Knowledge gaps in tropical Southeast Asian seagrass systems

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Knowledge gaps in tropical Southeast Asian seagrass systems

Jillian Lean Sim Ooi a,b,c,d,*, Gary A. Kendrick a,d, Kimberly P. Van Niel b,d, Yang Amri Affendi a,e

a School of Plant Biology, Faculty of Natural and Agricultural Sciences, The University of Western Australia, Crawley, 6009 Western Australia, Australiab School of Earth and Environment, Faculty of Natural and Agricultural Sciences, The University of Western Australia, Crawley, 6009 Western Australia, AustraliacDepartment of Geography, Faculty of Arts and Social Sciences, Universiti Malaya, Kuala Lumpur 50603, Malaysiad The UWA Oceans Institute, The University of Western Australia, Crawley, 6009 Western Australia, Australiae Institute of Biological Sciences, Faculty of Science, Universiti Malaya, Kuala Lumpur 50603, Malaysia

a r t i c l e i n f o

Article history:Received 10 March 2010Accepted 19 December 2010Available online 30 December 2010

Keywords:seagrasssedimentruderaltropicalforereefSoutheast AsiaMalaysiaPulau Tinggi

a b s t r a c t

Seagrasses are habitats with significant ecological and economic functions but we have limited knowl-edge of seagrasses in Southeast Asia, the hypothesized centre-of-origin for tropical seagrasses. There havebeen only 62 ISI-cited publications on the seagrasses of Southeast Asia in the last three decades and mostwork has been in few sites such as Northwest Luzon in the Philippines and South Sulawesi in Indonesia.Our understanding of the processes driving spatial and temporal distributions of seagrass species here hasfocussed primarily on backreef and estuarine seagrass meadows, with little work on forereef systems. Weused Pulau Tinggi, an island off the southeast coast of Peninsular Malaysia, as an example of a subtidalforereef system. It is characterized by a community of small and fast growing species such as Halophilaovalis (mean shoot density 1454.6 � 145.1 m−2) and Halodule uninervis (mean shoot density 861.7 � 372.0m−2) growing in relatively low light conditions (mean PAR 162.1 � 35.0 mmol m�2 s�1 at 10 m depth to405.8 � 99.0 mmol m�2 s�1 at 3 m water depth) on sediment with low carbonate (mean 9.24 � 1.74percentage dry weight), organic matter (mean 2.56 � 0.35 percentage dry weight) and silt-clay content(mean 2.28 � 2.43 percentage dry weight). The literature reveals that there is a range of drivers operatingin Southeast Asian seagrass systems and we suggest that this is because there are various types ofseagrass habitats in this region, i.e. backreef, forereef and estuary, each of which has site characteristicsand ecological drivers unique to it. Based on our case study of Pulau Tinggi, we suggest that seagrassesin forereef systems are more widespread in Southeast Asia than is reflected in the literature and thatthey are likely to be driven by recurring disturbance events such as monsoons, sediment burial andherbivory.

� 2010 Elsevier Ltd. All rights reserved.

1. Introduction

Seagrass habitats are important in maintaining ecological andeconomic functions (Costanza et al., 1997; Hemminga and Duarte,2000; Gullstrom et al., 2002; Duarte et al., 2005; Nyunja et al.,2009) but globally they are threatened by human impacts relatedto coastal development and increased pressures from artisanal fish-eries (Fortes,1988; Duarte, 2002;Waycott et al., 2009). Past efforts todetermine trajectories of seagrasses worldwide have drawn on datafrom the temperate North Atlantic, tropical Atlantic, Mediterraneanand the temperate Southern Oceans (Waycott et al., 2009). Incontrast, there is very little quantitative data, especially long time

series, from the tropical Indo-Pacific, inparticular Southeast Asia andeastern Africa (Gullstrom et al., 2002; Waycott et al., 2009). Ourunderstanding of the processes driving spatial and temporal distri-butions of seagrass species in these regions is rudimentary and hasfocused primarily on estuarine and backreef/lagoonal seagrassmeadows (Klumpp et al., 1993; Vermaat et al., 1995; Agawin et al.,1996; Duarte et al., 1997,2000; Stapel et al., 1997; Bach et al., 1998;Nakaoka and Aioi, 1999; Terrados et al., 1999; Holmer et al.,2001b,2006; Tanaka and Nakaoka, 2006; Vonk et al., 2008b), withlittle work on forereef systems.

Southeast Asia has the greatest diversity of seagrasses within theIndo-Pacificbiogeographic region,withupto17of the24 Indo-Pacificspecies found here. More importantly, Southeast Asia has beenhypothesized to be the centre-of-origin for tropical seagrasses (Shortet al., 2001). This biodiversity hotspot also coincides with the CoralTriangle, a centre of marine diversity for various taxa of molluscs,crustaceans, reef fishes, and scleractinian corals (Hoeksema, 2007),

* Corresponding author. The University of Western Australia, 35 Stirling Hwy,Perth, Western Australia 6009, Australia.

E-mail address: [email protected] (J.L.S. Ooi).

Contents lists available at ScienceDirect

Estuarine, Coastal and Shelf Science

journal homepage: www.elsevier .com/locate/ecss

0272-7714/$ e see front matter � 2010 Elsevier Ltd. All rights reserved.doi:10.1016/j.ecss.2010.12.021

Estuarine, Coastal and Shelf Science 92 (2011) 118e131


which further underlines its significance to us not just for seagrassesbut for the whole complex of marine biodiversity.

In this paper, we have three aims. First, we characterise the bodyof work on seagrasses in Southeast Asia through a review of theliterature. Second,wediscusswhat is knownabout ecological driversof seagrasses in Southeast Asia and focus on one major knowledgegap in the literature, the forereef seagrass system, dominated byruderal fast growing species. Third, we provide baseline data fora forereef system in Pulau Tinggi, Malaysia, outlining the differencesfrom the morewell-studied backreef and lagoonal seagrass systems.

2. Methods

2.1. Literature survey

A search of ISI-cited publications was performed on the Web ofScience in October 2009 and January 2010 by using the keywords“seagrass” and “Southeast Asia” as well as individual country names(Indonesia, Philippines, Thailand, Malaysia, Singapore, Vietnam,Myanmar, Cambodia and Brunei Darussalam). The records werefurther filtered to exclude those in which seagrasses were not the

main subjects of the study. The literature survey is presentedaccording tobreakdownbycountry, yearandhabitat.Here, ahabitat isdefined as amajor ecological area inhabited by a seagrass communityand is based on the model of Short et al. (2007) for the tropical Indo-Pacific bioregion. Three major seagrass habitats were used in thisstudy: estuaries (includesmudflats), backreefs (includes reefflats andlagoons landward of the reef crest) and forereefs (the area seaward ofthe reef; the term ‘deep coastal’was used in Short et al., 2007). Not allauthorswere specific about the type of habitats inwhich theyworkedandwhere therewasuncertainty, thesepublicationswere categorizedas “unknown”. In cases where a publication spanned 2e3 differentcountries, it was listed separately for each country and thereforecountedmore than once in the breakdown of publications by country.

2.2. Case study site: Pulau Tinggi

The field survey was conducted from 15 April to 15 May 2009 inpulau Tinggi (pulau¼ island), a continental island located 12 km offthe southeast coast of Peninsular Malaysia. Its seagrass meadowsare predominantly subtidal and occur in the forereef zone, i.e. onthe seaward side of the coral platforms and patch reefs (Fig. 1).

Fig. 1. Location of spot collection points in the seagrass meadows of Pulau Tinggi, off the south east coast of Peninsular Malaysia. Numbered points have seagrass. A, B, and C arewhere there was no seagrass and only sediment samples were collected.

J.L.S. Ooi et al. / Estuarine, Coastal and Shelf Science 92 (2011) 118e131 119


Coral reefs fringing the island are unusual as they are predomi-nantly found in shallow waters (<8 m), unlike most other reefs onthe east coast of Peninsular Malaysia (Harborne et al., 2000).Presently, the coral diversity of Pulau Tinggi is 142 scleractinianhard corals (De Silva et al., 1984; Harborne et al., 2000). The PulauTinggi group of islands were gazetted as a Marine Park in 1994under the Fisheries Act 1985 (Amended, 1993) and thereafter,waters up to 2 nautical miles from the lowest lowwater mark camewithin the jurisdiction of the Department of Marine Parks,Malaysia.

2.2.1. SeagrassTow video (sensu Holmes et al., 2007) was used to characterize

seagrass distribution where transects covered the range of sedi-mentary environments, water depth and bathymetric features.Sedimentary environments were sampled based on the north-easterly subsurface currents. Water depth between 3 and 10 mwastargeted for subtidal seagrasses, with sparser sampling in deeperwaters to 20m to test for deep water seagrasses (e.g. Halophiladecipiens). Bathymetric features from the maritime charts, such asgullies, submerged reefs and shoals were targeted for inclusion inthe tow video transects. Tow video was then point sub-sampled atshort distances (2e5 m) within the seagrass beds and longerdistances (10e40 m) outside seagrass beds. At each point, sea-grasses were identified to the genus level and other marine benthicelements were recorded (sediment, other biota, etc) to providea continuous spatial dataset for the study area. For this paper, wereported only seagrass presence in map form using ArcGIS 9.3.

Spot sampling was conducted at 26 locations with and withoutseagrass. At each location, four 100 mm diameter cores weresampled for seagrass biomass and density. A visual survey overapproximately 100e200 m2 area identified all seagrass species ateach sampling location. These were sorted, identified and pressedfor further taxonomic study using published guides (Kuo and denHartog, 2001; Waycott et al., 2004; Edang et al., 2008). Shootdensity and biomass were determined for species found in thecores. Shoots (above-ground components) were counted andseparated from rhizomes and roots (belowground components).Both aboveground and belowground components were spun ina lettuce dryer for approximately 30 s, dried for 24 h at 60 �C in anoven and reweighed as dry weight.

2.2.2. Sediment and lightSediment cores were collected in each of the 26 locations:

a 25 cm long and 5 cm diameter core was used to collect sedimentfor grain size analysis; a 50 ml Terumo syringe was used to collectsediment cores for organic matter and carbon analysis. For grainsize analysis, samples were rinsed in fresh water and dry-sieved for15 min through a series of graded sieves into Wentworth scalefractions of gravel (>2 mm), sand (63 mme2 mm) and silt-clay(<63 mm), after which dry weights were obtained for each fraction.Organic matter was determined using the loss-on-ignition methodin which samples were combusted for 4 h at 450 �C in a mufflefurnace and expressed as a percentage of dry weight loss. Totalcarbon and organic carbon were determined in a CN ElementalAnalyser. Samples for organic carbon analysis were decarbonatedusing HCl vapours for 48 h, precipitated in concentrated HCl, ovendried at 60 �C, ground down to a fine grain, and combusted at950 �C for approximately 5 min in a CN Analyzer (Yamamuro andKayanne, 1995). All carbon content was expressed as a percentageof dry weight. Inorganic carbon was estimated by subtractingorganic carbon from total carbon.

Light loggers (HOBO Onset) in watertight housing weredeployed in seagrass beds at water depths of 3.0, 4.5, 6.0, 10.0 and14.0 m (corrected to chart datum) to measure photosynthetically

active radiation (PAR) between 23rd April and 11th May 2009.These were also referenced to a light logger on land to obtainsurface irradiance (% SI).

3. Results

3.1. Literature survey

Consistent research on seagrasses in Southeast Asia beganapproximately in the mid-1990s (Fig. 2) and since then, 62 ISI-citedpublications have been produced. Most of this work was located inIndonesia (24 papers) and the Philippines (22 papers) (Fig. 3) witha concentration on specific areas. In Indonesia, 15 of the 24 paperswere located in Southwest Sulawesi; in the Philippines, 18 of the 22papers were located in Northwest Luzon (Table 1). The number ofseagrass studies on backreefs was many times more than those inother habitats (Fig. 4). Of the 107 sites reported in the literature,70% were based on backreef systems, 20% on estuaries, 1% onforereefs while 9% were unknown.

The seagrass flora of Southeast Asia is characterised by highdiversity. There are approximately 59 species worldwide, of whichseventeen are found in Southeast Asia (Green and Short, 2003).They range from the small and short-lived Halophila spp. to thelarge and persistent Enhalus acoroides. Size is an indicator of plantstrategy because it displays an allometric scaling to productivity(Duarte, 1991a; Vermaat et al., 1995). Small species such as

Fig. 2. Total number of ISI Web of Science publications on Southeast Asian seagrassesbetween 1986 and 2009 according to breakdown by blocks of 5 years.

Fig. 3. Total number of ISI Web of Science publications on Southeast Asian seagrassesbetween 1986 and 2009 according to breakdown by country.

J.L.S. Ooi et al. / Estuarine, Coastal and Shelf Science 92 (2011) 118e131120


Table

1Studyarea

,tax

on(w

ithdom

inan

celeve

lsas

specified

insourcereferences),h

abitat,h

ypothesized

drive

r,leve

lofs

tudy,an

dsourceof

ISI-citedpublicationson

Southea

stAsian

seag

rasses

betw

een19

86an

d20

09.Lev

elsof

study

aremolecule

(e.g.e

cophy

siolog

ical

andbioc

hem

ical

processes),ramet

(e.g.shoo

tan

droot

mea

suremen

ts),canop

y(e.g.shoo

tden

sity,b

iomass,co

ver),andlandscap

e(e.g.p

atch

shap

e,size

,fragm

entation

).In

caseswherewater

dep

this

not

specified

butEn

halusacoroide

sis

present,itis

designated

asa‘shallow’area

.

Studyarea

Taxo

n(1

,2,3,order

ofdom

inan

ce)

Hab

itat

Drive

rLe

velof

study

Source

Malay

sia

TelukKem

ang,

Neg

eriSe

mbilan

HO,H

U,H

DBackree

f,1.5e

2m

dep

thN.R.(new

reco

rdof

H.d

ecipiens)

Ram

etJapar

Sidik

etal.,19

95

Kem

aman

,Teren

ggan

ue

Estuary,

intertidal

Environmen

talforcing-reproduction

ofH.beccarii

Ram

etMuta

Harah

etal.,19

99

Malay

sia

N.R.

N.R.

N.R.(description

ofH.u

nine

rvis

andH.p

inifo

lia)

Ram

etJapar

Sidik

etal.,19

99

Port

Dickson

,Neg

eriSe

mbilan

CS

Backree

f,0.5e

2m

dep

thLigh

teffectson

C.serrulaphotosyn

thesis

Molecule

Abu

Hen

aet

al.,20

01

Pengk

alan

Nan

gka,

Kelan

tan

HB

Estuary,

intertidal

N.R.(reproductionof

H.b

eccarii)

Ram

etMuta

Harah

etal.,20

02

Malay

sia

N.R.

N.R.

N.R.(review

ofdistribution

)N.R.

Japar

Sidik

etal.,20

06Pu

lauGay

a,Sa

bah

HU,C

S,CR

Backree

f,0.7m

dep

thSe

dim

ente

silt-clay&turbidity

Ram

etecanop

yFree

man

etal.,20

08CS,

CRHU,T

H,H

OBackree

f,0.5m

dep

thSe

dim

ente

silt-clay&turbidity

Ram

etecanop

yFree

man

etal.,20

08

Philippines

Silaqu

iisland,n

orthwestLu

zon

EA,C

S,TH

,HU

Ree

fflat,shallow

Urchin

grazing

Can

opy

Klumppet

al.,19

93TH

1,E

A2,C

R3,C

S,SI,H

U,H

ORee

fflat,0

.5e3m

dep

thInterspecificinteraction

Ram

etVermaa

tet

al.,19

95

TH1,E

A2,C

R3,C

S,SI,H

U,H

ORee

fflat,sheltered,0

.8m

dep

thNutrients

eN

andPlim

itationon

T.he

mprichii,

E.acoroide

san

dC.

serrulata

Moleculeerametecanop

yAga

win

etal.,19

96

TH1,E

A2,C

R3,C

S,SI,H

U,H

ORee

fflat,0

.8m

dep

thSe

dim

ent-bu

rial

Can

opy

Duarte

etal.,19

97TH

1,E

A2,C

R3,C

S,SI,H

U,H

ORee

fflat,0

.8m

dep

thN.R.(flow

eringfreq

uen

cy)

Can

opy

Duarte

etal.,19

97TH

1,E

A2,C

R3,C

S,SI,H

U,H

ORee

fflat,<

3m

dep

thSe

dim

ente

siltationan

dlig

htpen

etration

Can

opy

Bachet

al.,19

98

TH1,E

A2,C

R3,C

S,SI,H

U,H

ORee

fflat,0

.8m

dep

thN.R.(be

lowgrou

ndbiom

ass)

Rhizosphere

Duarte

etal.,19

98TH

1,E

A2,C

R3,C

S,SI,H

U,H

ORee

fflat,1

.5m

dep

thSe

dim

ent-an

oxia

Can

opy

Terrad

oset

al.,19

99TH

1,E

A2,C

R3,C

S,SI,H

U,H

ORee

fflat,1

mdep

thSe

dim

ente

Nan

dPlim

itation

onE.

acoroide

sMoleculeerametecanop

yTe

rrad

oset

al.,19

99

TH1,E

A2,C

R3,C

S,SI,H

U,H

ORee

fflat,0

.8m

dep

thInterspecificco

mpetition

Can

opy

Duarte

etal.,20

00TH

1,E

A2,C

R3,C

S,SI,H

U,H

ORee

fflat,0

.8m

dep

thEn

vironmen

talforcing-T.

hemprichii,

E.acoroide

san

dC.

serrulata

Moleculeeramet

Aga

win

etal.,20

01

TH1,E

A2,C

R3,C

S,SI,H

U,H

ORee

fflat,0

.5m

dep

thSe

dim

ent-siltation,p

orew

ater

sulphideon

C.rotund

ata

Ram

et-canop

yHalunet

al.,20

02

TH,E

A,C

R,C

SRee

fflat,shallow

N.R.(sedim

entdep

osition

andproduction)

Can

opy

Gacia

etal.,20

03

THRee

fflat,shallow

Burial

effectson

seed

san

dseed

lings

Ram

etRollónet

al.,20

03EA

Ree

fflat,shallow

Burial

effectson

seed

san

dseed

lings

Ram

etRollónet

al.,20

03TH

,CS

Ree

fflat,1

.5m

dep

thLigh

tMoleculeeramet

Gacia

etal.,20

05Sa

ntiag

oIsland,

northwestLu

zon

EA,C

S,TH

,HU

Ree

fflat,shallow

Urchin

grazing

Can

opy

Klumppet

al.,19

93CR,E

A,H

UCoral

rock

withsiltov

erlaye

r,1m

dep

thInterspecificinteraction

Ram

etVermaa

tet

al.,19

95

TH1,E

A2,C

R3,C

S,SI,H

U,H

ORee

fflat,e

xposed

,0.6

mdep

thNutrients

eN

andPlim

itation

onT.

hemprichii,

E.acoroide

san

dC.

serrulata

Moleculeeramet

Aga

win

etal.,19

96

EA,C

S,HU,H

O,T

H,

Ree

fflat,<

1.0m

dep

thSe

dim

ente

siltationan

dlig

htpen

etration

Can

opy

Bachet

al.,19

98

TH1,E

A2,C

R3,C

S,SI,H

U,H

ORee

fflat,e

xposed

,0.6

mdep

thN.R.(be

lowgrou

ndbiom

ass)

Rhizosphere

Duarte

etal.,19

98EA

,CS,

CR,T

H,H

U,H

ORee

fflat,<

2.0m

dep

thSe

dim

ente

siltationan

dlig

htpen

etration

Can

opy

Bachet

al.,19

98

eRee

fflat,<

1.0m

dep

thSe

dim

ente

Nan

dPlim

itation

onE.

acoroide


yTe

rrad

oset

al.,19

99

(con

tinu

edon

next

page)


Author's personal copyTa

ble

1(con

tinu

ed)

Studyarea

Taxo

n(1

,2,3,order

ofdom

inan

ce)

Hab

itat

Drive

rLe

velof

study

Source

TH,E

A,C

R,C

SRee

fflat,shallow

N.R.(sedim

entdep

osition

andproduction)

Can

opy

Gacia

etal.,20

03

Cap

eBolinao

,northwestLu

zon

EA,CS

Ree

fflat,h

ighly

silted

area

,<0.5m

Sedim

ente

siltationan

dlig

htpen

etration

Can

opy

Bachet

al.,19

98

TH1,E

A2,C

R,C

S,SI,H

U,H

OEstuaryan

dreef

lago

on,

intertidal

to3m

dep

thSe

dim

ent-siltation

Can

opy

Terrad

oset

al.,19

98

eHighly

silted

area

,<1.0m

Sedim

ente

Nan

dPlim

itation

onE.

acoroide


yTe

rrad

oset

al.,19

99

TH1,E

A2,C

R,C

S,SI,H

U,H

ORee

fflat,<

3.0m

dep

thNutrientallocation

toplantparts

Ram

etTe

rrad

oset

al.,19

99TH

,EA

N.R.

N.R.(propag

ule

dispersalo

fT.

hemprichiian

dE.

acoroide

s)Ram

etLacapet

al.,20

02

CS,

CR,E

ASh

allow

N.R.(sedim

entdep

osition

andproduction)

Can

opy

Gacia

etal.,20

03

TH1,E

A2,C

R,C

S,SI,H

U,H

ORee

fflat,shallow

Patchfrag

men

tation

onE.

acoroide

sreproduction

Can

opye

landscap

eVermaa

tet

al.,20

04

Dacoisland,

offNeg

rosOrien

tal

eRee

fflat,shallow

Tidal

exposure

&day

length

onE.

acoroide

sRam

etEstacion

and

Fortes,1

988

Neg

rosOrien

tal

TH,E

A,C

R,C

S,HU,H

P,SI,H

ORee

fflat,shallow

N.R.(leaf

productivity,

biom

ass)

Moleculeerametecanop

yerh

izosphere

Tomasko

etal.,19

93

Puerto

Galera,

Mindoroisland

TH1,E

A,C

R,C

S,SI,H

U,H

ORee

fflat,<

3.0m

dep

thSe

dim

ent-siltation

Can

opy

Terrad

oset

al.,19

98TH

1,E

A,C

R,C

S,SI,H

U,H

ORee

fflat,<

3.0m

dep


toplantparts

Ram

etTe

rrad

oset

al.,19

99Pa

lawan

island

TH,E

A,C

R,C

S,SI,H

U,H

O<3.0m

dep

thSe

dim

ent-siltation

Can

opy

Terrad

oset

al.,19

98TH

,EA,C

R,C

S,SI,H

U,H

O,H

O<3.0m

dep


toplantparts

Ram

etTe

rrad

oset

al.,19

99HU,C

S,EA

Shallow

N.R.(sedim

entdep

osition

andproduction)

Can

opy

Gacia

etal.,20

03

EASh

allow

N.R.(sedim

entdep

osition

andproduction)

Can

opy

Gacia

etal.,20

03

Vietn

amNhaTran

gTH

Highen

ergy

coast,sh

allow

N.R.(sedim

entdep

osition

andproduction)

Can

opy

Gacia

etal.,20

03

EAHighen

ergy

coast,sh

allow

N.R.(sedim

entdep

osition

andproduction)

Can

opy

Gacia

etal.,20

03

TH,E

AHighen

ergy

coast,sh

allow

N.R.(sedim

entdep

osition

andproduction)

Can

opy

Gacia

etal.,20

03

Gia

Luan

,HaLo

ngBay

HO1,Z

J1,H

DPristineba

y,1.0e

2.0m

dep

thSe

ason

alturbidity

Ram

etecanop

yHuon

get

al.,20

03

Thailand

Talib

ongisland,S

outhwestTh

ailand

TH,E

A,C

R,C

S,SI,H

U,H

O<3.0m

dep

thSe

dim

ent-siltation

Can

opy

Terrad

oset

al.,19

98TH

,EA,C

R,C

S,SI,H

U,H

O<3.0m

dep


toplantparts

Ram

etTe

rrad

oset

al.,19

99EA

,TH,H

O0.5e

1.5m

dep

thSe

dim

ente

sulphideintrusion

Ram

etecanop

yerh

izosphere

Holmer

etal.,20

06TH

,HO,C

R0.3m

dep

thSe

dim

ente

sulphideintrusion

Ram

etecanop

yerh

izosphere

Holmer

etal.,20

06HO

0.8m

dep

thSe

dim

ente

sulphideintrusion

Ram

etecanop

yerh

izosphere

Holmer

etal.,20

06Ban

gRon

g,Ph

uke

tisland,

SouthwestTh

ailand

TH1,E

A,H

U,H

O<3.0m

dep

thSe

dim

ent-siltation

Can

opy

Terrad

oset

al.,19

98TH

1,E

A,H

U,H

O<3.0m

dep


toplantparts

Ram

etTe

rrad

oset

al.,19

99CR,T

H,E

AIntertidal

sandflat

Nutrients

Moleculeecanop

yHolmer

etal.,20

01Haa

dChao

Mai,T

rang,

SouthwestTh

ailand

HO1,C

R,C

S,EA

Intertidal

flat

Herbivo

rye

dugo

nggrazing

Can

opy-landscap

eNak

aoka

andAioi,19

99HO,T

H,E

A,C

R,H

UIntertidal

Intra-

andinterpatch

interaction

Ram

etecanop

yerh

izosphere-

landscap

eNak

aoka

and

Iizu

mi,20

00HO,T

H,E

A,C

S,HU

River

mou

th,<

3m

dep

thSe

dim

entation

andlig

htattenuation

effectson

Cymod

ocea

Ram

etecanop

yTa

nak

aan

dNak

aoka

,200

6CS

Finesand

N.R.(iron

plaqu

eon

C.Serrulataroots)

Ram

etPo

vidisaet

al.,20

09

Ban

PakMen

g,Tran

g,So

uthwestTh

ailand

CS

Finesand

N.R.(iron

plaqu

eon

C.serrulataroots)

Ram

etPo

vidisaet

al.,20

09

Phan

gnga

,So

uthwestTh

ailand

eRiver

mou

th,shallow

N.R.(intern

alnutrientco

ncentration

inE.

acoroide

sMoleculeeramet

Yam

amuro

etal.,20

04

CS,

CR,E

A,S

I,HU,H

P,HO

River

mou

th,<

2m

dep

thSe

dim

entation

andlig

htattenuation

effectson

Cymod

ocea

Ram

etecanop

yTa

nak

aan

dNak

aoka

,200

6



Table

1(con

tinu

ed)

Studyarea

Taxo

n(1

,2,3,order

ofdom

inan

ce)

Hab

itat

Drive

rLe

velof

study

Source

Indonesia

Baran

gLo

mpo,

SouthwestSu

lawesi

TH,E

ARee

fflat,carbo

natesand,<

1m

dep

thN.R.(sedim

entan

dporew

ater

nutrients)

N.R.

Erftem

eijeran

dMiddlebu

rg,1

993

Ree

fflat,carbo

natesand,<

1m

dep

thN.R.(primaryproductionrates)

Ram

etErftem

eijeret

al.,19

93TH

,EA

Ree

fflat,carbo

natesand,<

1m

dep

thTidal

exposure

&water

motion

Ram

etecanop

yErftem

eijeran

dHerman

,199

4TH

,EA

Ree

fflat,carbo

natesand,<

1m

dep

thNutrients

Ram

etErftem

eijeret

al.,19

94TH

,EA

Ree

fflat,carbo

natesand,<

1m

dep

thN.R.(nutrientcy

cling)

Molecule

Erftem

eijeran

dMiddelbu

rg,1

995

TH,E

A,C

RCarbo

natesandan

dco

ral

rubb

le,intertidal

N.R.(nutrientuptake

byT.

hemprichii)

Molecule

Stap

elet

al.,19

96

TH,E

A,C

RCarbo

natesandan

dco

ral

rubb

le,intertidal

N.R.(nutrientresorption

)Ram

etStap

elan

dHem

minga

,199

7TH

,EA

Ree

fflat,carbo

natesand,<

1m

dep

thTidal

exposure

effectson

T.he

mprichii

biom

assan

dnutrients

Moleculeeramet

Stap

elet

al.,19

97

TH1,E

ARee

fflat,carbo

natesand,<

1m

dep

thN.R.(nitroge

nretention

inT.

hemprichii)

Ram

etStap

elet

al.,20

01e

Coa

rsecarbon

ates,1

0e30

mdep

thN.R.(new

speciesH.sulaw

esii)

Ram

etKuo,

2007

Langk

aiisland,

SouthwestSu

lawesi

eRee

fflat,carbo

natesand,

intertidal

N.R.(nutrientuptake

byT.

hemprichii)

Molecule

Stap

elet

al.,19

96

HO

Forereef,1

2e16

mdep

thLigh

teffectson

primary

productionof

H.o

valis)

Moleculeeramet

Erftem

eijeran

dStap

el,1

999

eCoa

rsecarbon

ates,1

0e30

mdep

thN.R.(new

speciesH.sulaw

esii)

Ram

etKuo,

2007

Gusu

ngTa

llang,

SouthwestSu

lawesi

EACoa

stal

mudflat,

terrigen

ousmud,<

1m

dep

thN.R.(primaryproductionrates)

Ram

etErftem

eijeret

al.,19

93

EACoa

stal

mudflat,

terrigen

ousmud,<

1m

dep

thTidal

exposure

&water

motion

Ram

etecanop

yErftem

eijeran

dHerman

,199

4EA

Coa

stal

mudflat,

terrigen

ousmud,<

1m

dep

thN.R.(nutrientcy

cling)

Molecule

Erftem

eijeran

dMiddelbu

rg,1

995

EA1,T

HSa

ndyterrigen

ousmud,

intertidal

mudflat

N.R.(nutrientuptake

byT.

hemprichii)

Molecule

Stap

elet

al.,19

96

EA1,T

HSa

ndyterrigen

ousmud,

intertidal

mudflat

N.R.(nutrientresorption

)Ram

etStap

elan

dHem

minga

,199

7Bon

eBatan

gisland,

SouthwestSu

lawesi

TH,H

U,C

RRee

fflat

N.R.(orga

nic

Nuptake

rates)

Molecule

Von

ket

al.,20

08a

TH,H

U,C

R,H

ORee

fflat

Urchin

herbivo

ryRam

etecanop

yVon

ket

al.,20

08b

TH,H

U,C

R,E

A,H

ORee

fflat

N.R.(N

cycling)

Ram

etecanop

yVon

kan

dStap

el,2

008

TH,H

U,C

R,S

IRee

fflat

N.R.(root

arch

itecture)

Ram

etKiswaraet

al.,20

09e

Forereef,C

oarsecarbon

ates,1

0e30

mdep

thN.R.(new

speciesH.sulaw

esii)

Ram

etKuo,

2007

Hog

aIsland,W

akatob

iPa

rk,

Southea

stSu

lawesi

TH,E

A,C

R,H

OIntertidal

N.R.(hab

itat

complexity

and

shrimpco

mmunities)

Can

opy

Unsw

orth

etal.,20

07

TH,E

A,C

R,H

OIntertidal

N.R.(scarid

fish

herbivo

ry)

Can

opy

Unsw

orth

etal.,20

07Se

laya

rgrou

pof

islands,

South

Sulawesi

EA,T

H,C

S,CR,S

I,HU,H

P,HO,T

C<1.0e

7m

dep

thN.R.(hea

vymetalsin

seag

rasses)

Ram

etNienhuis,1

986

TH,E

A,C

R<2m

dep

thN.R.(productionan

dco

nsu

mption

rates)

Moleculeeramet

Lindeb

oom

and

Sandee

,198

9Ta

kaBon

eRatearch

ipelag

o,So

uth

Sulawesi

EA,T

H,C

S,CR,S

I,HU,H

P,HO,T

C<1.0e

7m

dep

thN.R.(hea

vymetalsin

seag

rasses)

Ram

etNienhuis,1

986

HU1,H

O1.25

e7.45

mdep

thN.R.(productionan

dco

nsu

mption

rates)

Moleculeeramet

Lindeb

oom

and

Sandee

,198

9Ta

mbu

nan

island,

offKom

odoisland

EA,T

H,C

S,CR,S

I,HU,H

P,HO,T

C<1.0e

7m

dep

thN.R.(hea

vymetalsin

seag

rasses)

Ram

etNienhuis,1

986

TH1,E

A<1.0m

dep

thN.R.(productionan

dco

nsu

mption

rates)

Moleculeeramet

Lindeb

oom

and

Sandee

,198

9Sa

ngg

arBay

,Sumba

waisland

EA,T

H,C

S,CR,S

I,HU,H

P,HO,T

C<1.0e

7m

dep

thN.R.(hea

vymetalsin

seag

rasses)

Ram

etNienhuis,1

986

HU,S

I<1.3dep

thN.R.(productionan

dco

nsu

mption

rates)

Moleculeeramet

Lindeb

oom

and

Sandee

,198

9Ban

tenBay

,WestJava

EA1,T

H,C

R,C

S,HU,S

I,HM

Coral

deb

ris,sand-m

uddy

subs

trate

N.R.(seag

rass

spatial

datab

asedev

elop

men

t)Can

opy-landscap

eDou

venet

al.,20

03

EAMudto

coralsu

bstrate,

<1m

dep

thTu

rbidity&ep

iphytes

Ram

etKiswaraet

al.,20

05CR,C

S,HU,S

I,EA

,TH

Mudto

coralsu

bstrate,

<1m

dep

thN.R.(root

arch

itecture)

Ram

etKiswaraet

al.,20

09

(con

tinu

edon

next

page)



Halophila spp., Halodule spp. and Cymodocea spp. are fast growing,have high growth and turnover rates, and low longevity (Duarte,1991a; Hillman et al., 1995; Duarte and Chiscano, 1999) (Table 2).They are regarded as ruderal species in seagrass communities. Incontrast, climax species such as Thalassia hemprichii and Enhalusacoroides are relatively large, slow-growing and long-lived(Vermaat et al., 1995). These species grow either in monospecificstands or in dense multispecific meadows with high spatialcomplexity. In the latter, larger forms such as Thalassia hemprichiiand Cymodocea species (mean leaf height 15e20 cm) are thecanopy formers, while Halodule (w10 cm) and Halophila (w5 cm)occur in the understory. If E. acoroides occurs in these mixedmeadows, it extends upward to around 60 cm (Vermaat et al., 1995)and is akin to emergent tree species in terrestrial forests.

3.2. Case study site: Pulau Tinggi

Pulau Tinggi and its surrounding islands are ringed by fringingreefs (Fig. 1). The largest reefs extend to around 180 m from shore,but most measure less than 100 m across. Subtidal seagrassmeadows were restricted to the southwestern shores betweenSebirah Besar in the north west and Tanjung Mali in the south eastincluding extensive, well-established meadows between PulauSimbang, Mentigi, Naga Kechil and Naga Besar to the south (Fig. 1).This strong geographically restricted distribution appears to belinked to the direction of monsoonal storms from the northeast,combined with the steep bathymetry found on the north easterncoastline. This results in sand andmud substrata and corals, but notseagrass, along the northern coastline. Seagrasses generallyoccurred seaward of coral reefs between 3 and 10 m water depthcorrected to chart datum but the optimal depth for multispecificmeadows appeared to be between 3 and 6 m. Seagrass and coralreefs were separated by a 5e10 m halo with no vegetation.

3.2.1. SeagrassThe seagrass meadows of Pulau Tinggi occur as subtidal multi-

specific meadows in the forereef zone, covering an area of approxi-mately 3 km2. The most widespread species were Halophila ovalis (R.Ta

ble

1(con

tinu

ed)

Studyarea

Taxo

n(1

,2,3,order

ofdom

inan

ce)

Hab

itat

Drive

rLe

velo

fstudy

Source

Balikpap

anBay

,EastKalim

antan

HU1,H

O,C

RIntertidal

Dugo

ngherbivo

ryCan

opy

deIongh

etal.,20

07Deraw

anisland,e

astKalim

antan

TH,C

R,H

U,H

P,HO/H

Oa,

SISh

allow

N.R.(orga

nic

Nuptake

rates)

Molecule

Evrard

etal.,20

05Le

aseislands,Moluccas

HU1,H

O,T

H,C

R,C

SIntertidal

Dugo

ngherbivo

ryCan

opy

deIongh

etal.,20

07Nan

gBay

,EastAmbo

nisland

TH,C

R,H

U,H

O,E

ASa

ndy-muddytidal

flat

Dugo

ngherbivo

ryCan

opy

deIongh

etal.,19

95

Mya

nmar

Bush

byisland,M

yeik

arch

ipelag

oCR1,H

OFinesand,shallow

reef

flat

N.R.S

eagrassdistribution

andinve

ntory

Can

opy-landscap

eNov

aket

al.,20

09

Anneisland,M

yeik

arch

ipelag

oHP

Intertidal

sandba

nk

N.R.S

eagrassdistribution

andinve

ntory

Can

opy-landscap

eNov

aket

al.,20

09

Lampiislan

d(5

sites),

Mye

ikarch

ipelag

oCR,S

I,TH

,HO,H

U,E

ASa

ndyto

finesand,ree

fflat

N.R.S

eagrassdistribution

andinve

ntory

Can

opy-landscap

eNov

aket

al.,20

09

Kyu

nPila,M

yeik

arch

ipelag

oHO,H

UFinesand,ree

fflat

N.R.S

eagrassdistribution

andinve

ntory

Can

opy-landscap

eNov

aket

al.,20

09

Budaisland(3

sites),

Mye

ikarch

ipelag

oHO,C

R,H

U,T

HSa

ndba

nkan

dreef

flat,

intertidal

N.R.S

eagrassdistribution

andinve

ntory

Can

opy-landscap

eNov

aket

al.,20

09

Russel

island,M

yeik

arch

ipelag

oHU

Sand,ree

fflat

N.R.S

eagrassdistribution

andinve

ntory

Can

opy-landscap

eNov

aket

al.,20

09

N.R.¼

not

releva

nt.EA

¼E.

acoroide

s,TH

¼T.

hemprichii,CR¼

C.rotund

ata,

CS¼

C.serrulata,

HU

¼H.u

nine

rvis,H

P¼

H.p

inifo

lia,S

I¼

S.isoe

tifoliu

m,H

O¼

H.o

valis,H

B¼

H.b

eccarii,HD

¼H.d

ecipiens,H

M¼

H.m

inor,

TC¼

T.cilia

tum,Z

J¼

Z.japo

nica.

Backreef 76 sites

Unknown10 sites

Estuary20 sites

Forereef1 site

Fig. 4. Breakdown of sites documented in ISI-cited literature between 1986 and 2009according to habitat. Values in the pie chart are the number of sites in each habitatcategory. Backreef is the zone between reef crest and land. Forereef is the zonebetween reef crest and sea. Estuary includes sites on intertidal mud flats. A site iscategorized as Unknown if there is uncertainty about its habitat.



Br.) Hooker f. and Halodule uninervis (Forsskal) Ascherson. Other co-occurring seagrass species were Cymodocea serrulata (R. Brown)Ascherson, Syringodium isoetifolium (Ascherson) Dandy, Halophilaminor (Zollinger) den Hartog, Halophila decipiens Ostenfeld, and Hal-ophila spinulosa (R. Brown) Ascherson. The only backreef seagrassmeadow occurred at sampling point 21 (Fig. 1). Here, Cymodocearotundata Ehrenberg & Hemprich ex Ascherson and Thalassia hem-prichii (Ehrenberg)Aschersonco-occurred inwater less than1mdeep.

The edge of the seagrass meadows in the forereef zone wererepresented by the species Halophila ovalis and Halodule uninervis(both wide and thin leafed variants). Within 2e5 m of the edge ofthe seagrass, Cymodocea serrulata and Syringodium isoetifoliumbecame more abundant, but were still minor components of theseagrass meadow. At the deeper seaward edge, in 9e10 m depths

Halophila ovalis dominated but was patchy with little biomass. Also,other Halophila species were found at the deeper edge including H.decipiens and H. minor. Although we towed cameras down to25e30m depths, we found no seagrass beyond the 10e12m slopes.The deeper waters were either unvegetated fine sands or sessileinvertebrate communities represented by seawhips and seafanswith few corals.

Halophila ovalis and Halodule uninervis occurred in shootdensities of 159e2451 and 127e2005 shoots m�2, respectively(Table 3). Biomass ranged between 1.6 and 32.0 gm dry weight m�2

for Halophila ovalis shoots, 0.7e38.1 gm dry weight m�2 for Hal-ophila ovalis roots and rhizomes, 2.4e31.5 gm dry weight m�2 forHalodule uninervis shoots, and 6.9e64.9 gm dry weight m�2 for H.uninervis roots and rhizomes.

Table 2Average biological properties of common tropical seagrasses ranging from small colonizing species (Halophila ovalis) to large, persistent species (Enhalus acoroides). Extractedfrom 1Duarte (1991a) and 2Vermaat et al. (1995).

Species Rhizome diameter (mm) Rhizome elongation (cm yr�1) Shoot longevity (yr) Leaf turnover (yr�1)

Halophila ovalis 1.51 574.01 0.21 20.91

Halodule uninervis 1.01 136.51 0.21 13.01

Syringodium isoetifolium 1.31 75.01 1.461 11.01

Cymodocea serrulata 2.01 216.01 1.981 12.11

Thalassia hemprichii 4.01 87.61 >2.02 18.31

Enhalus acoroides 15.01 0.91 >2.02 5.41

Table 3Seagrass and physical characteristics in Pulau Tinggi, southeast Peninsular Malaysia, 15 Aprile15 May 2009.

Mean � standard deviation Minimum-Maximum

Seagrass variables - communitySpecies richness (m�2) 2.00 � 1.00 1.00e4.00Aboveground biomass (g DW m�2) 45.72 � 145.07 3.30e754.20Belowground biomass (g DW m�2) 46.65 � 68.11 2.60e345.60Total biomass (g DW m�2) 92.38 � 209.58 6.40e1099.90Shoot density (m�2) 1869.70 � 936.77 350.20e3336.30

Seagrass variables e by species

Halophila ovalisShoot density (m�2) 1454.57 � 795.47 159.20e2451.30Aboveground biomass (g DW m�2) 11.41 � 8.90 1.60e32.00Belowground biomass (g DW m�2) 14.11 � 10.73 0.7e38.10Total biomass (g DW m�2) 25.53 � 15.53 2.30e56.20

Halodule uninervisShoot density (m�2) 861.67 � 371.91 127.34e2005.60Aboveground biomass (g DW m�2) 11.25 � 5.78 2.36e31.52Belowground biomass (g DW m�2) 31.67 � 19.16 6.89e64.93Total biomass (g DW m�2) 42.91 � 28.56 9.40e88.90

Cymodocea serrulataShoot density (m�2) 95.50 � 100.70 31.83e318.35Aboveground biomass (g DW m�2) 2.98 � 5.00 1.04e5.64Belowground biomass (g DW m�2) 10.50 � 16.89 0.88e35.58Total biomass (g DW m�2) 13.47 � 9.52 2.70e44.20

Syringodium isoetifoliumShoot density (m�2) 439.30 � 291.10 178.28e700.37Aboveground biomass (g DW m�2) 4.46 � 3.77 2.79e6.13Belowground biomass (g DW m�2) 12.83 � 9.45 8.54e17.11Total biomass (g DW m�2) 17.28 � 5.19 11.30e23.20

Physical variables

Water depth (m) 5.19 � 2.37 <1.00e10.72Silt-clay (% DW) 2.28 � 2.43 0.25e10.45Sand (% DW) 92.55 � 6.09 74.02e98.68Gravel (%DW) 5.20 � 6.28 0.40e25.87Organic matter (% DW) 2.56 � 0.35 1.77e3.40Total carbon (% DW) 9.44 � 1.63 4.32e11.18Organic carbon (% DW) 0.22 � 0.38 0.09e2.02Inorganic carbon (% DW) 9.24 � 1.74 4.16e11.00PAR (mmol m�2 s�1) at 3 m (% SI) 405.80 � 98.90 (37.30 � 3.30) 134.90e554.00PAR (mmol m�2 s�1) at 6 m (% SI) 227.60 � 52.60 (20.10 � 1.30) 85.3e312.20PAR (mmol m�2 s�1) at 10 m (% SI) 162.06 � 34.90 (15.00 � 1.50) 65.6e210.00

PAR ¼ photosynthetically active radiation; %SI ¼ percentage surface irradiance.



Simple correlation, although not a positive test of competitiveinteractions, can provide a means of exploring potential interactionbetween species. There were neither large nor significant rela-tionships between any of the species at Pulau Tinggi.

3.2.2. Sediment and lightSediment had a relatively coarse grain size distribution mainly

composed of the sand fraction (63 mme1 mm) (Table 3). The silt-clay fraction ranged from 0.3 to 10.5%. Organic matter ranged from1.8 to 3.4%. Total carbon ranged from 4.3 to 11.2%, which consistedof more inorganic (4.2e11.0%) than organic carbon (0.1e2.0%). Lightdecreased with depth, ranging from a mean of 162.1 mmol m�2 s�1

in 10 me405.8 mmol m�2 s�1 in 3 m. This translated into a range ofsurface irradiance from 15 to 37%, respectively.

4. Discussion

4.1. Seagrasses poorly studied

Publications on seagrasses in Southeast Asia began emergingconsistently only since the mid-1990s (Fig. 2), beginning in Sulawesi,Indonesia. However, the geographical distribution of published sea-grass studies is restricted and 75% of the published literature hascome from locations in Indonesia and the Philippines (Fig. 3). Onlya limited number of sites within these two countries have beenwell-studied, i.e. Northwest Luzon in the Philippines and SouthwestSulawesi in Indonesia (Table 1). Indonesian seagrasses have receivedinterest through Netherland’s aid programmes, mainly for studies onnutrient dynamics, seagrassefauna interactions and taxonomy,phenology and inventory work (Table 1). Philippine seagrasses havebeenwell studied in northern Luzonmostly through EuropeanUnionaid programs, with the literature dominated by studies on sexualreproduction, nutrient dynamics, sediment effects, phenology andbasic biology. In Thailand (9 papers), seagrasses have been studiedmainly for nutrientdynamics, sediment effects anddugongeseagrassinteractions. Knowledge of Malaysian seagrasses (7 papers) isrestricted to seagrass distribution, taxonomy and phenology at a fewlocations. There is even less known of seagrass meadows in Vietnam,Myanmar, Cambodia, Brunei Darussalam and Singapore.

4.2. Ecological drivers in Southeast Asian seagrass systems

Research on ecological drivers in the seagrass systems of South-east Asia has concentrated on sedimentary drivers, followed by light,herbivory and competition (Table 1). Sediment drives plant growththrough nutrient availability, but nutrient limitation varies betweensite and species (Erftemeijer andMiddleburg,1993; Erftemeijer et al.,1994; Agawin et al., 1996; Holmer et al., 2001). However, there isa clear relationship between the amount of silt-clay in sediment andseagrass species richness and biomass: when silt-clay exceeds 15%,species richness and community leaf biomass declines (Terradoset al., 1998). Silt-clay reduces light availability, contributes to sedi-ment organic matter and anoxia, increases sulphur toxicity andchanges nutrient availability (Bach et al., 1998; Freeman et al., 2008;Erftemeijer and Middleburg, 1993; Kamp-Nielsen et al., 2002). Aspecies-specific response to silt-claycontenthas beenobserved, fromthe most to least sensitive: Syringodium isoetifolium > Cymodocearotundata > Thalassia hemprichii > Cymodocea serrulata > Haloduleuninervis > Halophila ovalis > Enhalus acoroides (Bach et al., 1998;Terrados et al., 1998).

Seagrasses may also be affected by dynamic sedimentary envi-ronments created by the highly diverse community of burrowers inseagrass beds (Vonk et al., 2008a). Shrimp mounds measuring20e30 cm inheight occurred inBolinao at a density of 3m�2 (Duarteet al.,1997). Thesemounds impose burial stress on seagrasses. Burial

levels of 2e4 cm result in 50% mortality within 4 months for manyof the common tropical species (Duarte et al., 1997). As a result ofthe variation in size between species, there is a species-specificresponse to burial (Cabaco et al., 2008). For tropical species, thesequence of species from the most sensitive to the least is Halophilaovalis > Thalassia hemprichii > (Cymodocea rotundata, Syringodiumisoetifolium, Halodule uninervis) > Cymodocea serrulata > Enhalusacoroides (Duarte et al., 1997). Tolerance of seagrass to burial is alsolinked to sediment condition. When buried under anoxic sediment,seagrasses are less likely to survive (Halun et al., 2002; Ralph et al.,2006). At the ramet level, sediment burial may be expected to causeseagrasses to develop morphological changes to cope with burialstress i.e. vertical rhizomes and leaf lengthmay be expected to havea positive relationship with sedimentation to escape burial (Duarteet al., 1997). Despite this, not all tropical species respond similarly(see Tanaka and Nakaoka, 2006).

The relationship between light and photosynthesis for SoutheastAsian seagrass systems has beendetermined for intertidal C. serrulata(Abu Hena et al., 2001), deep water H. ovalis (Erftemeijer and Stapel,1999), T. hemprichii-dominated meadows (Erftemeijer et al., 1993)and mixed community meadows (Gacia et al., 2005). Light exertscontrol over the vertical depth limitation of seagrass meadows(Duarte,1991b). Species that are successful indeepor turbidwater aresmall and structurally simple forms such as H. decipiens and H. ovaliswhich have low photosynthetic rates and light requirements and areconsidered shade-adapted. There is evidence that subtidal andshallow/intertidal communities adopt different strategies inresponding to light. For instance, theHalophiladeepwaterpopulationin Sulawesi has a relatively lower light compensation point (33 mmolphotons m�2 s�1) than those in shallow water (50e340 mmolphotons m�2 s�1) (Erftemeijer and Stapel, 1999). However, the influ-ence of light does not extend to all scales. When temporal changes inlight is considered in combination with temperature, rainfall andwater turbulence, there is a strong association with the photosyn-thetic performance of E. acoroides, T. hemprichii and C. rotundata butnot with their growth and abundance (Agawin et al., 2001).

Other likely drivers in Southeast Asian seagrass systems areherbivory and competition. Dugongs graze preferentially on ruderalspecies such as H. uninervis which has high nitrogen and starchcontent (Sheppard et al., 2007) andH. ovaliswhich, althoughnot highin nutrition, occurs in high abundance (Yamamuro and Chirapart,2005). Dugong herds remove whole plants, but complete regrowthof Halophila sp and H. uninervis meadows occurs quickly, rangingfrom 20 days to less than 5 months (Nakaoka and Aioi, 1999;Supanwanid, 1996; de Iongh et al., 1995). Rotational grazing, i.e.seasonal grazing in an area, coincideswith timeswhen belowgroundbiomass andcarbohydrate content in rhizomes are greatest, has beenobserved in intertidalH.uninervismeadowsaround theAru islandsofIndonesia (de Iongh et al., 2007). For dugong grazing to act as amajoragent of disturbance thatmodifies the landscape, large herds need tobe present. Less than 50 individuals are estimated to inhabit the Gulfof Thailand, less than 100 individuals are in theAndaman Sea (Marshet al., 2002), and less than 40 individuals are estimated for the Leaseislands in Indonesia (de Iongh et al., 2007). These are small pop-ulations, especiallywhen compared to those inHervey Bay, Australia,for example, where the population numbers between 600 and 2250dugongs (Marsh et al., 1996). However, seagrass meadows inSoutheast Asia have high abundance of herbivorous fish (Salita et al.,2003). Scaridfish herbivores consume an average of 4 times the dailygrowth of T. hemprichii and E. acoroides (Unsworth et al., 2007).Although this may result in more losses than gains in the seagrasscommunity, depletion does not occur because overgrazing pressureis not continuous through time (Unsworth et al., 2007).

Knowledge of competitive interactions in seagrass systems isthe most limited of all ecological drivers (Table 1). Observations of



competition for light and nutrients between small and large speciesinmultispecific meadows have been suggested (Agawin et al., 1996;Duarte et al., 1997; Bach et al., 1998), but there has been only onedirect test of competition. In the Philippines, interspecific compe-tition was not apparent as a driving force because the removal of T.hemprichii did not result in a reduction of extant species asexpected (Duarte et al., 2000). The differential partitioning of rootsbelowground may explain this lack of response. Thus, althoughthese plants co-occur in above ground space, they are not truecompetitors in the sense defined by Grime (1977), because they donot share the same belowground space. The study of how roots aredistributed belowground can provide insight into the processesthat produce multispecific meadows in Southeast Asia.

The literature reveals that there is a range of biotic and abioticdrivers operating in Southeast Asian seagrass systems and this ispresumably because there are various types of seagrass habitats inthis region, i.e. backreef, forereef and estuary, each of which has sitecharacteristics and ecological drivers unique to it.

4.3. Very limited knowledge of forereef systems

Seagrass communities on backreef systems have received themost attention, amounting to 71% of the total sites reported in theliterature (Fig. 4, Table 1). Backreefs have high carbonate sediment(Erftemeijer, 1994) and are usually dominated by slower-growingspecies such as Thalassia hemprichii and Enhalus acoroides (Table 1).Seagrasses in estuaries were much less reported than those onbackreefs (18%) and came mainly from studies in southwestThailand where extensive tidal mudflats dominated by seagrasses

occur in large estuaries fringed by mangroves. Here, the mostcommon research theme was sediment and nutrient effects onseagrasses (Holmer et al., 2001, 2006; Yamamuro et al., 2004;Tanaka and Nakaoka, 2006).

Forereef systems were the most poorly represented in theliterature. We found one publication on a forereef habitat, whichwas on the primary productivity of Halophila ovalis beds inSouthwest Sulawesi (Erftemeijer and Stapel, 1999). These mono-specific beds occurred in depths exceeding 10 m under conditionsof low light and unconsolidated sediment. Here, environmentalconditions were apparently sufficiently different from those inother habitats for the seagrasses to develop unique morphologicalcharacteristics, leading to a suggestion that these were, in fact,a new species, Halophila sulawesii sp. nov. (Kuo, 2007). Many moreof these types of forereef meadows were said to occur aroundislands in Southwest Sulawesi but that little was known of them(Erftemeijer and Stapel, 1999). This is a scenario which hasremained very much the same a decade later.

4.4. Pulau Tinggi as a representative forereef system

Here we use Pulau Tinggi, Malaysia, as an example of a forereefsystem. This seagrass system is dominated by ruderal or colonizingspecies such as Halodule uninervis and Halophila ovalis (Table 3).The shoot density, aboveground and belowground biomass of H.ovalis were approximately two orders of magnitude greater thanmost of those recorded in other multispecific meadows in South-east Asia (Table 4). In Bolinao, Puerto Galera, and El Nido, H. ovalisandH. uninervis are under-storey species found under the canopy of

Table 4Mean shoot density and biomass of selected Southeast Asian seagrasses. All are multispecific meadows except for Langkai island.

Species/Location Shoot density(shoots m�2)

Aboveground biomass(g DW m�2)

Belowground biomass(g DW m�2)

Total biomass(g DW m�2)

Halophila ovalisPulau Tinggi (this study) 1455 � 795 11.4 � 8.9 14.1 � 10.7 25.5 � 15.5Bolinao, Phil.a,b,c,d,e 12e388 3.1 0.1e0.9 0.2Pto Galera, Phil.d e 3.9 e e

El Nido, Phil.d e 0.6 e e

Flores Sea, Indon.f 69 � 117 e e e

Langkai island, Indon.g 1099 � 195 e e 10.93 � 2.65

Halodule uninervisPulau Tinggi (this study) 862 � 372 11.3 � 5.8 31.7 � 19.2 42.91 � 28.7Bolinao, Phil.a,b,c,d,e 8e1064 29.4 2.8e6.7 7.3Pto Galera, Phil.d e 4.9 e e

El Nido, Phil.d e 4.2 e e


Langkai island, Indon.g e e e e

Cymodocea serrulataPulau Tinggi (this study) 96 � 101 3.0 � 5.0 10.5 � 16.9 13.5 � 9.5Bolinao, Phil.a,b,c,d,e 2e214 31.7 e 2.7Pto Galera, Phil.d e 4.3 e e

El Nido, Phil.d 696 � 767 5.7 e e

Flores Sea, Indon.f e e e e


Syringodium isoetifoliumPulau Tinggi (this study) 439 � 291 4.5 � 3.8 12.8 � 9.5 17.3 � 5.2Bolinao, Phil.a,b,c,d,e 4e396 33.0 1.8e2.1 14.3Pto Galera, Phil.d e 1.5 e e

El Nido, Phil.d e e e e



a Bach et al. (1998).b Vermaat et al. (1995).c Duarte et al. (1997).d Terrados et al. (1998).e Duarte et al. (1998).f Kuriandewa et al. (2003).g Erftemeijer and Stapel (1999).



climax species such as T. hemprichii and E. acoroides (Vermaat et al.,1995). These species occur in backreefs and estuaries, but not inforereef systems (Table 1) because E. acoroides requires very lowtides for surface pollination (Den Hartog and Kuo, 2006) while T.hemprichii is less successful in areas with mobile substratumbecause its seeds do not tolerate burial well (Rollon et al., 2003).The dominance of ruderal species is an indicator of disturbance forclonal organisms such as corals and terrestrial grass (Grime, 1977;Edinger and Risk, 2000). Therefore, the species composition inPulau Tinggi indicates that it is a system with recurring physicaldisturbance.

Forereef systems also occur around many other islands off thesoutheast coast of Peninsular Malaysia (e.g. Pulau Sibu Hujung,Pulau Sibu Kukus and Pulau Besar in Johor; the Seri Buat Archi-pelago in Pahang). These are mostly continental islands withnarrow fringing reefs and a wide but gentle slope towards deepwaters. In Pulau Tinggi, we estimate the ratio of backreef to forereefarea to be 1:6, and we speculate that other continental islands inSoutheast Asia may have similar areas of forereefs suitable forseagrasses. We suggest that seagrasses in forereef systems aremorewidespread in Southeast Asia than is reflected in the literature.

4.4.1. Monsoons and lightThe distribution of seagrass on the sheltered south and south-

western shores of Pulau Tinggi (Fig.1), and their limitation to depthsof less than 10 m, leads us to consider their broad scale distributionto be spatially limited by monsoons and light. Monsoonal winds inthe vicinity of Pulau Tinggi come from the northeast. No seagrassmeadows were found on the north and northeastern shores. Thesestrong, seasonalwindsoccurNovember toMarch in accordancewiththe ‘winter’ conditions in temperate regions and are characterizedby low sea temperature and high waves although the absolutedifferences are small. During the northwestmonsoon of 2009,meansea surface temperature andmeanwave height around Pulau Tinggiwas 28.2 � 0.8 �C and 1.12 � 0.5 m. At other times, these were29.4 � 0.5 �C and 0.9 � 0.2 m (data from the Department of Mete-orology, Malaysia). Monsoons may affect seagrasses by uprootingand removing them, and causing a reduction in light reachingmeadows. Storm events affect different species differently,depending on their robustness. In the Caribbean, robust seagrassessuch as Thalassia testudinum were not significantly affected bysimulated hurricanes (Cruz-Palacios and van Tussenbroek, 2005),but in Australia, deep water seagrass (>10 m) and shallow waterseagrass (<10 m) of mainly Halophila and Halodule species weregreatly reduced by stormevents, the former by light deprivation andthe latterbyuprooting (Preenet al.,1995).Off Florida, thebroad scale(hundreds of meters) spatial distribution of oceanic Halophila deci-pienswas altered when Hurricane Irene redistributed seed banks in1999 (Bell et al., 2008), after which plant clonal organization oper-ating at the small scale (m) imposed patterns within patches (Bellet al., 2008).

Recovery after large scale flooding is possible and ranges from 2years for deep-waterHalophila communities (Preen et al., 1995) to 3years for intertidal Zostera capricornii in Queensland, Australia(Campbell and McKenzie, 2004). Examples from subtropicalAustralia show that if there are remains of vegetative fragments,asexual/vegetative growth is a strong mechanism for recoloniza-tion, and species such as S. isoetifolium are stronger vegetativecolonizers thanH. uninervis, C. serrulata, C. rotundata andH. ovalis. Ifonly seed banks are available, strong sexual reproducers such as H.ovalis are more likely to begin patch initiation but may eventuallybe displaced by vegetative colonizers (Rasheed, 2004).

In Southeast Asia, monsoonal effects on seagrasses have notbeen studied in depth. Monsoons could play a role in maintainingmixed tropical meadows by imposing recurring disturbance and

opening up gaps for ruderal species. Conversely, seagrass growth insheltered areas may be enhanced when monsoons bring increasednutrients through rainfall and terrestrial runoff. In our preliminarysurvey in March 2010 immediately after the monsoon season inPulau Tinggi, canopy heights of C. serrulata, H. uninervis and S.isoetifolium were greater than before the monsoon (personalobservation), which lends support to this idea.

On the sheltered southern shores of the island where seagrasseswere found, these were limited to water depths of 3e10 m, corre-sponding to 37% and 15% of surface irradiance (Table 3) which iswithin the range of minimal surface irradiance found in seagrasssystems worldwide (Duarte, 1991b; Lee et al., 2007). Overall, thisforereef system receives light at an order of magnitude lower thanbackreef systems in Southeast Asia (Agawin et al., 2001; Gacia et al.,2005), and this is an important feature of forereef systems whencompared to backreef systems. Species that are successful in deepor turbid water are shade-adapted types such as H. decipiens and H.ovalis. In Pulau Tinggi, these two species were always the only onesfound at the deeper limit of the meadow because they employstrategies to cope in light conditions lower than backreef speciesare used to, such as having a lower light compensation point andconsistent electron transport rates (Erftemeijer and Stapel, 1999;Campbell et al., 2008).

4.4.2. SedimentThe sedimentary environment of Pulau Tinggi has organic

matter and organic carbon lower in comparison to most otherseagrass areas of Southeast Asia (Kennedy et al., 2004). Its silt-claycontent is also low (mean 2.28� 2.43% dryweight) when comparedto backreef systems. For example, silt-clay content was 5.2% inBolinao, 8.0% in Puerto Galera, and 12.2% in Palawan (Terrados et al.,1998). In looking for comparisons to other seagrass communities inthe region, it also became clear that there has been very little workdone on linking seagrass distribution and abundance to sedimentconditions in low-carbonate substrate. Backreef systems typicallyhave high carbonate ofmore than 90% (Erftemeijer andMiddleburg,1993; Erftemeijer, 1994), which indicated that seagrasses here arenutrient limited because of phosphate adsorption onto carbonatesediment. However, conflicting results were found between SouthSulawesi (Erftemeijer and Herman, 1994) and Northwest Luzon(Agawin et al., 1996), indicating the variability of these habitatsacross the region, and site-specific differences in the ways sea-grasses respond to their environments. In contrast, Pulau Tinggihas low inorganic carbon (carbonate) sediments (10.8 � 3.7% dryweight). How this affects nutrient availability for seagrasses, andfurthermore, how light and sediment in combination affect subtidalseagrasses remains to be studied.

Shrimp mounds were a common feature of the Pulau Tinggiforereef system with a density of at least 2 mounds m�2. Theaverage mound measured 15 cm in height and 40 cm in diameterand caused the development of gaps in the otherwise continuousseagrass meadow. These mounds were recolonised in sequence byH. ovalis and H. uninervis and gradually flattened out in approxi-mately 3e4 weeks. Considering how ubiquitous these moundswere in this system, we hypothesize that they have an importantrole to play in creating spatial complexity in the seagrass bed.

4.4.3. HerbivoryWe saw evidence for herbivory at the coral reefeseagrass

interface and within the seagrass meadows. An interesting featurein the coraleseagrass interface zone was the occurrence ofa consistent halo of bare substratum measuring 5e10 m width.There is evidence that fish and urchin herbivory is responsible forhalo formation in the Caribbean (Randall, 1965; Earle, 1972; Ogdenet al., 1973; Hay, 1984; Tribble, 1981), but has not been reported for



Southeast Asian seagrasses. An understanding of how and why thishalo develops will provide insights into habitat utilization by fishand urchins and hence, coral and seagrass connectivity.

Within the meadow itself, it was noticeable that dugongfeeding trails were found in areas with high Halodule uninervisbiomass. Ruderal species such as Halodule and Halophila speciesare known to be the preferred diet of dugongs (de Iongh et al.,1995), making forereef systems important habitats to study forherbivory effects.

4.4.4. CompetitionWe foundmultispecific meadows in Pulau Tinggi but correlation

analysis did not reveal any potential interactions. Belowgroundpartitioning of roots was suggested as an explanation for thebackreef system in Bolinao but there, differences in the root depthsbetween species were large. Climax species such as E. acoroides andT. hemprichii have rhizomes that extend down to a mean depth of7.52 and 6.52 cm respectively, and may not compete for nutrientswith species such as H. ovalis and H. uninerviswhich maintain rootsin the upper 3 cm of sediment (Duarte et al., 1998). In Pulau Tinggi,the size classes of species are similar. Furthermore, its major speciesare all located in the upper 3 cm of sediment but despite this, do notdisplay strong species partitioning of habitat, and occur in mixedspecies meadows. In Pulau Tinggi, studies on interspecific interac-tions in relation to the partitioning of root biomass may revealinteractions different from those in the Duarte et al. study (1997).

With regards to the response of seagrasses to underlyingdrivers, particularly in multispecific meadows, it is valuable toarticulate these responses in relation to plant strategies such as theC-S-R model of Grime (1977). This distinction was first tested fortropical seagrasses in Cockle Bay, Australia, where H. ovalis wasclassified as a ruderal species (high disturbance/low stress), H.uninervis was classified as a stress tolerant species (low distur-bance/high stress), S. isoetifolium and C. serrulatawere classified ascompetitor species (low disturbance/low stress) (Birch and Birch,1984). In the seagrass literature, references are made to pioneerand climax species, but there have not been explicit tests of thistriangular model of plant strategies as applied to tropical sea-grasses. Considering that the Pulau Tinggi seagrass community is inan early stage of succession, there are several questions that couldprovide new insight such as how do ruderal species “colonize” insubtidal habitats? In Pulau Tinggi, the occurrence of mostlyH. ovalison meadow perimeters that surround dense multispecific centresindicates that H. ovalis adopts a guerilla strategy, i.e. it colonizespreviously uninhabited substrate through rapid horizontal rhizomeexpansion. There is little understanding of how H. ovalis leads patchadvancement and whether this species serves to facilitate condi-tions in these frontal areas for other species. It is conceivable that H.ovalis facilitates seagrass colonization by providing sedimentstability (Fonseca, 1989), but this remains to be tested in the field.Studies in Bootless Bay, Papua New Guinea, and Cockle Bay,Australia, addressed succession based on plant strategies (ruderal-stress tolerators-competitors), but reported contrasting results.More work linking theoretical plant strategies with seagrassdistribution and abundance is required. Even in terrestrial grass-lands where there is an extensive literature on plant life strategies,there were problems in proving relationships between the C-S-Rplant strategies with feedback on soil conditions (Markham et al.,2009). For seagrasses, this hypothesized model provides an inter-esting way of interpreting species-specific responses in relation toresource allocation, growth and reproductive strategies. It has yetto be directly tested in tropical multispecific meadows. Seagrassesin Southeast Asia occur in backreef, forereef, and estuarine habitats,each with different disturbance and stress regimes. Thus we mightexpect different successional models for each system.

5. Conclusions

Seagrasses in Southeast Asia have been poorly studied, witha geographical focus on Indonesia and the Philippines. In compar-ison, we know very little about the seagrasses of Thailand, Malaysia,Singapore, Cambodia, Burma and Brunei Darussalam. Furthermore,ruderal species-dominated systems in subtidal forereefs have beenneglected in the literature in comparison to backreefs. Forereefs arevery different systems from the more well-studied backreefs interms of their light climate and sedimentary environment and wesuggest that these habitats are more widespread in Southeast Asiathan is reflected in the literature. Pulau Tinggi, southeast PeninsularMalaysia, has an extensive subtidal seagrass community in theforereef zone. It is characterized by low carbonate content, as wellas low organic matter and silt-clay, which makes it unique becausemost seagrassesediment interactions in other parts of SoutheastAsia have been conducted in high carbonate reef areas. Our surveyindicates that disturbance events, sediment characteristics,herbivory and light are potentially strong drivers towards whichour future research will be directed.

Acknowledgements

We acknowledge the Economic Planning Unit and the MarinePark Department of Malaysia for research permits. We thank SEA-BUDS, Renae Hovey, and Ben Piek for field assistance; RosmadiFauzi and Wong Ching Lee for administrative support; and SabasExplorer for logistical support. This research was partly funded bythe MOSTI E-Science grant (04-01-03-SF0177). J.O.L.S. was sup-ported by the Endeavour International Postgraduate ResearchScholarship and the University Postgraduate Award (the Universityof Western Australia), and the Hadiah Cuti Belajar program (Uni-versiti Malaya).

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Knowledge gaps in tropical Southeast Asian seagrass systems

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