Succession patterns in algal turf vegetation on a Caribbean coral reef
16
Botanica Marina 54 (2011): 111–126 2011 by Walter de Gruyter • Berlin • New York. DOI 10.1515/BOT.2011.021 2010/064 Article in press - uncorrected proof Succession patterns in algal turf vegetation on a Caribbean coral reef Anna Fricke 1,2, *, Mirta Teichberg 1 , Svenja Beilfuss 1 and Kai Bischof 2 1 Leibniz Center for Tropical Marine Ecology (ZMT), Fahrenheitstrasse 6, 28359 Bremen, Germany, e-mail: [email protected] 2 Department of Marine Botany, University of Bremen, Leobener Str. NW2, 28359 Bremen, Germany * Corresponding author Abstract Over the past three decades, Caribbean coral reefs have dras- tically changed in structure and organization due to anthro- pogenically driven environmental changes. The prognostic trend indicates a shift from coral- to more algal-dominated reefs coupled with a loss in biodiversity and destabilization of reef structure. This study focuses on the composition of the most common algal growth form, the turf, and investi- gates turf succession within a fringing Caribbean coral reef. In a field study starting October 2007, we followed succes- sion of turf algal assemblages grown on artificial substrata for periods of 15 up to 333 days at different water depths (5, 15 and 25 m). Species composition and abundance, biodiversity, total cover, and biomass were investigated and compared in uni- and multivariate analyses. Despite the pro- nounced change in coral reef structure over the past years, we found little difference from primary succession patterns described 30 years earlier. Succession patterns revealed a high diversity, mainly driven by the filamentous brown algal order Ectocarpales, the crustose green alga Pringsheimiella scutata at early stage, and diverse filamentous Cyanobacteria at later stages. Overall, the study provides insight into the early successional stages of coral reef vegetation by identi- fying the key species and discussing possible factors deter- mining reef development in relation to environmental change. Keywords: Curacao; Cyanobacteria; Ectocarpales; ¸ epibenthic; filamentous algae. Introduction The dominant algal growth form in shallow coral reef eco- systems is turf, a common, multi-specific assemblage of green, red and brown seaweeds, intermixed with filamentous Cyanobacteria (Odum and Odum 1955, Stephenson and Stephenson 1972, Morrissey 1980). Turf algal assemblages are rarely characterized by their constituent species. Identi- fication is difficult because of small sizes, common morpho- logical plasticity (Lewis et al. 1987) and different alternating life cycles (e.g., Thornber 2006). Furthermore, despite their high biodiversity ( )20 species in approx. 1 cm 2 ; Diaz-Pulido and McCook 2002), turf algae appear unobtrusive as low patchy turfs and scattered tufts within the heterogeneous structure of coral reefs (Hiatt and Strasburg 1960, Dahl 1973). Due to their role as primary producers and their rapid turn- over of organic matter, turf algae form the base of reef tro- phic structure (Wanders 1976, Carpenter 1985, Klumpp and Mckinnon 1992, Copertino et al. 2005, Carpenter and Williams 2007) and perform multiple additional functions in coral reef ecosystems. They form microhabitats for several invertebrates (Hacker and Steneck 1990, Olabarria and Chapman 2001, Pardo et al. 2007) and smaller demersal fish- es (Goncalves et al. 2002). They serve as a nutrient source ¸ and can accumulate detritus and sediments that provide raw materials for nutrient recycling, e.g., nitrogen fixation by fil- amentous Cyanobacteria (Wiebe et al. 1975, Williams and Carpenter 1997, Diez et al. 2007). Algal turf frequently occurs in areas that are subject to moderate grazing pressure and physical stresses (Hay 1981). Its characteristic densely packed, filamentous and finely- branched algae make it less accessible to herbivores than larger seaweeds (Hay 1981). Nevertheless, the high grazing pressure in tropical waters usually prevents the algae from reaching a high standing crop (Steneck and Watling 1982, Hackney and Sze 1988). Despite the positive ecological role of algal turf communities in coral reef ecosystems, they are in permanent competition for space with other benthic biota, including corals (McCook et al. 2001). Due to the opportun- istic life histories of many turf algal species, they can rapidly colonize damaged or dead coral colonies after disturbance events (Diaz-Pulido and McCook 2002, 2004, Titlyanov et al. 2005). Different natural and anthropogenic factors drive the stepwise replacement of hard corals on Caribbean reefs, including alteration of herbivore density, e.g., by general overfishing (Hughes et al. 2003) and mass mortality of the sea urchin Diadema antillarum Philippi 1845 (Hughes et al. 1985, Idjadi et al. 2010), eutrophication (Littler et al. 2010), extreme weather (Hoegh-Guldberg et al. 2007) such as hur- ricanes (Wilkinson and Souter 2008) and coral diseases (Les- ser et al. 2007). Changes in the benthos have been observed in the Caribbean and worldwide, starting with a reduction of corals, and ending in an increase in macroalgae (Diaz-Pulido et al. 2009) and Cyanobacteria (Paul et al. 2005). Overall, not only the degree of turf algal formation, but also algal species composition affects coral communities, as species specific interactions have been observed (Jompa and McCook 2003, Titlyanov and Titlyanova 2008). In conse-
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Transcript of Succession patterns in algal turf vegetation on a Caribbean coral reef
Botanica Marina 54 (2011): 111–126 � 2011 by Walter de Gruyter • Berlin • New York. DOI 10.1515/BOT.2011.021
2010/064
Article in press - uncorrected proof
Succession patterns in algal turf vegetation on a Caribbean
coral reef
Anna Fricke1,2,*, Mirta Teichberg1, Svenja Beilfuss1
and Kai Bischof2
1 Leibniz Center for Tropical Marine Ecology (ZMT),Fahrenheitstrasse 6, 28359 Bremen, Germany,e-mail: [email protected] Department of Marine Botany, University of Bremen,Leobener Str. NW2, 28359 Bremen, Germany
* Corresponding author
Abstract
Over the past three decades, Caribbean coral reefs have dras-tically changed in structure and organization due to anthro-pogenically driven environmental changes. The prognostictrend indicates a shift from coral- to more algal-dominatedreefs coupled with a loss in biodiversity and destabilizationof reef structure. This study focuses on the composition ofthe most common algal growth form, the turf, and investi-gates turf succession within a fringing Caribbean coral reef.In a field study starting October 2007, we followed succes-sion of turf algal assemblages grown on artificial substratafor periods of 15 up to 333 days at different water depths(5, 15 and 25 m). Species composition and abundance,biodiversity, total cover, and biomass were investigated andcompared in uni- and multivariate analyses. Despite the pro-nounced change in coral reef structure over the past years,we found little difference from primary succession patternsdescribed 30 years earlier. Succession patterns revealed ahigh diversity, mainly driven by the filamentous brown algalorder Ectocarpales, the crustose green alga Pringsheimiellascutata at early stage, and diverse filamentous Cyanobacteriaat later stages. Overall, the study provides insight into theearly successional stages of coral reef vegetation by identi-fying the key species and discussing possible factors deter-mining reef development in relation to environmentalchange.
Keywords: Curacao; Cyanobacteria; Ectocarpales;¸epibenthic; filamentous algae.
Introduction
The dominant algal growth form in shallow coral reef eco-systems is turf, a common, multi-specific assemblage ofgreen, red and brown seaweeds, intermixed with filamentousCyanobacteria (Odum and Odum 1955, Stephenson andStephenson 1972, Morrissey 1980). Turf algal assemblagesare rarely characterized by their constituent species. Identi-
fication is difficult because of small sizes, common morpho-logical plasticity (Lewis et al. 1987) and different alternatinglife cycles (e.g., Thornber 2006). Furthermore, despite theirhigh biodiversity ()20 species in approx. 1 cm2; Diaz-Pulidoand McCook 2002), turf algae appear unobtrusive as lowpatchy turfs and scattered tufts within the heterogeneousstructure of coral reefs (Hiatt and Strasburg 1960, Dahl1973).
Due to their role as primary producers and their rapid turn-over of organic matter, turf algae form the base of reef tro-phic structure (Wanders 1976, Carpenter 1985, Klumpp andMckinnon 1992, Copertino et al. 2005, Carpenter andWilliams 2007) and perform multiple additional functions incoral reef ecosystems. They form microhabitats for severalinvertebrates (Hacker and Steneck 1990, Olabarria andChapman 2001, Pardo et al. 2007) and smaller demersal fish-es (Goncalves et al. 2002). They serve as a nutrient source¸and can accumulate detritus and sediments that provide rawmaterials for nutrient recycling, e.g., nitrogen fixation by fil-amentous Cyanobacteria (Wiebe et al. 1975, Williams andCarpenter 1997, Diez et al. 2007).
Algal turf frequently occurs in areas that are subject tomoderate grazing pressure and physical stresses (Hay 1981).Its characteristic densely packed, filamentous and finely-branched algae make it less accessible to herbivores thanlarger seaweeds (Hay 1981). Nevertheless, the high grazingpressure in tropical waters usually prevents the algae fromreaching a high standing crop (Steneck and Watling 1982,Hackney and Sze 1988). Despite the positive ecological roleof algal turf communities in coral reef ecosystems, they arein permanent competition for space with other benthic biota,including corals (McCook et al. 2001). Due to the opportun-istic life histories of many turf algal species, they can rapidlycolonize damaged or dead coral colonies after disturbanceevents (Diaz-Pulido and McCook 2002, 2004, Titlyanov etal. 2005). Different natural and anthropogenic factors drivethe stepwise replacement of hard corals on Caribbean reefs,including alteration of herbivore density, e.g., by generaloverfishing (Hughes et al. 2003) and mass mortality of thesea urchin Diadema antillarum Philippi 1845 (Hughes et al.1985, Idjadi et al. 2010), eutrophication (Littler et al. 2010),extreme weather (Hoegh-Guldberg et al. 2007) such as hur-ricanes (Wilkinson and Souter 2008) and coral diseases (Les-ser et al. 2007). Changes in the benthos have been observedin the Caribbean and worldwide, starting with a reduction ofcorals, and ending in an increase in macroalgae (Diaz-Pulidoet al. 2009) and Cyanobacteria (Paul et al. 2005).
Overall, not only the degree of turf algal formation, butalso algal species composition affects coral communities, asspecies specific interactions have been observed (Jompa andMcCook 2003, Titlyanov and Titlyanova 2008). In conse-
112 A. Fricke et al.: Succession of algal communities in a coral reef
Article in press - uncorrected proof
quence, a better knowledge of turf algal communities isurgently needed to better understand the fate of damagedcoral reefs and to help predict coral reef resilience. A crucialrequirement for better understanding of turf algal vegetationis to gain an improved knowledge of basic drivers of devel-opment and composition over time. In general, we distin-guish between ecological succession, orderly change in thecomposition or structure of an assemblage, and seasonal var-iations (Begon et al. 1991).
Generally, succession in marine epibenthic communitiesstarts with the adhesion of particulate matter on surfaces,followed by the aggregation of bacteria and microalgae andthe formation of a biofilm (reviewed in O’Toole et al. 2000,Stoodley et al. 2002, Zardus et al. 2008). These biofilms,formed within hours (e.g., Cuba and Blake 1983) provide thebase for settlement of filamentous algae and Cyanobacteria.
At our study site, prior studies of turf algal distributionand ecology were conducted by van den Hoek (1969, 1978),van den Hoek et al. (1972, 1975) and Wanders (1976a,b,1977). Van den Hoek and his co-workers investigated thezonation patterns of algae, corals and gorgonians along dif-ferent transects within the reef using phytosociological meth-ods along with monitoring of environmental parameters (e.g.,light and water movement). Wanders emphasized primaryproductivity (Wanders 1976a,b) and investigated the succes-sion of turf algal vegetation in relation to different substrataand grazing pressure (Wanders 1977). Since these studies,performed over 30 years ago, major changes, like the dis-appearance of the formerly abundant sea urchin Diademaantillarium (Bak et al. 1984) and an increase in the macro-phyte Lobophora variegata (J.V. Lamouroux) Womersley exE.C. Oliveira (Nugues and Bak 2008), have been observed.Furthermore, as shown by Bak et al. (2005), the coral com-munity significantly changes among water depths, mainlydriven by a decrease in photosynthetically active radiation(PAR) and an increase in temperature alterations possiblyconnected with deep water upwelling events.
To investigate possible variations in the succession of turfalgal communities caused by environmental changes in thepast 30 years, we observed succession over 333 days andcompared findings with results of a similar study conductedat the same site approximately 30 years previously (Wanders1977). Additionally, we investigated possible depth-relateddifferences in vegetation development by comparing 280-day-old turf algal assemblages from shallow and deepwaters. The main goals of our study were 1) to describe earlysuccession and identify the most important settlers, and 2) todiscuss different factors potentially affecting turf algal veg-etation in relation to the increase of algal biomass observedon the coral reef over the past years.
Materials and methods
Study area
The study was conducted on Curacao, former Netherlands¸Antilles (128019–128239N; 688449–698109W). The island isbordered by a fringing reef formed by plateaus of Pleistocene
coral limestone that form steep cliffs on the seaward site (forfurther details, see van den Hoek et al. 1972, Wanders 1976).The observation site, Buoy 0 (128079N, 698579W), Klein Pis-cadeira, is located off the southwestern coast of the island,100 m west of the entrance to Piscadeira Bay. Inshore, thereef forms a shallow slope leading to a steep drop-off at10 m water depth approximately 100 m from shore (van denHoek et al. 1975). The mean daily tidal range is about0.15 m, with a maximum of 0.3 m during spring tides (Wan-ders 1976). The zonation of benthic algae in relation to coralsand gorgonians was previously investigated at this site byvan den Hoek (1969) and van den Hoek et al. (1972, 1975),who distinguished seven different algal and coral commu-nities starting with a eulittoral Cyanobacterial assemblage at0.5 m above high water level, and a deep water algal vege-tation at the lower limit of the phytal zone at 65 m depth.In the present study, succession in turf algal vegetation wasinvestigated on the slope at 5 m, on the drop off at 15 m,and at 25 m water depth. The 5 m site on the reef slope hadan almost horizontal sandy bottom with scattered coral rub-ble. The benthos at this site is characterized by the soft coralsPseudopterogorgia acerosa Pallas 1766, Plexaura flexuosaLamouroux 1821 and P. homomalla Esper 1792 (‘‘gorgoniancommunity’’, van den Hoek 1978) and a high turf algaldiversity (58 species in 25 m2, van den Hoek et al. 1975).At the drop off at 15 and 25 m, the reef was dominated byscleractinian corals, such as Agaricia agaricites Linnaeus1758, Montastraea cavernosa Linnaeus 1767 and Poritesastreoides Lamarck 1816 (‘‘roof shingle community’’, vanden Hoek 1978). The algal assemblage here was previouslyfound to be less diverse (van den Hoek et al. 1975) andmainly composed of the brown fleshy alga Lobophora varie-gata (Nugues and Bak 2008).
Measurement of abiotic environmental factors
Underwater light conditions were measured on three datesduring the experimental period in the spring season of 2008,using a submersible spectroradiometer (RAMSES ACC UV-Vis, 280–700 nm, Trios, Oldenburg, Germany) and a sub-mersible radiometer (LI-1000, Li-Cor, Lincoln, USA) equip-ped with LICOR 190 (air) and a 192 (underwater) quantumsensor (cosine corrected), down to 15 m water depth. Dupli-cate measurements were made and irradiance was averagedfor each depth. Additionally, the three different measure-ments taken were averaged to calculate the average attenu-ation coefficient of downward irradiance (Kd). Kd wascalculated as ln(Iz1/Iz2)/z, where Iz1 and Iz2 are the irradiancesmeasured at two different depths, and z the interval betweenthose two depths (m) (Kirk 1994).
Water motion at 5 and 15 m depths was measured withthe clod card technique described by Jokiel and Morrissey(1993). Clod cards (ns3) built of plaster of Paris were pre-weighed and fixed horizontally on the experimental set-upsnext to the settlement tiles (see below). Additionally, a con-trol was placed in an aquarium filled with ambient seawater.During transport within the water column, clod cards wereprotected in plastic bags to avoid dissolution. After a period
A. Fricke et al.: Succession of algal communities in a coral reef 113
Article in press - uncorrected proof
Figure 1 Overview of the experimental set-up in 5 m water depth:ceramic settlement tiles (9.6=9.6 cm) were exposed on PVC panelsfixed on a frame made of concrete reinforcement bars (100=200 cm) anchored on cinder blocks.
Figure 2 Underwater light regime, showing the attenuation ofPAR (400–720 nm), measured on three dates during the experimentin spring season 2008 down to 14 m water depth. Data is showingaverages ("SD).Duplicate measurements were made and irradiance was averagedfor each depth.
of three days, clod cards were sampled, dried at 608C overthree days and weighed.
Experimental set-up
To examine the different stages of succession in the algalturf vegetation, we exposed a series of settlement tilesbetween March 2008 and May 2008 at different water depths(5, 15 and 25 m). In each water depth, we installed coloni-zation set-ups composed of oblong gray polyvinyl chloride(PVC) panels (75=20 cm). At 5 and 15 m, the PVC panelswere fixed on a frame made of concrete reinforcement bars(100=200 cm), anchored on cinder blocks (at 5 and 15 mwater depth, Figure 1). In 25 m water depth, a single PVCpanel was deployed, fixed on a cinder block directly. At alldepths, settlement panels were fixed horizontally to the watersurface, 20 cm from the ground. Each PVC panel carriedfour settlement panels fixed by PVC clamps. In order to pro-vide homogeneity of settlement conditions, we used artificial
settlement panels wexperimental unit (EU); 9.6=9.6 cmx rath-er than natural substrate. EUs were sampled from the PVCpanels at different times by scuba diving.
Settlement substratum
The choice of the right settlement substrata is crucial forbenthic succession, as discussed in detail by Davis (2009).Microstructure, e.g., surface rugosity, plays a particularlyimportant role in the settlement or post-settlement survivor-ship of epibiota. Artificial substrata may be used to providea homogenous substratum that is reproducible on a micro-meter scale. Due to easy handling and replication, artificialsubstrata offer the possibility for different comparison stud-ies, e.g., survey studies at different times or between differentsites, where natural substratum varies. Thus, in our study weused unglazed ceramic tiles which have proven to be suitablefor epibiotic growth in other studies (Bers and Wahl 2004,Zacher et al. 2007, Fricke et al. 2008).
Natural succession
To investigate the difference in sequential succession on thecoral reef, we analyzed 1) stepwise succession within anassemblage growing at 5 m and 2) compared late stage com-munities growing in different water depths (5, 15 and 25 m).To examine the stepwise succession at 5 m, we analyzed tilesthat had been exposed underwater for 15, 28, 41, 54 and333 days in March 2008 (ns4).
To compare the respective late successional assemblagestages between 5, 15 and 25 m water depth, we sampled tilesthat were exposed for 280 days from May 2008 to February2009 (ns4). In addition, we compared the 333-day-old‘‘succession assemblage’’ with the 280-day-old ‘‘5 m assem-blage’’ in a consideration of the representativeness of 5 mlate stage communities.
During sampling, each EU was placed in an individualplastic bag filled with ambient seawater. To avoid damagethrough excessive solar radiation or temperature, EUs werewrapped in an opaque bag and transported to the laboratory(-15 min) in an insulated box filled with ambient seawater.
Vegetation analyses
To determine successional patterns of the turf algae, per-centage cover of individual taxa were recorded from eachtile collected using a binocular microscope (12=, Zeiss Ste-mi SV6, Hamburg, Germany) with an ocular grid (10/10divisions, 1 cm2 per visual field). Each EU was rinsed gentlywith filtered (60 mm) seawater using a wash bottle in orderto remove grazers and sediment. To avoid any edge effect,only the central part of the EU (25 cm2) was assessed. Over-all, four visual fields (4 cm2) were analyzed for each EU.Percentage cover of taxa exceeding 5% were grouped andcategorized in 5% increments (1%, 2%, 3%, 4%, 5%,5–10%, 10–15%, 15–20%, etc. to 95–100%). Due to three-dimensionality, certain taxa overlapped, which caused theoverall sum of cover to exceed 100%. For the youngerassemblages (15–54 days), all individuals present were
114 A. Fricke et al.: Succession of algal communities in a coral reef
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Tab
le1
Mea
n("
SD)
perc
enta
geco
ver
ofta
xaen
coun
tere
don
cera
mic
settl
emen
ttil
eson
5di
ffer
ent
days
duri
ngsu
cces
sion
in5
mw
ater
dept
h(1
5–33
3da
ys)
and
afte
r28
0da
ysat
diff
eren
tw
ater
dept
hs(5
,15
and
25m
).
No.
Taxa
/spe
cies
Succ
essi
onat
5m
wat
erde
pth
(in
days
)A
ssem
blag
esat
diff
eren
tw
ater
dept
hs
1528
4154
333
5m
15m
25m
Chl
orop
hyta
1B
ryop
sis
0.3"
0.6
•B
.pe
nnat
aJ.
V.
Lam
ouro
ux18
092
Der
besi
a0.
2"0.
40.
7"1.
20.
1"0.
30.
4"0.
60.
2"0.
40.
5"1.
0•
D.
fast
igia
taW
.R.
Tayl
or19
283
Cha
etom
orph
a1.
4"1.
82.
9"2.
40.
8"1.
0•
C.
grac
ilis
Kut
zing
1845
4C
lado
phor
a1.
3"1.
82.
3"1.
23.
5"3.
12.
0"1.
83.
1"1.
60.
8"1.
21.
8"1.
7•
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laet
evir
ens
(Dil
lwyn
)K
utzi
ng18
43•
C.
lini
form
isK
utzi
ng18
495
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ngsh
eim
iell
a2.
1"0.
63.
5"1.
411
"1
20"
87.
8"2.
08.
4"3.
126
"1
2.1"
1.8
•P.
scut
ata
(Rei
nke)
Mar
chew
iank
a19
256
Ulv
a5.
1"3.
12.
7"2.
10.
8"1.
21.
9"2.
22.
5"1.
09.
6"3.
60.
3"0.
60.
7"0.
8•
U.
flex
uosa
subs
p.pa
rado
xa(C
.A
gard
h)M
.J.
Wyn
ne20
05•
U.
chae
tom
orph
oide
s(B
ørge
sen)
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den,
Blo
mst
er,
Mag
gs,
P.C
.Si
lva,
M.J
.St
anho
peet
J.R
.W
aala
nd20
03Ph
aeop
hyce
ae7
Spha
cela
ria
2.8"
1.0
1.6"
1.1
1.2"
1.0
4.3"
8.0
20"
314
"8
12"
93.
6"0.
8•
S.tr
ibul
oide
sM
eneg
hini
1840
•S.
nova
e-ho
llan
diae
Sond
er18
45•
S.ri
gidu
laK
utzi
ng18
438
Ect
ocar
pale
s10
"3
7.3"
5.2
10"
819
"11
9.2"
6.1
14"
1316
"7
2.4"
2.7
•F
eldm
anni
air
regu
lari
s(K
utzi
ng)
G.
Ham
el19
39•
F.in
dica
(Son
der)
Wom
ersl
eyet
A.
Bai
ley
1970
•H
inck
sia
mit
chel
liae
(Har
vey)
P.C
.Si
lva
1987
9D
icty
otal
es0.
6"1.
30.
3"0.
610
Cru
st.
Phae
ophy
ceae
*0.
8"0.
61.
4"0.
91.
6"1.
33.
1"2.
40.
1"0.
30.
2"0.
40.
2"0.
2R
hodo
phyt
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ocha
etiu
m0.
6"1.
3•
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barb
aden
se(V
icke
rs)
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gese
n19
1512
Cen
troc
eras
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5.3
6.6"
6.4
0.4"
0.6
•C
.cl
avul
atum
(C.
Aga
rdh)
Mon
tagn
e18
4613
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amiu
m3.
8"7.
5•
C.
nite
ns(C
.A
gard
h)J.
Aga
rdh
1851
A. Fricke et al.: Succession of algal communities in a coral reef 115
Article in press - uncorrected proof
(Tab
le1
cont
inue
d)
No.
Taxa
/spe
cies
Succ
essi
onat
5m
wat
erde
pth
(in
days
)A
ssem
blag
esat
diff
eren
tw
ater
dept
hs
1528
4154
333
5m
15m
25m
14C
eram
ium
0.6"
1.3
0.4"
0.8
0.5"
0.5
6.5"
8.0
0.9"
1.4
1.1"
2.3
0.6"
0.7
0.3"
0.6
•C
.ci
mbr
icum
f.fl
acci
dum
(H.E
.Pe
ters
en)
Furn
ari
etSe
rio
inC
ecer
eet
al.
1996
•C
.ci
mbr
icum
H.E
.Pe
ters
enin
Ros
envi
nge
1924
•G
ayli
ella
flac
cida
(Har
vey
exK
utzi
ng)
T.O
.C
hoet
L.J
.M
cIvo
rin
Cho
etal
.20
0815
Taen
iom
a0.
1"0.
1•
T.na
num
(Kut
zing
)Pa
penf
uss
1952
16P
olys
ipho
nia
0.3"
0.6
3.4"
3.3
0.4"
0.4
1.3"
1.0
0.8"
1.0
0.3"
0.6
0.2"
0.4
2.3"
3.5
•P.
scop
ulor
umva
r.vi
llum
(J.
Aga
rdh)
Hol
lenb
erg
1968
17H
erpo
siph
onia
25"
1213
"10
3.4"
2.8
•H
.bi
pinn
ata
M.A
.H
owe
1920
•H
.se
cund
a(C
.A
gard
h)A
mbr
onn
1880
18L
aure
ncia
/Cho
ndri
a1.
3"1.
00.
1"0.
10.
1"0.
11.
8"3.
10.
3"0.
4•
Cho
ndri
acu
rvil
inea
taF.
S.C
ollin
set
Her
vey
1917
•L
aure
ncia
obtu
sa(H
udso
n)J.
V.
Lam
ouro
ux18
1319
Ano
tric
hium
0.3"
0.6
1.3"
1.9
0.6"
0.9
1.9"
2.1
•A
.te
nue
(C.
Aga
rdh)
Nag
eli
1862
20L
ejol
isia
0.4"
0.7
•L
.ex
posi
taC
.W.
Schn
eide
ret
Sear
les
inSe
arle
set
Schn
eide
r19
8921
Wra
ngel
ia14
"16
•W
.ar
gus
(Mon
tagn
e)M
onta
gne
1856
22G
riff
iths
ia1.
3"2.
5•
G.
glob
ulif
era
Har
vey
exK
utzi
ng18
6223
Hyd
roli
thon
0.4"
0.3
2.9"
2.5
4.9"
3.7
1.3"
1.4
2.3"
2.0
0.2"
0.4
0.2"
0.4
0.3"
0.6
•H
.fa
rino
sum
(J.V
.L
amou
roux
)D
.Pe
nros
eet
Y.M
.C
ham
berl
ain
1993
24Ja
nia
0.3"
0.6
•J.
capi
llac
eaH
arve
y18
53C
yano
bact
eria
25D
icho
thri
x1.
1"0.
60.
4"0.
30.
4"0.
30.
6"1.
321
"3
36"
180.
1"0.
1•
D.
utah
ensi
sT
ilden
1898
26R
ivul
aria
0.3"
0.6
0.4"
0.8
•R
.po
lyot
is(J
.A
gard
h)H
auck
1884
116 A. Fricke et al.: Succession of algal communities in a coral reef
Article in press - uncorrected proof
(Tab
le1
cont
inue
d)
No.
Taxa
/spe
cies
Succ
essi
onat
5m
wat
erde
pth
(in
days
)A
ssem
blag
esat
diff
eren
tw
ater
dept
hs
1528
4154
333
5m
15m
25m
27R
ivul
aria
spp.
0.8"
1.3
1.6"
1.5
6.6"
3.6
1.9"
3.8
28O
scil
lato
ria
0.1"
0.1
0.3"
0.4
0.6"
0.7
•O
.pr
ince
psV
auch
erex
Gom
ont
1892
29C
alot
hrix
spp.
0.3"
0.5
0.4"
0.8
0.2"
0.4
•C
.cr
usta
cea
Scho
usbo
eex
Thu
ret
1876
30Fi
lam
ento
usC
yano
bact
eria
0.4"
0.6
1.4"
0.1
5.2"
3.1
7.0"
6.3
33"
740
"19
20"
829
"10
•L
yngb
yaco
nfer
void
esC
.A
gard
h18
24•
L.
maj
uscu
la(D
illw
yn)
Har
vey
exG
omon
t18
92•
L.
sem
iple
na(C
.A
gard
h)J.
Aga
rdh
exG
omon
t18
92•
Pho
rmid
ium
Kut
zing
exG
omon
t,18
92•
Toly
poth
rix
Kut
zing
exB
orne
tet
Flah
ault,
1886
Bac
illar
ioph
yta
31Tu
bedw
ellin
gdi
atom
s0.
7"1.
20.
3"0.
42.
0"1.
78.
9"6.
00.
1"0.
3Fo
ram
inif
era
32P
lano
rbul
ina
0.2"
0.4
0.7"
0.6
1.1"
1.2
2.8"
2.2
2.2"
1.8
13"
420
"9
•P.
acer
vali
sH
.B.
Bra
dy18
8433
Sori
tes
5.5"
3.0
2.9"
3.0
0.2"
0.4
•S.
dom
inic
ensi
sH
ofke
r19
76B
enth
icfa
una
34Sp
iror
bina
e0.
1"0.
10.
5"1.
00.
1"0.
11.
3"1.
02.
4"2.
4•
Neo
dexi
ospi
rafo
ram
inos
a•
N.
form
osa
35A
scid
iace
ae0.
9"0.
9
Taxa
are
num
bere
dan
dsp
ecie
s(t
hrou
ghla
ter
mic
rosc
opic
anal
yses
)ar
elis
ted
belo
wea
chta
xon.
ns4.
For
each
asse
mbl
age
(col
umn)
,va
lues
for
the
two
mos
tab
unda
ntta
xaar
epr
inte
din
bold
.*C
rust
.Ph
aeop
hyce
ae:
Thi
sta
xon
cont
aine
ddi
scs
ofph
aeop
hyce
ance
lls,
whi
chw
ere
obse
rved
tobe
part
ofE
ctoc
arpa
les,
orSp
hace
lari
a.E
ctoc
arpa
les
and
Spha
cela
rial
esbo
thfo
rmcr
eepi
ngpr
ostr
ate
fila
men
ts,
whi
char
eof
ten
unite
dto
form
disc
s(v
ande
nH
oek
etal
.19
95).
A. Fricke et al.: Succession of algal communities in a coral reef 117
Article in press - uncorrected proof
investigated, whereas for the older assemblages ()54 days),the most abundant taxa were investigated. Taxa were iden-tified to the lowest taxonomic level possible. Due to smallsizes and partly missing fertile structures or other morpho-logically important features, different species had to begrouped together in some cases for analysis of their quanti-tative importance within the assemblage structure. Speciesidentification was based on common identification literature(e.g., Boergesen 1913–1914, 1915–1920, Taylor 1960,Fletcher 1987, Abbott 1999, Littler and Littler 2000, Abbottand Huisman 2004, Dawes and Mathieson 2008), and thealgal taxonomy applied is in accordance with Guiry and Gui-ry (2010).
To confirm species identifications, a defined area of eachEU was scraped and fixed in 4% formalin, and additionalobject slides were prepared and analyzed later using a com-pound microscope (50–400= magnification, Axioscope,Zeiss, Hamburg, Germany).
Species richness (S) and evenness (J9) were determined foreach sampling time and successional stage from the taxaidentified. Additionally, total algal biomass and % coverwere recorded. To determine total algal biomass, the algalmaterial from the central part of each tile was removed witha sterilized razorblade, dried over 3 days at 608C, andweighted.
Univariate analyses
One-way analyses of variances (ANOVAs) were performedto test differences in biodiversity wincluding species richness(S) and evenness (J9)x, total algal biomass and total % coverbetween assemblages of different successional stages (factor:age) and different depths (factor: depth). Homogeneity ofvariances was tested using Cochran’s test, and variances werehomogenized by square root or log transformation whennecessary. Tukey’s test of honestly significant difference(HSD) was used for post-hoc tests. Percentage cover datawere arcsine-transformed prior to analyses.
Multivariate analyses
To compare the different assemblages by species composi-tion, all communities were analyzed by analyses of similarity(ANOSIM) using PRIMER v6 (Clarke and Warwick 2006).ANOSIMs were based on Bray-Curtis similarity indices cal-culated from percentage cover prior to square root transfor-mations in order to scale-down the importance of the highlyabundant taxa. Similarity percentages (SIMPER) were usedto determine the relative contribution of single taxa respon-sible for differences in specific species composition amongtreatments. To visualize changes among different assem-blages during early and late succession, the transformed datawere subsequently analyzed using cluster analysis in con-junction with the similarity profile (SIMPROF) routine basedon calculations of Bray-Curtis similarity matrices (Bray andCurtis 1957). Clusters identified by the SIMPROF test werevisualized using multi-dimensional scaling (MDS) plots.
Results
Abiotic environmental factors
Light attenuation varied strongly with water depth (Figure 2).The respective Kd values at 5 and 15 m water depth were onaverage 0.14 m-1 and 0.07 m-1 for PAR, 0.11 m-1 and 0.06 m-1
for UVA, and 0.24 m-1 and 0.16 m-1 for UVB.Relative water movement at the study site significantly
decreased with depth (ANOVA: F2,8s204.29, p-0.001). Theloss of clod card material was 1.8 times higher in 5 m(62"2%) than in 15 m water depth (35"3%).
On 16 October 2008, a hurricane event (Hurricane Omar)occurred, causing considerable damage to the coastal area.
General pattern of species composition
The different turf algal assemblages grown on unglazedceramic tiles between 15 and 333 days at different waterdepths (5–25 m) consisted of a total of 35 different taxa(Table 1). Among macroalgae sensu lato, we distinguished6 Chlorophyceae (Ch; 8 identified species), 4 Phaeophyceae(Ph; 6 identified species), 14 Rhodophyta (Rh; 18 identifiedspecies) and 6 Cyanobacteria (Cy; 9 identified species), 2foraminiferans (Fo) and 2 taxa of macrobenthic fauna (Fa),including Serpulidae and Ascidiaceae (Table 1). In additionto the macroalgae, a form of tube dwelling diatom (Di) wasincluded when it was very abundant and visible under obser-vational conditions (Table 1). Overall, a minimum of 41 algaland cyanobacterial species (Table 1) was found.
Succession in 5 m water depth
The turf algal assemblage in the shallow coral reef at 5 mwater depth colonized rapidly (Figure 3A). After a period of15 days, the assemblage comprised of 14 taxa, with the fil-amentous Ectocarpales (Ph, Feldmannia irregularis, F. indi-ca, Hincksia mitchelliae; Figure 3B, Table 1) as the mostdominant, followed by Ulva (Ch, U. flexuosa subsp. para-doxa, U. chaetomorphoides, Table 1) and the Sphacelariales(Ph, Sphacelaria tribuloides, S. novae-hollandiae, S. rigi-dula; Table 1). Several other species, like Bryopsis pennata(Ch) and Anotrichum tenue (Rh) appeared after 15 and28 days (Table 1). Between 28 and 41 days, the assemblagestrongly changed in composition (Table 2, Figure 4), mainlydue to the occurrence of crust-forming Pringsheimiella scu-tata (Ch; Figure 3C), which increased strongly and domi-nated the turf together with the Ectocarpales after 54 days(Table 1, Figure 3A). After 333 days, the turf was clearlydominated by the heterocystous cyanobacterium Dichothrix(Figure 3D), diverse filamentous Cyanobacteria, and the redalgae Herposiphonia (Table 1, Figure 3E).
Species richness significantly increased at the end of theobserved succession after 333 days, whereas no change wasobserved in the evenness (Table 3). Percentage coverincreased significantly after 54 and 333 days (Figure 5, Table3). Overall biomass was still low after 54 days (1.95"0.6mg cm-2) but significantly increased at the end of the studyat 333 days (6.5"2.5 mg cm-2; Table 3).
118 A. Fricke et al.: Succession of algal communities in a coral reef
Article in press - uncorrected proof
Figure 3 Changes in cover of most abundant taxa during succession in 5 m water depth.(A) Graph showing all taxa reaching )5% cover after 15 days and )10% cover after 333 days of succession. Values are means"SD, ns4.(B–E) Most abundant species, preserved in 4% formalin: (B) Feldmannia irregularis (Ph, Ectocarpales), (C) Pringsheimiella scutata (Chl),(D) Dichothrix utahensis (Cy), (E) Herposiphonia bipennata (Rh). Scale bars in Figure 3B–E: 100 mm.
Comparison of assemblages grown at different water
depths
To compare assemblages grown at different water depths, wewanted to use samples representative of late succession. Acomparison of the 280-day and 333-day turfs at 5 m waterdepth showed no difference in structure, neither in the bio-diversity nor in taxon composition (Table 3, Figure 4); there-fore, we assumed that 280-day assemblages were stable anda good representation of late stage structure.
The late turfs differed significantly in their taxon com-position between different depths (Table 2). While the 5 mturf was mainly composed of different groups of Cyanobac-teria, the 15 m turf had a more balanced composition ofChlorophyta, Rhodophyta and Phaeophyceae, with few Cya-nobacteria and a slightly higher proportion of benthic fauna;the 25 m turf was clearly dominated by non-heterocystousfilamentous Cyanobacteria (e.g., Lyngbya spp., Table 1) andbenthic fauna, mainly the foraminiferans Planorbulina spp.(Planorbulina acervalis) (Tables 1 and 2). Overall the maindifference was found between 5 and 15 m water depth,caused by the high abundance of Dichothrix (Cy), whichsignificantly decreased with depth and was absent at 25 m(Tables 1 and 2). Also, Herposiphonia (Rh) or Centroceras(Rh) vanished, whereas Planorbulina (Fo) significantlyincreased with increasing depth (Tables 1 and 2).
Despite these changes, no difference was observed in spe-cies richness or evenness (Table 3). Total biomass and per-cent cover decreased significantly between 5 and 25 m waterdepth (Figure 6).
Discussion
The algal turf vegetation in the shallow coral reef colonizedrapidly, reaching high diversity within a short time. The early
successional pattern we found in the present study was sim-ilar to that found at the same study site 30 years earlier byWanders (1977). In that study, turf algal communities weregrown on asbestos plates (60=30 cm) placed 40 cm abovethe bottom in 2 m water depth, and succession was followedfrom 14 up to 105 days from October 1972 to January 1973.In conformity with our results, the early succession patternwas clearly dominated by the filamentous Ectocarpales (Ph,Hincksia granulosa), whereas, after 42 days, a crustose Pro-toderma-like green alga (Protoderma sp.) increased its abun-dance and dominated the turf together with the Ectocarpales.From Wanders’ description, it is possible that this Protoder-ma-like crustose alga is actually the species we identified asPringsheimiella scutata (Ch). Moreover, the observed shiftfrom opportunistic filamentous (r-selected species) towardsmore competitive fleshy algal species (K-selected species),such as Centroceras clavulatum or Wrangelia argus, after105 days in accord with the classical theory of succession(Begon et al. 1991).
Because a similar pattern was found in our study 30 yearslater in a different season (rainy vs. dry) and on a differentsubstratum (asbestos plates vs. ceramic), the sequenceobserved may represent typical early succession on the shal-low reefs of this region. Interestingly, this pattern did notseem to be affected by the loss in coral cover and increasein algal biomass observed over the past 30 years (Bak et al.2005, Hoegh-Guldberg et al. 2007, Mumby and Steneck2008, Diaz-Pulido et al. 2009). This indicates that the forcesaffecting early stage vegetation within the coral reef ecosys-tem are still functioning or are not affected by the environ-mental change, e.g., changes in grazing pressure, nutrientavailability, temperatures, underwater light regime, etc.
In addition to the increase in fleshy algal species, weobserved a clear dominance of filamentous Cyanobacteriaafter 333 days. This trend is partially evident in the data of
A. Fricke et al.: Succession of algal communities in a coral reef 119
Article in press - uncorrected proof
Tab
le2
Ana
lyse
sof
sim
ilari
ty(A
NO
SIM
)an
dsi
mila
rity
perc
enta
ges
(SIM
PER
)te
stin
gth
eef
fect
sof
succ
essi
onal
stag
e(i
nda
ys)
at5
mw
ater
dept
h,an
dw
ater
dept
h(5
,15
,an
d25
m)
on28
0-da
y-ol
das
sem
blag
es.
Succ
essi
onin
5m
wat
erde
pth
AN
OSI
M(o
vera
ll)G
loba
lR
s0.
642,
ps0.
001
Succ
essi
onal
stag
es15
™28
days
28™
41da
ys41
™54
days
54™
333
days
AN
OSI
MR
s0.
49,
ps0.
03R
s0.
35ps
0.03
n.s.
Rs
1ps
0.03
SIM
PER
Dis
sim
ilari
ty40
%D
issi
mila
rity
38%
Dis
sim
ilari
ty61
%11
%q
Pol
ysip
honi
a(R
h)11
%q
Pri
ngsh
eim
iell
a(C
h)12
%q
pH
erpo
siph
onia
(Rh)
10%
qH
ydro
lith
on(R
h)9%
-Pol
ysip
honi
a(R
h)10
%q
Dic
hoth
rix
(Cy)
9%-U
lva
(Ch)
9%q
Ect
ocar
pale
s(P
h)8%
qFi
l.C
yano
bact
eria
9%-E
ctoc
arpa
les
(Ph)
8%-U
lva
(Ch)
8%q
Spha
cela
ria
(Ph)
8%-L
aure
ncia
/Cho
ndri
a(R
h)7%
qFi
l.C
yano
bact
eria
7%-a
Tube
dwel
ling.
diat
oms
(Di)
6%q
pC
lado
phor
a(C
h)7%
qTu
bedw
ellin
gdi
atom
s(D
i)7%
-aR
ivul
aria
sp.
(cy)
Ass
embl
ages
grow
nat
diff
eren
tw
ater
dept
hs(5
,15
and
25m
)A
NO
SIM
(ove
rall)
Glo
bal
Rs
0.94
2ps
0.00
1W
ater
dept
hs5™
15m
15™
25m
5™25
mA
NO
SIM
Rs
0.96
9,ps
0.03
Rs
0.81
3,ps
0.03
Rs
0.99
,ps
0.03
SIM
PER
Dis
sim
ilari
ty52
%D
issi
mila
rity
46%
Dis
sim
ilari
ty54
%16
%-D
icho
thri
x(C
y)16
%-P
ring
shei
mie
lla
(Ch)
18%
-aD
icho
thri
x(C
y)7%
-Ulv
a(C
h)10
%-E
ctoc
arpa
les
(Ph)
9%q
Pla
norb
ulin
a(F
a)7%
qP
ring
shei
mie
lla
(Ch)
9%-a
Wra
ngel
ia(R
h)9%
-aH
erpo
siph
onia
(Rh)
6%q
pW
rang
elia
(Rh)
6%q
Fil.
Cya
nosa
(Cy)
7%-U
lva
(Ch)
6%q
Pla
norb
ulin
a(F
a)6%
-aH
erpo
siph
onia
(Rh)
7%-E
ctoc
arpa
les
(Ph)
6%-H
erpo
siph
onia
(Rh)
5%-S
phac
elar
ia(P
h)6%
-aC
entr
ocer
as(R
h)6%
-Fil.
Cya
noba
cter
ia
Glo
bal
anal
ysis
resu
ltsof
AN
OSI
M(R
,p)
test
ing
for
both
indi
vidu
alan
dpa
ired
trea
tmen
tdi
ffer
ence
sar
eal
sogi
ven.
Res
ults
ofSI
MPE
Ran
alys
isar
egi
ven
aspe
rcen
tdi
ssim
ilari
tyfo
rea
chsi
gnif
ican
tlydi
ffer
ent
trea
tmen
tpa
ir,f
ollo
wed
byth
epe
rcen
tco
ntri
butio
nof
each
sing
leta
xon
toth
edi
ffer
ence
.The
Tabl
esh
ows
all
taxa
that
cont
ribu
ted
to)
50%
ofsp
ecie
sco
mpo
sitio
nam
ong
trea
tmen
ts.
Incr
ease
dor
decr
ease
dab
unda
nce
and
abse
nce
orpr
esen
ceof
each
taxo
nw
ithre
spec
tto
succ
essi
ontim
eor
incr
easi
ngw
ater
dept
har
esy
mbo
lized
with
q/-
and
a/p,
resp
ectiv
ely.
Hig
her
clas
sifi
catio
nof
each
taxo
nis
give
nin
brac
kets
:C
h,C
hlor
ophy
ta;
Cy,
Cya
noba
cter
ia;
Di,
diat
oms;
Fa,
bent
hic
faun
a;Ph
,Ph
aeop
hyce
ae;
Rh,
Rho
doph
yta;
Fil.,
fila
men
tous
;n.
s.,
not
sign
ific
ant
diff
eren
ces.
120 A. Fricke et al.: Succession of algal communities in a coral reef
Article in press - uncorrected proof
Figure 4 Non-metric multi-dimensional scaling (nMDS) plot, showing differences in assemblage structure between successional stages ofdifferent ages (15–333 days) and water depths (5–25 m) for 280 days old assemblages.Assemblage age is given as number of days. Superimposed clusters (line) identified by sequence of SIMPROF tests (p-0.05) on dendrogramsat similarity levels of 60%. The taxon abundances were square root transformed before converting to Bray-Curtis similarities. The stresslevel -0.2 indicates a still potentially useful presentation of the data after compression into 2 dimensions.
Wanders (1977), who reported an increase in the cyanobac-terium Calothrix crustacea at the end of the study after105 days.
This dominance in Cyanobacteria may be due to their highcontent of nitrogenous secondary metabolites (Pennings etal. 1997, Albert et al. 2005, Paul et al. 2005) which can detergrazers, like herbivorous fishes (Tsuda and Kami 1973,Thacker et al. 2001), and act as chemical defense againstpotential competitors (Nagle and Paul 1998, Ross et al.2009). Corresponding to the ‘‘inhibition model’’ of Connelland Slatyer (1977), this might promote selective browsing inthe algal turf to the benefit of Cyanobacteria (Pennings et al.1997, Albert et al. 2005, Paul et al. 2005). General algal fieldguides report a restricted distribution of Cyanobacteria toshallow waters (e.g., Littler and Littler 2000, 2008), how-ever, in our study they were highly abundant over the wholedepth range. Thus, the differences in taxon compositionbetween depths were mainly caused by a different compo-sition of cyanobacterial species from the tuft-forming hete-rocystous Dichothrix spp. (Cy, D. utahensis) abundant in 5 mwater depth to the non-heterocystous genera like Lyngbyaand Oscillatoria dominating in the drop-off assemblages.
Interestingly, no Dichothrix species were found in the tran-sects of van den Hoek (1969, 1978) and van den Hoek et al.(1972, 1975). Such species may have been grouped underthe genus Calothrix (e.g., Calothrix sp.) since both generahave basal heterocysts. Nevertheless, in these transects (op.cit.) the heterocyst-forming Cyanobacteria (e.g., Calothrixscopulorum, Brachytrichia quotyi) were most abundant atshallower depths in the upper eulittoral (van den Hoek et al.1975), whereas members of non-heterocyst forming generaLyngbya (e.g., L. aestuarii, L. majuscula, L. sordida) and
Oscillatoria (O. bonnemaisonii) were more abundant indeeper waters (van den Hoek et al. 1975; van den Hoek1978).
Light plays an important role in algal vegetation by driv-ing photosynthetic reactions (Kirk 1994). Thus, in our study,the significant decrease in biomass and cover may be relatedto the observed depth-related decrease in light quantity, asmediating grazing pressure was observed to be highest atshallower depths in the research area (S. Beilfuss personalcommunication).
Furthermore varying distributions of cyanobacterial typesmight be correlated with differences in light requirements ofthe different species, as photosynthesis, heterocyst formation(Campbell et al. 1993), nitrogenase activity and growth ratesare strongly dependent on light quality and quantity (e.g.,Staal et al. 2001, 2002, Bell and Fu 2005, Rabouille et al.2006).
In addition to heterocystous Cyanobacteria, the red algalspecies Herposiphonia spp. (Rh, H. bipennata and H. secun-da) were highly abundant in the shallow reef in old vege-tation, but decreased in the drop-off where other red algaelike Wrangelia argus and Ceramium nitens were more abun-dant. Although Herposiphonia bipennata (Rh) was notobserved in early surveys (van den Hoek et al. 1975; vanden Hoek 1978), Herposiphonia secunda and the relatedHerposiphonia tenella were found in a broad range of depthsfrom 2 m down to 30 m (van den Hoek et al. 1975; van denHoek 1978). Ceramium nitens (Rh) is mentioned as a com-mon species of the elevated turf in the deep reef at this site(van den Hoek et al. 1975, Vooren 1981), whereas Wrangeliaargus was observed at depths F20 m (van den Hoek 1978).
In addition to the differences in Cyanobacteria and algalcover, there was an increase in benthic fauna with increasing
A. Fricke et al.: Succession of algal communities in a coral reef 121
Article in press - uncorrected proof
Tab
le3
Ove
rvie
wof
diff
eren
tan
alys
esco
mpa
ring
diff
eren
tun
ivar
iate
depe
nden
tva
riab
les
wbio
mas
san
ddi
vers
itym
easu
rem
ents
incl
udin
gsp
ecie
sri
chne
ss(S
)an
dE
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ces. depth. The crust-forming benthic foraminiferan Planorbulina
spp. was found in high abundance at 25 m water depth. Thisgenus is able to attach itself permanently to the substratumusing an organic settlement cue and therefore becomes anintegrative part of the reef (Langer 1993). In contrast, thesecond observed benthic foraminiferan Sorites spp. had areversed pattern decreasing in abundance with increasingdepth. This might be explained by endosymbiontic relation-ships, as miliolid foraminiferans of this genus are known tohost light dependent dinoflagellates (Pawlowski et al. 2001,Pochon and Pawlowski 2006).
The availability of propagules, spores and larvae and theirdispersal ranges may play important roles in assemblagedevelopment, but they are largely dependent on water flowand boundary layer thickness (Abelson and Denny 1997,Koehl and Hadfield 2010). The results from the clod cardsindicate that water flow differed along the reef slope, whichmay also explain the differences in species composition atdifferent depths.
The patterns in early succession are important because ear-ly settlers have been found to shape their communities. Forexample, the presence of a certain species can either facilitateor inhibit the colonization of other species (Connell and Sla-tyer 1977). The early settlers identified in our study wereprimarily filamentous, but there was also one green crustosealga.
Some species of crustose red algae can increase thesettlement success of coral larvae (Birrell et al. 2008), butno studies have been done on green crustose species so far.This might be a crucial point as other species of the Ulvel-laceae, like Ulvella lens have been shown to induce the set-tlement of molluscs and sea urchins (reviewed in Fusetani2004). Further studies on the effect of these algal species oncoral larval settlement are warranted.
Different ecological interactions drive and shape the coralreef community. As most benthic coral organisms are sessile,and as light is essential for all photosynthesizing organisms(e.g., macroalgae, Cyanobacteria, endosymbiotic dinoflagel-lates), there is permanent competition for potential settlingspace (Jackson and Buss 1975, Benayahu and Loya 1981,Box and Mumby 2007). Under the right conditions macroal-gae and Cyanobacteria may outcompete corals through fastergrowth (Jamaluddin and Laurence 2003, Titlyanov and Tit-lyanova 2008). The combination of nutrient limitation (Lar-ned 1998) and high grazing pressure (Wanders 1977,Williams and Polunin 2001), however, in the coral reef envi-ronment controls macroalgal growth (Hackney and Sze1988). Grazing pressure is often thought to be an importantfactor influencing the zonation of corals and algal vegetation(Littler et al. 1995) as it suppresses algal growth, mainly inshallower waters (van den Hoek et al. 1975, Wanders 1976,1977). Unfortunately in our study, we did not measure anyeffect of grazing pressure, but it might have a potential rel-evance, as high abundances of herbivorous and omnivorousfishes were observed in the area (S. Beilfuss personal com-munication) in addition to diverse mesograzers, like amphi-pods, nudibranchs or polyplacophores, which were frequentlysighted within the turf algal.
122 A. Fricke et al.: Succession of algal communities in a coral reef
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Figure 5 Changes in species richness (S), evenness (J9), biomass and cover (%) during succession in 5 m water depth.Shared lower case letters indicate no significant differences between means (Tukey-Kramer post-hoc tests, p)0.05). Values are means"SD,ns4.
Figure 6 Changes in species richness (S), evenness (J9), biomass and cover (%) among different water depths (5–25 m).Shared lower case letters indicate no significant differences between means (Tukey-Kramer post-hoc tests, p)0.05). Values are means"SD,ns4.
A. Fricke et al.: Succession of algal communities in a coral reef 123
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Conclusion
Interestingly, although the Caribbean coral reefs have strong-ly changed in structure and organization (Knowlton 2001,McCook et al. 2001, Hoegh-Guldberg et al. 2007), turf veg-etation has the same primary succession pattern as it did 30years ago (Wanders 1977), a pattern characterized by highspecies diversity. As the early steps seem to be relativelyconsistent, the older successional stages appear to be affectedby a variety of different environmental factors connectedwith water depth. It is crucial to address these potentialchanges in algal species composition, as many species-spe-cific coral-alga interactions have been observed in differentfield studies (Jompa and McCook 2003, Titlyanov and Tit-lyanova 2008).
Consequently, it is essential to identify the key playerswithin algal turf at the lowest possible taxonomic level, rath-er than to work with the entire functional group of turf algae.Furthermore, as not only filamentous algae and Cyanobac-teria, but also other organisms, like benthic foraminiferansor frondose and fleshy macroalgae (e.g., Laurencia spp.,Chondria spp. Dictyotales) are found within these mixedassemblages, algal turf might even serve as ‘‘retreat areas’’for certain species, which would disperse out into other hab-itats as soon as environmental conditions change.
Due to increasing anthropogenically-driven environmentalchange and the connected reorganization of coral reef eco-systems (Mumby and Steneck 2008, Diaz-Pulido et al. 2009),a better understanding of the processes shaping and drivingthe algal turf will become increasingly important for projec-tions of the future state of coral reef ecosystems.
Acknowledgements
We like to thank especially Prof. Rolf Bak (NIOZ, Texel), who gaveus an in-depth introduction to the field site. For kind assistance withdiving and field work we like to thank Dr. Maggy Nugues (ZMTBremen), Julia Kesting and Danielle Lommen. For taxonomical helpand support, we like to thank especially Prof. Tamara Titlyanova.Furthermore, we thank Prof. Angela Wulff, Prof. Pamela HallockMuller, Alexander V. Rzhavsky, and Dr. Birgit Heyduck-Soller. Weare grateful to the staff of the CARMABI foundation: Dr. Mark J.A.Vermeij, Dr. Adolphe Debrot, Carlos Winterdaal, Oscar Frans, SislinRosalia et al. for friendly support. We also like to thank MartinNowak and the workshop-team of the University of Bremen fortechnical support. This study was supported by the Bremen Inter-national Graduate School for Marine Sciences (GLOMAR) that isfunded by the German Research Foundation (DFG) within the frameof the Excellence Initiative by the German federal and state gov-ernments to promote science and research at German universities.
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Received 17 June, 2010; accepted 26 January, 2011; online first 11March, 2011
