Knowledge gaps in tropical Southeast Asian seagrass systems

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

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Estuarine, Coastal and Shelf Science

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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

* Corresponding author. The University of WesterPerth, Western Australia 6009, Australia.

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

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

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.

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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

n Australia, 35 Stirling Hwy,

Ooi).

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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),

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

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

Fig. 1. Location of spot collection points in the seagrass meadows of Pulau Tinggi, off the sowhere there was no seagrass and only sediment samples were collected.

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).

uth east coast of Peninsular Malaysia. Numbered points have seagrass. A, B, and C are

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

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

Table 1Study area, taxon (with dominance levels as specified in source references), habitat, hypothesized driver, level of study, and source of ISI-cited publications on Southeast Asian seagrasses between 1986 and 2009. Levels of studyare molecule (e.g. ecophysiological and biochemical processes), ramet (e.g. shoot and root measurements), canopy (e.g. shoot density, biomass, cover), and landscape (e.g. patch shape, size, fragmentation). In cases where waterdepth is not specified but Enhalus acoroides is present, it is designated as a ‘shallow’ area.

Study area Taxon (1, 2, 3, order of dominance) Habitat Driver Level of study Source

MalaysiaTeluk Kemang,

Negeri SembilanHO, HU, HD Backreef, 1.5e2 m depth N.R. (new record of H. decipiens) Ramet Japar Sidik et al., 1995

Kemaman, Terengganu e Estuary, intertidal Environmental forcing - reproductionof H.beccarii

Ramet Muta Harah et al., 1999

Malaysia N.R. N.R. N.R. (description of H. uninervisand H. pinifolia)

Ramet Japar Sidik et al., 1999

Port Dickson,Negeri Sembilan

CS Backreef, 0.5e2 m depth Light effects on C. serrula photosynthesis Molecule Abu Hena et al., 2001

Pengkalan Nangka,Kelantan

HB Estuary, intertidal N.R. (reproduction of H. beccarii) Ramet Muta Harah et al., 2002

Malaysia N.R. N.R. N.R. (review of distribution) N.R. Japar Sidik et al., 2006Pulau Gaya, Sabah HU, CS, CR Backreef, 0.7 m depth Sediment e silt-clay & turbidity Rametecanopy Freeman et al., 2008

CS, CR HU, TH, HO Backreef, 0.5 m depth Sediment e silt-clay & turbidity Rametecanopy Freeman et al., 2008

PhilippinesSilaqui island, northwest Luzon EA, CS, TH, HU Reef flat, shallow Urchin grazing Canopy Klumpp et al., 1993

TH1, EA2, CR3, CS,SI, HU, HO

Reef flat, 0.5e3 m depth Interspecific interaction Ramet Vermaat et al., 1995

TH1, EA2, CR3, CS, SI, HU, HO Reef flat, sheltered, 0.8 m depth Nutrients e N and P limitation onT. hemprichii,E. acoroides and C. serrulata

Moleculeerametecanopy Agawin et al., 1996

TH1, EA2, CR3, CS, SI, HU, HO Reef flat, 0.8 m depth Sediment - burial Canopy Duarte et al., 1997TH1, EA2, CR3, CS, SI, HU, HO Reef flat, 0.8 m depth N.R. (flowering frequency) Canopy Duarte et al., 1997TH1, EA2, CR3, CS, SI, HU, HO Reef flat, <3 m depth Sediment e siltation and

light penetrationCanopy Bach et al., 1998

TH1, EA2, CR3, CS, SI, HU, HO Reef flat, 0.8 m depth N.R. (belowground biomass) Rhizosphere Duarte et al., 1998TH1, EA2, CR3, CS, SI, HU, HO Reef flat, 1.5 m depth Sediment - anoxia Canopy Terrados et al., 1999TH1, EA2, CR3, CS, SI, HU, HO Reef flat, 1 m depth Sediment e N and P limitation

on E. acoroidesMoleculeerametecanopy Terrados et al., 1999

TH1, EA2, CR3, CS, SI, HU, HO Reef flat, 0.8 m depth Interspecific competition Canopy Duarte et al., 2000TH1, EA2, CR3, CS, SI, HU, HO Reef flat, 0.8 m depth Environmental forcing - T. hemprichii,

E. acoroides and C. serrulataMoleculeeramet Agawin et al., 2001

TH1, EA2, CR3, CS, SI, HU, HO Reef flat, 0.5 m depth Sediment - siltation, porewatersulphide on C. rotundata

Ramet - canopy Halun et al., 2002

TH, EA, CR, CS Reef flat, shallow N.R. (sediment depositionand production)

Canopy Gacia et al., 2003

TH Reef flat, shallow Burial effects on seeds and seedlings Ramet Rollón et al., 2003EA Reef flat, shallow Burial effects on seeds and seedlings Ramet Rollón et al., 2003TH, CS Reef flat, 1.5 m depth Light Moleculeeramet Gacia et al., 2005

Santiago Island,northwest Luzon

EA, CS, TH, HU Reef flat, shallow Urchin grazing Canopy Klumpp et al., 1993CR, EA, HU Coral rock with silt overlayer,

1 m depthInterspecific interaction Ramet Vermaat et al., 1995

TH1, EA2, CR3, CS, SI, HU, HO Reef flat, exposed, 0.6 m depth Nutrients e N and P limitationon T. hemprichii,E. acoroides and C. serrulata

Moleculeeramet Agawin et al., 1996

EA, CS, HU, HO, TH, Reef flat, < 1.0 m depth Sediment e siltation andlight penetration

Canopy Bach et al., 1998

TH1, EA2, CR3, CS, SI, HU, HO Reef flat, exposed, 0.6 m depth N.R. (belowground biomass) Rhizosphere Duarte et al., 1998EA, CS, CR, TH, HU, HO Reef flat, <2.0 m depth Sediment e siltation and

light penetrationCanopy Bach et al., 1998

e Reef flat, <1.0 m depth Sediment e N and P limitationon E. acoroides

Moleculeerametecanopy Terrados et al., 1999

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Table 1 (continued)


TH, EA, CR, CS Reef flat, shallow N.R. (sediment depositionand production)


Cape Bolinao,northwest Luzon

EA,CS Reef flat, highly silted area, <0.5 m Sediment e siltation andlight penetration

Canopy Bach et al., 1998

TH1, EA2, CR, CS,SI, HU, HO

Estuary and reef lagoon,intertidal to 3 m depth

Sediment - siltation Canopy Terrados et al., 1998

e Highly silted area, <1.0 m Sediment e N and P limitationon E. acoroides

Moleculeerametecanopy Terrados et al., 1999

TH1, EA2, CR, CS, SI, HU, HO Reef flat, <3.0 m depth Nutrient allocation to plant parts Ramet Terrados et al., 1999TH, EA N.R. N.R. (propagule dispersal of

T. hemprichii and E. acoroides)Ramet Lacap et al., 2002

CS, CR, EA Shallow N.R. (sediment depositionand production)


TH1, EA2, CR, CS, SI, HU, HO Reef flat, shallow Patch fragmentation onE. acoroides reproduction

Canopyelandscape Vermaat et al., 2004

Daco island,off Negros Oriental

e Reef flat, shallow Tidal exposure & day lengthon E. acoroides

Ramet Estacion andFortes, 1988

Negros Oriental TH, EA, CR, CS, HU, HP, SI, HO Reef flat, shallow N.R. (leaf productivity, biomass) Moleculeerametecanopyerhizosphere

Tomasko et al., 1993

Puerto Galera,Mindoro island

TH1, EA, CR, CS, SI, HU, HO Reef flat, <3.0 m depth Sediment - siltation Canopy Terrados et al., 1998TH1, EA, CR, CS, SI, HU, HO Reef flat, <3.0 m depth Nutrient allocation to plant parts Ramet Terrados et al., 1999

Palawan island TH, EA, CR, CS, SI, HU, HO <3.0 m depth Sediment - siltation Canopy Terrados et al., 1998TH, EA, CR, CS, SI, HU, HO, HO <3.0 m depth Nutrient allocation to plant parts Ramet Terrados et al., 1999HU, CS, EA Shallow N.R. (sediment deposition

and production)Canopy Gacia et al., 2003

EA Shallow N.R. (sediment depositionand production)


VietnamNha Trang TH High energy coast, shallow N.R. (sediment deposition

and production)Canopy Gacia et al., 2003

EA High energy coast, shallow N.R. (sediment depositionand production)


TH, EA High energy coast, shallow N.R. (sediment depositionand production)


Gia Luan, Ha Long Bay HO1, ZJ1, HD Pristine bay, 1.0e2.0 m depth Seasonal turbidity Rametecanopy Huong et al., 2003

ThailandTalibong island, Southwest Thailand TH, EA, CR, CS, SI, HU, HO <3.0 m depth Sediment - siltation Canopy Terrados et al., 1998

TH, EA, CR, CS, SI, HU, HO <3.0 m depth Nutrient allocation to plant parts Ramet Terrados et al., 1999EA, TH, HO 0.5e1.5 m depth Sediment e sulphide intrusion Rametecanopy erhizosphere Holmer et al., 2006TH, HO, CR 0.3 m depth Sediment e sulphide intrusion Rametecanopy erhizosphere Holmer et al., 2006HO 0.8 m depth Sediment e sulphide intrusion Rametecanopy erhizosphere Holmer et al., 2006

Bang Rong, Phuket island,Southwest Thailand

TH1, EA, HU, HO <3.0 m depth Sediment - siltation Canopy Terrados et al., 1998TH1, EA, HU, HO <3.0 m depth Nutrient allocation to plant parts Ramet Terrados et al., 1999CR, TH, EA Intertidal sand flat Nutrients Moleculeecanopy Holmer et al., 2001

Haad Chao Mai, Trang,Southwest Thailand

HO1, CR, CS, EA Intertidal flat Herbivory e dugong grazing Canopy-landscape Nakaoka and Aioi, 1999HO, TH, EA, CR, HU Intertidal Intra- and interpatch interaction Rametecanopyerhizosphere-

landscapeNakaoka andIizumi, 2000

HO, TH, EA, CS, HU River mouth, <3 m depth Sedimentation and light attenuationeffects on Cymodocea

Rametecanopy Tanaka andNakaoka, 2006

CS Fine sand N.R. (iron plaqueon C. Serrulata roots)

Ramet Povidisa et al., 2009

Ban Pak Meng, Trang,Southwest Thailand

CS Fine sand N.R. (iron plaque onC. serrulata roots)

Ramet Povidisa et al., 2009

Phangnga,Southwest Thailand

e River mouth, shallow N.R. (internal nutrient concentrationin E. acoroides

Moleculeeramet Yamamuro et al., 2004

CS, CR, EA, SI, HU, HP, HO River mouth, <2 m depth Sedimentation and light attenuationeffects on Cymodocea

Rametecanopy Tanaka andNakaoka, 2006

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Table 1 (continued)


IndonesiaBarang Lompo,

Southwest SulawesiTH, EA Reef flat, carbonate sand, <1 m depth N.R. (sediment and

porewater nutrients)N.R. Erftemeijer and

Middleburg, 1993Reef flat, carbonate sand, <1 m depth N.R. (primary production rates) Ramet Erftemeijer et al., 1993

TH, EA Reef flat, carbonate sand, <1 m depth Tidal exposure & water motion Rametecanopy Erftemeijer andHerman, 1994

TH, EA Reef flat, carbonate sand, <1 m depth Nutrients Ramet Erftemeijer et al., 1994TH, EA Reef flat, carbonate sand, <1 m depth N.R. (nutrient cycling) Molecule Erftemeijer and

Middelburg, 1995TH, EA, CR Carbonate sand and coral

rubble, intertidalN.R. (nutrient uptake by T. hemprichii) Molecule Stapel et al., 1996

TH, EA, CR Carbonate sand and coralrubble, intertidal

N.R. (nutrient resorption) Ramet Stapel andHemminga, 1997

TH, EA Reef flat, carbonate sand, <1 m depth Tidal exposure effects on T. hemprichiibiomass and nutrients

Moleculeeramet Stapel et al., 1997

TH1, EA Reef flat, carbonate sand, <1 m depth N.R. (nitrogen retention in T. hemprichii) Ramet Stapel et al., 2001e Coarse carbonates, 10e30 m depth N.R. (new species H. sulawesii) Ramet Kuo, 2007

Langkai island,Southwest Sulawesi

e Reef flat, carbonate sand,intertidal

N.R. (nutrient uptake by T. hemprichii) Molecule Stapel et al., 1996

HO Forereef, 12e16 m depth Light effects on primaryproduction of H. ovalis)

Moleculeeramet Erftemeijer andStapel, 1999

e Coarse carbonates, 10e30 m depth N.R. (new species H. sulawesii) Ramet Kuo, 2007Gusung Tallang,

Southwest SulawesiEA Coastal mudflat,

terrigenous mud, <1 m depthN.R. (primary production rates) Ramet Erftemeijer et al., 1993

EA Coastal mudflat,terrigenous mud, <1 m depth

Tidal exposure & water motion Rametecanopy Erftemeijer andHerman, 1994

EA Coastal mudflat,terrigenous mud, <1 m depth

N.R. (nutrient cycling) Molecule Erftemeijer andMiddelburg, 1995

EA1, TH Sandy terrigenous mud,intertidal mudflat

N.R. (nutrient uptake by T. hemprichii) Molecule Stapel et al., 1996

EA1, TH Sandy terrigenous mud,intertidal mudflat

N.R. (nutrient resorption) Ramet Stapel andHemminga, 1997

Bone Batang island,Southwest Sulawesi

TH, HU, CR Reef flat N.R. (organic N uptake rates) Molecule Vonk et al., 2008aTH, HU, CR, HO Reef flat Urchin herbivory Rametecanopy Vonk et al., 2008bTH, HU, CR, EA, HO Reef flat N.R. (N cycling) Rametecanopy Vonk and Stapel, 2008TH, HU, CR, SI Reef flat N.R. (root architecture) Ramet Kiswara et al., 2009e Forereef, Coarse carbonates, 10e30 m depth N.R. (new species H. sulawesii) Ramet Kuo, 2007

Hoga Island, Wakatobi Park,Southeast Sulawesi

TH, EA, CR, HO Intertidal N.R. (habitat complexity andshrimp communities)

Canopy Unsworth et al., 2007

TH, EA, CR, HO Intertidal N.R. (scarid fish herbivory) Canopy Unsworth et al., 2007Selayar group of islands,

South SulawesiEA, TH, CS, CR, SI, HU, HP, HO, TC <1.0e7 m depth N.R. (heavy metals in seagrasses) Ramet Nienhuis, 1986TH, EA, CR <2 m depth N.R. (production and

consumption rates)Moleculeeramet Lindeboom and

Sandee, 1989Taka Bone Rate archipelago,

South SulawesiEA, TH, CS, CR, SI, HU, HP, HO, TC <1.0e7 m depth N.R. (heavy metals in seagrasses) Ramet Nienhuis, 1986HU1, HO 1.25e7.45 m depth N.R. (production and


Sandee, 1989Tambunan island,

off Komodo islandEA, TH, CS, CR, SI, HU, HP, HO, TC <1.0e7 m depth N.R. (heavy metals in seagrasses) Ramet Nienhuis, 1986TH1, EA <1.0 m depth N.R. (production and


Sandee, 1989Sanggar Bay, Sumbawa island EA, TH, CS, CR, SI, HU, HP, HO, TC <1.0e7 m depth N.R. (heavy metals in seagrasses) Ramet Nienhuis, 1986

HU, SI <1.3 depth N.R. (production andconsumption rates)

Moleculeeramet Lindeboom andSandee, 1989

Banten Bay, West Java EA1, TH, CR, CS, HU, SI, HM Coral debris, sand-muddysubstrate

N.R. (seagrass spatialdatabase development)

Canopy-landscape Douven et al., 2003

EA Mud to coral substrate, < 1 m depth Turbidity & epiphytes Ramet Kiswara et al., 2005CR, CS, HU, SI, EA, TH Mud to coral substrate, < 1 m depth N.R. (root architecture) Ramet Kiswara et al., 2009

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Table

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

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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.


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.

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


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

Table 3Seagrass and physical characteristics in Pulau Tinggi, southeast Peninsular Malaysia, 15 A

Mean � s

Seagrass variables - communitySpecies richness (m�2) 2.00 � 1.0Aboveground biomass (g DW m�2) 45.72 � 1Belowground biomass (g DW m�2) 46.65 � 6Total biomass (g DW m�2) 92.38 � 2Shoot density (m�2) 1869.70 �Seagrass variables e by species

Halophila ovalisShoot density (m�2) 1454.57 �Aboveground biomass (g DW m�2) 11.41 � 8Belowground biomass (g DW m�2) 14.11 � 1Total biomass (g DW m�2) 25.53 � 1

Halodule uninervisShoot density (m�2) 861.67 �Aboveground biomass (g DW m�2) 11.25 � 5Belowground biomass (g DW m�2) 31.67 � 1Total biomass (g DW m�2) 42.91 � 2

Cymodocea serrulataShoot density (m�2) 95.50 � 1Aboveground biomass (g DW m�2) 2.98 � 5.0Belowground biomass (g DW m�2) 10.50 � 1Total biomass (g DW m�2) 13.47 � 9

Syringodium isoetifoliumShoot density (m�2) 439.30 �Aboveground biomass (g DW m�2) 4.46 � 3.7Belowground biomass (g DW m�2) 12.83 � 9Total biomass (g DW m�2) 17.28 � 5

Physical variables

Water depth (m) 5.19 � 2.3Silt-clay (% DW) 2.28 � 2.4Sand (% DW) 92.55 � 6Gravel (%DW) 5.20 � 6.2Organic matter (% DW) 2.56 � 0.3Total carbon (% DW) 9.44 � 1.6Organic carbon (% DW) 0.22 � 0.3Inorganic carbon (% DW) 9.24 � 1.7PAR (mmol m�2 s�1) at 3 m (% SI) 405.80 �PAR (mmol m�2 s�1) at 6 m (% SI) 227.60 �PAR (mmol m�2 s�1) at 10 m (% SI) 162.06 �

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

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.

prile15 May 2009.

tandard deviation Minimum-Maximum

0 1.00e4.0045.07 3.30e754.208.11 2.60e345.6009.58 6.40e1099.90936.77 350.20e3336.30

795.47 159.20e2451.30.90 1.60e32.000.73 0.7e38.105.53 2.30e56.20

371.91 127.34e2005.60.78 2.36e31.529.16 6.89e64.938.56 9.40e88.90

00.70 31.83e318.350 1.04e5.646.89 0.88e35.58.52 2.70e44.20

291.10 178.28e700.377 2.79e6.13.45 8.54e17.11.19 11.30e23.20

7 <1.00e10.723 0.25e10.45.09 74.02e98.688 0.40e25.875 1.77e3.403 4.32e11.188 0.09e2.024 4.16e11.0098.90 (37.30 � 3.30) 134.90e554.0052.60 (20.10 � 1.30) 85.3e312.2034.90 (15.00 � 1.50) 65.6e210.00


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

Table 4Mean shoot density and biomass of selected Southeast Asian seagrasses. All are multispe

Species/Location Shoot density(shoots m�2)

Abovegroun(g DW m�2)

Halophila ovalisPulau Tinggi (this study) 1455 � 795 11.4 � 8.9Bolinao, Phil.a,b,c,d,e 12e388 3.1Pto Galera, Phil.d e 3.9El Nido, Phil.d e 0.6Flores Sea, Indon.f 69 � 117 e

Langkai island, Indon.g 1099 � 195 e

Halodule uninervisPulau Tinggi (this study) 862 � 372 11.3 � 5.8Bolinao, Phil.a,b,c,d,e 8e1064 29.4Pto Galera, Phil.d e 4.9El Nido, Phil.d e 4.2Flores Sea, Indon.f 2847 � 5689 e

Langkai island, Indon.g e e

Cymodocea serrulataPulau Tinggi (this study) 96 � 101 3.0 � 5.0Bolinao, Phil.a,b,c,d,e 2e214 31.7Pto Galera, Phil.d e 4.3El Nido, Phil.d 696 � 767 5.7Flores Sea, Indon.f e e


Syringodium isoetifoliumPulau Tinggi (this study) 439 � 291 4.5 � 3.8Bolinao, Phil.a,b,c,d,e 4e396 33.0Pto Galera, Phil.d e 1.5El Nido, Phil.d e e

Flores Sea, Indon.f 2504 � 1736 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).

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

cific meadows except for Langkai island.

d biomass Belowground biomass(g DW m�2)

Total biomass(g DW m�2)

14.1 � 10.7 25.5 � 15.50.1e0.9 0.2e e

e e

e e

e 10.93 � 2.65

31.7 � 19.2 42.91 � 28.72.8e6.7 7.3e e

e e

e e

e e

10.5 � 16.9 13.5 � 9.5e 2.7e e

e e

e e

e e

12.8 � 9.5 17.3 � 5.21.8e2.1 14.3e e

e e

e e

e e


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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