gas emissions and improve methods in estimating

how much carbon is stored in coastal areas The Cluster is composed ofseven Australian Universities and one Australian Research Institute work-ing with the CSIROrsquos Wealth from Oceans Flagship Funding support

was also provided by an Australian Research Council DECRA Fellowship(DE130101084) to PIM

Submitted 30 November 2014

Revised 7 May 2015

Accepted 1 June 2015

Associate editor Thomas Anderson

Hill et al Can macroalgae contribute to blue carbon

18