Does transported seagrass provide an important trophic link in unvegetated, nearshore areas?

Estuarine, Coastal and Shelf Science 63 (2005) 633e643

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Does transported seagrass provide an importanttrophic link in unvegetated, nearshore areas?

Glenn A. Hyndes*, Paul S. Lavery

Centre for Ecosystem Management, School of Natural Sciences, Edith Cowan University, 100 Joondalup Drive,

Joondalup, WA 6027, Australia

Received 16 August 2004; accepted 17 January 2005

Abstract

The contribution of detritus from seagrass and other primary producers to faunal production in unvegetated nearshore areas was

examined primarily using stable isotopes. Fish, macroinvertebrates, meiofauna and primary producers (seagrasses, macroalgae,seston and benthic microalgae) were sampled from sites in south-western Australia. All samples were analysed for d13C and d15Nvalues and fish gut contents were determined. d13C values for seagrasses in the region were high compared to other macrophytes,

ranging from 49.9 to �8.2& compared to �19.8 to �12.6& for macroalgae. The d15N values ranged between 4.0 and 7.7& for thered, brown and green algae, and between 3.2 and 5.9& for seagrasses. Seston and benthic microalgae samples had a mean d13Cvalue of �12.8 and �14.0&, respectively, and their d15N values were comparable to the macroalgae. All invertebrate fauna hadmean d13C values considerably lower than seagrasses. However, individual samples harpacticoid copepods and polychaetes had

a value as high as �11.7&. d15N values for consumers were higher than those of the primary producers, except for copepods andamphipods. The d13C values for fish had a relatively small range, between �16.6 and �13.1&, and the d15N values of fish wereelevated compared to the invertebrates and primary producers, ranging mostly between 10.0 and 12.6&. Mixing model analysis

based on d13C values indicated that seagrass ranked low as a likely carbon source for all invertebrates other than harpacticoidcopepods at a single site and some samples of polychaetes. The d13C values for fish were similar to those of a combination ofharpacticoid and calanoid copepods, amphipods and polychaetes. The consumption of harpacticoid copepods by some fish species

indicates that Amphibolis and Posidonia species in south-western Australia can contribute to the food web of unvegetated nearshoreareas as detritus, but brown algae is likely to make a greater contribution. At least for the time of year that was sampled, the flow ofdetrital seagrass material into the foodweb may be mediated by specific detrivores, in this case harpactacoid copepods, rather than

by all detritivores.� 2005 Elsevier Ltd. All rights reserved.

Keywords: detritus; fish community; dietary analysis; stable isotopes; Australia; Posidonia; Amphibolis

1. Introduction

Seagrass meadows occur in many coastal environ-ments around the world where they often provide animportant habitat for many fish species (e.g. Thayeret al., 1975; Orth and Heck, 1980; Ferrell and Bell, 1991;

* Corresponding author.

E-mail address: [email protected] (G.A. Hyndes).

0272-7714/$ - see front matter � 2005 Elsevier Ltd. All rights reserved.

doi:10.1016/j.ecss.2005.01.008

Sogard and Able, 1991; Connolly, 1994). Seagrass cancontribute to the food web in these ecosystems eitherdirectly through grazing on seagrass leaves (Valentineet al., 1997, 2000) or indirectly through grazing on theattached epiphytic algae (Kitting et al., 1984). However,the food webs in these ecosystems are generallyconsidered to be detrital-based (Benner et al., 1984;Cebrian et al., 1997; Vizzini et al., 2002). Unlike seagrassmeadows, unvegetated substratum is often considereda ‘‘poor substitute’’ as a habitat for fauna, due to its lack

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634 G.A. Hyndes, P.S. Lavery / Estuarine, Coastal and Shelf Science 63 (2005) 633e643

of structural complexity and lower productivity. Despitethis, nearshore unvegetated habitats can contain nu-merous fish (e.g. Ayvazian and Hyndes, 1995; Hyndeset al., 1996; Clark, 1997; Lenanton, 1982; Ruiz et al.,1993), indicating that fish production can be high.

One major mechanism of sustaining productivity inthe unvegetated nearshore waters is likely to be theimportation of primary production from adjacentvegetated habitats, for example seagrass and algae thathave been dislodged during storm events (Kirkman andKendrick, 1997). Accumulations of detached macro-phytes along the shoreline have been shown to enhancethe habitat function of unvegetetated nearshore areas byincreasing structural complexity and food availability(Lenanton et al., 1982; Robertson and Lenanton, 1984).The transient nature of detached macrophyte accumu-lations may limit the dependence of fish species on themas habitat, though the degradation of this material islikely to provide an important nutrient source (seeKirkman and Kendrick, 1997). The transportation ofplant material between coastal habitats may providea trophic link, with secondary production and habitatavailability in unvegetated nearshore areas being sup-ported by primary production from elsewhere.

Only a few studies have addressed the issue ofwhether seagrass contributes to fish or decapod pro-duction in areas outside of seagrass meadows inestuarine (Kitting et al., 1984; Loneragan et al., 1997),coastal embayment (Marguillier et al., 1997; Lepointet al., 2000) and continental shelf (Thresher et al., 1992;Davonport and Bax, 2002) ecosystems. All of thesestudies have used stable isotope techniques to trace theassimilation of seagrass through the food chain, but themajority have only examined one species of consumerdue to their focus on particular fisheries species.

In south-western Australia, Posidonia and Amphibolisspecies are dominant meadow-forming seagrasses. Theseand other seagrasses are conspicuous and significantcontributors to benthic primary production, accountingfor about 70% of the vegetated benthic habitat in theregion surrounding the study site (Dept. Environ.Protection, unpublished data). They are therefore pre-sumed to make a significant contribution to the detritalpool, though the trophic significance of this is poorlystudied. These seagrasses have high above-groundbiomass and rates of leaf turnover in the order of 5e200 days (Marba and Walker, 1999), providing a con-tinual supply of detached leaf material. Much of thedetached material is transported onto sandy-beachecosystems (Hansen, unpublished data) or accumulatesin deeper unvegetated nearshore areas. It has long beensuspected that this material plays an important role insupporting food webs in the unvegetated, nearshoreecosystems. The main aim of the present study was,therefore, to establish whether seagrasses contribute tothe food web in unvegetated, nearshore habitats of

coastal embayments. The d13C and d15N values of thepredominant primary producers (seagrass, macroalgae,phytoplankton and benthic microalgae), that werepresent or likely to accumulate in these areas, weredetermined on living material to establish the majorsource(s) of carbon and nitrogen for the fauna ofunvegetated nearshore waters. To help interpret theisotope results, dietary data were also collected and,where possible, complemented with published dietarydata.

2. Materials and methods

2.1. Field locations and sample collection

Fish (juveniles of larger species and both juvenilesand adults of smaller species) were collected using a21 m seine net (3 and 9 mm mesh in the wings andpocket, respectively) during late summer and autumn(February to April) 2001 in unvegetated nearshore areasat five sites within Cockburn Sound, Warnbro Soundand Safety Bay in south-western Australia (Fig. 1).Hansen (unpublished data) and Lenanton et al. (1982)have described the transient, but regular, accumulationof wrack on beaches adjacent to the study area. Largenumbers of juveniles representing numerous speciesrecruit and remain in the nearshore waters for pro-tracted periods during late spring to early autumn(Hyndes et al., 1996; Hyndes, unpublished data). Thepresent study was carried out towards the end of thisperiod when the juveniles are likely to have occupied theunvegetated habitats for several weeks to a few months.Furthermore, the study was restricted to those species offish that typically occur over unvegetated areas (Ayva-zian and Hyndes, 1995; Hyndes, unpublished data).Where possible, three individuals of each species werecollected at each site. Fish were placed in an ice slurryand returned to the laboratory for processing.

Potential prey were collected at each site using a250 mm mesh dip net for copepods and amphipods anda sediment core (90 mm internal diameter) for poly-chaetes and bivalve molluscs. Dip netting was carriedout over a broad area (O1000 m2) within each site. Dueto the small size of copepods and amphipods, allindividuals within each sample were pooled for eachtaxonomic group (i.e. gammeridean amphipods, har-pacticoid copepods and calanoid copepods) to provideenough material for analyses. For larger prey, such aspolychaetes, up to three individuals were collected fromeach site. Copepods and amphipods were placed insample jars and placed in a cool storage container fortheir return to the laboratory. Polychaetes were ex-tracted from the sediment using sieves and similarly,placed in sample jars on ice. Since no molluscs werecollected using either this method or a shovel, they were

635G.A. Hyndes, P.S. Lavery / Estuarine, Coastal and Shelf Science 63 (2005) 633e643

not considered to form a major part of the infauna atthe study sites.

Fresh (green) seagrass leaves and detached macro-algae were collected from the macrophyte wrack at eachsite. The same material was also collected from nearbyoffshore seagrass meadows (living seagrass leaves) andreefs (attached macroalgae). These meadows and reefswere distributed widely throughout the study region atdistances of hundreds of metres to several kilometresfrom the nearshore sampling sites. This encompassedthe spatial scale and likely hydrodynamic connectivity ofthe region and ensured variability in the d13C and d15Nvalues of all the primary producers in the broader regionwas incorporated into the study. Epiphytic algae werenot collected or analysed since these are known to besimilar in composition to reef algae (Phillips et al., 1997;Lavery and Vanderklift, 2002), making discriminationbetween these two sources of algae difficult. Instead, it

Fig. 1. Map showing the location of sampling sites for fish and

decapods and their potential prey and primary food sources in south-

western Australia. Symbols indicate the organisms sampled at each

site: C Z fish and decapods and their potential prey and seston;

- Z seagrass and epiphytes; , Z reef algae; and X Z benthic

micro-algae.

was assumed that the isotopic signature of both reef andepiphytic algae were the same.

A sample of seston (phytoplankton and detritus) wascollected from each nearshore site by pumping 1000 l ofwater sequentially through a 63 mm sieve and 20 mmplankton net. Each sample retained in the plankton netwas placed into a sample jar and placed on ice in a darkcontainer. The sample from one site was not retaineddue to the large contribution of particulate detritalmaterial in the sample. Since benthic microalgae wereonly visible at one site, sampling of this primaryproducer was restricted to this single site. The micro-algal sample was collected over a wide area usinga syringe to carefully suck up the surface layer of algae(with some detritus) material, after which, the samplewas placed on ice and returned to the laboratory.Subsequent examination by light microscopy showedthat the samples contained approximately 70% by areaof benthic microalgae.

2.2. Sample preparation

Muscle tissue was dissected from each fish anddecapod for stable isotope analyses. Polychaetes,amphipods and copepods were kept alive in filteredand aerated seawater overnight to clear their guts.Seagrass leaves were scraped using a razor blade toremove epiphyte material. To separate benthic micro-algae from the sediment, each sample was placed ina beaker containing filtered seawater and agitated usinga magnetic stirrer. The solution was briefly allowed tosettle prior to pouring off the supernatant containing thesuspended algal cells.

All samples were rinsed in filtered seawater, dried at60 �C until dry (approx. 24 h) and then ground usinga mortar and pestle. For samples of small crustaceansand scraped seagrass leaves, a sub-sample was acidtreated in 1% HCl to remove carbonates for d13Canalyses, and the remainder was retained for d15Nanalysis.

2.3. Stable isotope analyses

The d13C and d15N values of dried and weighedsamples (5e12 mg) of plant and animal material weredetermined using an ANCA-NT/20-20 stable isotoperatio mass spectrometer (Europa Scientific, Crewe, UK),expressed as the relative per mil (&) difference betweenthe sample and the conventional standards Peedeebelemnite limestone and N2 in air, respectively. Refer-ence standards of flour and glutamic acid were used inall analyses with an analytical precision of 0.1&. For thesamples of some consumers that required acid washing(particularly harpacticoid copepods), insufficient mate-rial was available for both d13C and d15N. In those cases,


analyses focused on d13C. All other samples we analysedsimultaneously for d13C and d15N.

2.4. Data analyses

Due to the patchy distribution of primary producersand consumers throughout the study region, meaningfulcomparisons could not be made at the site level. For thisreason, comparisons of stable isotope data have beenrestricted to the whole system where sites encompass thevariability within that system. Mean d13C and d15Nvalues were calculated for each species or group ofprimary producer, invertebrate and fish.

The mixing model Isosource (Phillips and Greg,2003) was used to estimate the potential bounds ofcontribution of the 10 primary producer groups to thefirst order consumers. Due to the restriction of Isosourceto 10 sources, representatives of the seagrasses andbrown, red and green algae were used in the analyses(contributions from the red and green algae wereassumed to be derived from either detached reef algaeor epiphytic algae on detached seagrass leaves). Foreach primary consumer, the frequency and range of thepossible contribution (0e100%) of each possible source(primary producer) at increments of 1% were de-termined. Solutions were considered feasible wherecombinations summed to within 0.1&. As recommen-ded by Phillips and Greg (2003), the range between 1e99% is given, as the tails of the distributions aresensitive to small numbers.

Mixing model analyses have been restricted to theprimary consumers, copepods, amphipods and poly-chaetes, as they graze either on plant or detrital materialand represent the product of 1e2 trophic steps. Theenrichment of d15N between trophic levels can be highlyvariable for marine invertebrates (Rolff, 2000; Vanderk-lift and Ponsard, 2003). Furthermore, d15N can increaselinearly with the logarithmic size of organisms (Rolff,2000), rather than in the step-wise increase per trophiclevel that is often assumed. For this reason, we have notused d15N values in the mixing model. Since d13C exhibitsminimal or no enrichment between trophic groups(Rolff, 2000; Staddon, 2004), we have restricted themixing model analyses to this isotope and not adjustedd13C values of consumers. For invertebrate groups, theIsosource model was initially run using the mean d13Cvalues. However, as some invertebrates displayed signif-icant among-sample variability in d13C values, the modelwas also run using the minimum and maximum d13Cvalues for groups with sample sizes of three or more.

2.5. Dietary analyses

The stomachs were removed from each fish collectedfor stable isotope analyses and stored in 70% ethanol.Where possible, each dietary item in each stomach was

identified to the lowest possible taxon (usually Class orOrder) under a binocular microscope. Due to theadvanced stage of digestion, the contribution of eachdietary item was recorded as its percentage contributionto the total volume of all dietary items present in eachstomach (Hyslop, 1980). The contribution by volume(%V) of each dietary item to the stomachs of all fishacross all sites was calculated for each species.

3. Results

3.1. Stable isotope values

Compared to the other macrophytes, d13C values forseagrasses were high, ranging from �9.9& for Posidoniaaustralis to �8.2& for Posidonia sinuosa (Table 1,Fig. 2). In comparison, the mean d13C values of redalgae in the study region ranged between �19.8 and�16.9& (Table 1, Fig. 2) and brown algae ranged from�18.1& for Ecklonia radiata to approximately �15.8&for Sargassum species. The green algae had higher d13Cvalues than red algae, but overlapped the range ofbrown algae. Ulva sp. and Codium duthiae were similarto those of the majority of brown algae (�17.1 and�15.5&, respectively), while the two Caulerpa specieshad higher d13C values (�12.6 and �13.4&). The d15Nvalues ranged between 4.0 and 7.7& for the red, brownand green algae, and between 3.2 and 5.9& forseagrasses.

Seston samples (phytoplankton and the 20e63 mmfraction of detrital material) had a mean d13C value of�12.8& (Table 1, Fig. 2). Similarly, benthic microalgae,which could only be collected from one site (Fig. 1), hada d13C value of �14.0&. The d15N values of benthicmicroalgae and seston fell within the range for macro-algae (Table 1, Fig. 2).

All fauna had d13C values considerably lower thanseagrasses and, with the exception of copepods andamphipods, all d15N values were high compared to theprimary producers. The mean d13C value for calanoidcopepods and gammaridean amphipods (�15.5 and�17.2&, respectively) were low relative to seagrass,green algae, seston and benthic microalgae (Table 1,Fig. 2). Harpacticoid copepods had a d13C value of�15.1&, slightly higher than those of amphipods andcalanoid copepods. It should be noted, however, thatthe d13C values of harpacticoid copepods were highlyvariable among sites, ranging from �18.7& to �11.8&(d15N values were not available for all sites), with theupper value approaching that of seagrasses. Polychaetesand the crab Portunus pelagicus had d13C values ofapproximately �14.6&, which were slightly higher tothose of calanoid copepods and amphipods, but hadelevated d15N values compared with all primaryproducers. Similar to harpacticoid copepods, the d13C


Table 1

Mean and standard error values of d15N and d13C of fish and decapods and their potential prey and primary food source in the unvegetated,

nearshore waters of south-western Australia

Species Code d15N d13C Sample

size

Number

of sitesMean 1SE Mean 1SE

Microalgae Seston (phytoplankton) Se 4.9 1.1 �12.8 3.2 4a 4

Benthic microalgae Bm 6.0 �14.0 1a 1

Seagrass Amphibolis griffithii Ag 4.4 0.3 �9.0 1.1 6 3

Posidonia australis Pa 3.2 0.4 �9.9 0.5 3 1

Posidonia coriacea Pc 4.3 0.7 �9.6 0.9 7 2

Posidonia sinuosa Ps 5.9 0.5 �8.25 0.4 3 2

Green algae Caulerpa flexilis Cf 5.5 0.5 �12.6 0.3 6 2

Caulerpa gemminata Cg 7.7 2.0 �13.4 0.3 6 2

Codium duthaeie Cd 4.8 0.1 �15.5 0.6 6 2

Ulva sp. Ul 5.7 0.2 �17.1 1.0 3 3

Red algae Hypnea sp. A Ha 6.8 1.6 �19.8 0.8 3 1

Hypnea sp. B Hb 5.4 0.4 �19.6 0.7 3 1

Rhodophyta sp. A Ra 6.8 2.4 �16.9 5.1 4 2

Rhodophyta sp. B Rb 6.5 1.4 �17.8 0.4 3 1

Brown algae Ecklonia radiata Er 5.3 0.3 �18.1 1.1 7 2

Sargassum sp. A Sa 5.7 0.8 �15.8 1.6 12 3

Sargassum sp. B Sb 5.7 0.3 �16.0 1.2 9 3

Invertebrates Amphipoda Am 7.3 0.7 �17.2 0.1 3a 3

Calanoid copepod Cc 4.9 �15.5 2a 2

Harpacticoid copepodb Hc 6.9 �15.1 1.4 4a 4

Ostracods Os �16.3 1a 1

Polychaeta Po 9.3 1.9 �14.8 0.9 11 3

Portunus pelagicus Pp 9.0 0.6 �14.4 1.0 3 2

Fish Aldrichetta forsteri Af 12.0 0.4 �16.6 0.3 3 1

Ammotretis elongatus Ae 10.4 1.2 �14.7 0.3 6 2

Ammotretis rostratus Ar 10.7 0.5 �14.5 1.2 6 2

Atherinomorus ogilbyi Ao 12.0 0.4 �15.9 0.2 3 1

Cnidoglanis macrocephalus Cm 11.5 0.2 �15.9 1.7 3 1

Favonigobius lateralis Fl 11.0 0.8 �13.1 0.3 3 1

Mugil cephalus Mc 12.6 0.5 �13.8 0.4 3 1

Pseudorhombus jenynsii Pj 10.6 1.0 �15.0 0.8 3 1

Rabdosargus sarba Rs 10.3 1.6 �13.9 0.9 7 3

Sillago bassensis Sa 11.1 1.1 �14.6 1.0 3 1

Sillago burrus Sb 9.5 1.5 �13.6 0.8 6 2

Sillago schomburgkii Ss 11.7 0.6 �13.8 0.2 5 2

Sillago vittata Sv 10.5 0.4 �14.3 0.8 9 3

Silliginodes punctata Sp 10.5 1.6 �14.0 0.8 11 4

a Sample comprised more than one organism.b d15N data available for only one of the four samples.

values for polychaetes were highly variable amongsamples, ranging from �17.3& to �11.7&. The d15Nfor calanoid copepods were lower than the amphipodsand harpacticoid copepods, which in turn, were lowerthan the polychaetes and P. pelagicus (Table 1, Fig. 2).

The d13C values for fish had a relatively small range,between �16.6 and �13.1& (Fig. 2). Those forAldrichetta forsteri, Cnidoglanis macrocephalus andAtherinomorus ogilbyi were low (�16.6 to �15.9&)compared to the remaining fish species. This remaininggroup of fish, which included Sillaginodes punctata,Sillago burrus, Favonigobius lateralis and Rhabdosargussarba, had values ranging from �15.0 and �13.1&(Table 1, Fig. 2). While the d15N values of fish weretypically elevated compared to the invertebrates andprimary producers, they formed a broad group with the

majority ranging between 10.0 and 12.6& (Table 1,Fig. 2).

Using the mean d13C values, the mixing model resultsindicated that seagrass ranked low in terms of itscontribution to amphipods, calanoid and harpacticoidcopepods and polychaetes (Fig. 3). For amphipods,green (Ulva), red and brown (Ecklonia) algae rankedhigh, while seston and the majority of algae ranked highfor calanoid and harpacticoid copepods and polychaetes(Fig. 3). Since 13C varied widely for the different samplesof harpacticoid copepods (�18.7 to �11.8&) andindividual polychaetes (�17.3 to �11.7&), separatemixing model analyses were run on the extreme values.For both groups of organisms, macroalgae rated highfor the lower values (�18.7 and �17.3&), with Hypneabeing particularly prominent for harpacticoid copepods.


Fig. 2. Mean values of d15N and d13C of (A) potential primary food sources, and (B) fish and decapods and their potential prey in the unvegetated,

nearshore waters of south-western Australia. Boxes in dashed lines encapsulate the range of values for different groups of primary producers.

Standard error values are located in Table 1.

In contrast, seagrasses and seston, and to a lesser extentbenthic micro-algae, rated high for individuals withhigher d13C values (�11.8 and �11.7&). Since Posidoniaaustralis and P. sinuosa formed the extremes of the d13Crange of seagrasses (Table 1), the other two seagrassspecies (P. coriacea and Amphibolis griffithii) would haveproduced similar results.

3.2. Diets of fish species

All of the fish species collected from the nearshorewaters ingested predominantly invertebrates, comprisingmainly small crustacea or polychaetes and/or fish,

whereas no species consumed plant material (Fig. 4).The diets of species such as Cnidoglanis macrocephalusand Sillago vittata were dominated by harpacticoidcopepods (O77% of the volume), whereas S. bassensisconsumed mainly calanoid copepods (70%). In contrast,species such as S. punctata, S. schomburgkii andAmmotretis elongatus consumed large volumes of poly-chaetes (O60%) (Fig. 4). Aldrichetta forsteri andAtherinamorus ogilbyi consumed considerable volumesof foraminifera (64 and 46%, respectively). Ammotretisrostratus and Rhabdosargus sarba consumed largevolumes of teleosts (38 and 47%, respectively), with theformer of these two species also consuming carid shrimpand squid and the latter also ingesting amphipods.


P. australis

P. sin

uosa

Sest

on

Bent

hic

mic

ro-a

lgae

Cau

lerp

a

Ulv

a

Hypnea

Rho

doph

yta

Ecklo

nia

Sargassum

Polychaetes (n=11)

0

0.2

0.4

0.6

0.8

1.0 Calanoid copepods (n=2)

P. australis

P. sin

uosa

Sest

on

Bent

hic

mic

ro-a

lgae

Cau

lerp

a

Ulv

a

Hypnea

Rho

doph

yta

Ecklo

nia

Sargassum

Harpacticoid copepods (n=4)

0

0.2

0.4

0.6

0.8

1.0Amphipods (n=3)

Fig. 3. Box-whisker plots representing the distribution of the feasible contributions of seven representative primary producers to amphipods,

harpacticoid and calanoid copepods and polychaetes based on d13C values. Plots show minimum, 1st, 50th and 99th percentiles and maximum values

of the distributions.

4. Discussion

The high d15N values of fish, relative to those ofprimary producers (O5&), combined with the pre-dominance of invertebrate prey in the diets of speciescaught in the study region indicates that both seagrassand algae were not consumed directly by these speciesduring the period of this study. This conclusion issupported by several other studies in the region thatexamined diets over much longer timescales and alsoshowed that fish in the nearshore waters consumemainly small crustacean and polychaete prey (Table 2).Since this diet is typical of nearshore fish communitiesthroughout south-western Australia (Ayvazian andHyndes, 1995), energy flow to fish relies on theconsumption of invertebrates that graze either directlyon fresh plant material or indirectly through detritus.

The d13C values for fish were similar to those ofa combination of harpacticoid and calanoid copepods,amphipods and polychaetes. Since d13C is expected to beenriched by only 0e1& for each trophic step (Petersonand Fry, 1987), the d13C values of consumers is likely toreflect the proportion of each prey type that isconsumed. For example, the lower d13C values forAldrichetta forsteri, Cnidoglanis macrocephalus andAtherinomorus ogilbyi were similar to those of amphi-pods and calanoid copepods. While the small samplesizes in this study did not show that these speciesconsumed large quantities of amphipods and calanoidcopepods over the timescale of our study, other studieshave shown their diets to be dominated particularlyby amphipods in nearshore areas where wrack hasaccumulated (Lenanton et al., 1982; Robertson andLenanton, 1984). Thus, the relatively low d13C values of


these fish species are likely to reflect the greaterconsumption of these prey. The higher than expectedenrichment of 15N (O5&) in these fish species comparedto their prey (Minagawa and Wada, 1984), may indicatethat they assimilate a relatively high proportion of theirnitrogen from polychaetes, another important preyspecies (Robertson and Lenanton, 1984), that hadgreater d15N values.

The higher d13C values for the remaining fish speciesare consistent with them consuming greater quantities ofpolychaetes and/or harpacticoid copepods, which ex-hibited higher d13C values than amphipods and calanoidcopepods. Since species, such as Sillago bassensis, S.vittata, S. punctata and Pseudorhombus jenynsii consumelarge volumes of polychaetes (Table 2), these higherd13C values are likely to reflect the greater consumptionof this prey type. Smaller juveniles of S. vittata and S.punctata can also consume relatively high proportions ofharpacticoid copepods (Schafer et al., 2002; Whitehead

Fig. 4. Percentage volume contribution of prey types to the diets of

a range of fish species collected from the sampling sites in south-

western Australia. Sample sizes shown above each column.

and Hyndes, unpublished data), which would, similarly,account for their elevated d13C values.

On the basis of the mixing model using d13C data,detached seagrass is unlikely to be assimilated byamphipods and calanoid copepods. For seagrass tomake a considerable contribution, these prey groupswould also need to consume similar proportions of algaethat are more depleted in 13C than the most depleted redalga found in the present study (e.g. Hypnea spp.; Table2, Fig. 3). The results therefore indicate that amphipodsand calanoid copepods are most likely to assimilatecarbon from either a mixture of all types of algae, orentirely from brown algae. The greater consumption ofbrown over red algae by the amphipod Allorchestescompressa (Robertson and Lucas, 1983) supports thelatter scenario. In comparison, the greater consumptionof seagrass over red algae by this amphipod species(Robertson and Lucas, 1983) suggests that, whileseagrass may be ingested, it is not assimilated. Ingestionof seagrass may allow these amphipods to digest theperiphyton or bacteria associated with the seagrassleaves, though typical isotopic signatures of thesecomponents are not available. Thus, our results suggestthat, like the amphipod Talitrus saltator in wrack alongthe shoreline of France (Adin and Riera, 2003),amphipods in nearshore waters of south-western Aus-tralia are likely to assimilate carbon mainly from brownalgae.

Errant polychaetes, whose d13C values were slightlyelevated to those of calanoid copepods and amphipods,also do not appear to obtain their carbon from seagrass.The higher d15N values for polychaetes relative to most

Table 2

Composition of the diets, in order of dominance (by volume), for

species of fish found in nearshore coastal waters of south-western

Australia. Data represent a collation of results from Lenanton et al.

(1982), Prince et al. (1982), Robertson and Lenanton (1984), Gill and

Potter (1993), Hyndes et al. (1997), de Lestang et al. (2000) and Schafer

et al. (2002)

Fish species Dietary composition

Cnidoglanis macrocephalus Amphipods, bivalves and polychaetes

Mugil cephalus Planktonic copepods, detritus and

cladocerans

Favonigobius lateralis Errant polychaetes, tanaids and

amphipods

Sillago schomburgkii Polychaetes and amphipods

Sillago burrus Errant polychaetes, copepods and

amphipods

Sillago vittata Copepods, amphipods, polychaetes

Sillago bassensis Amphipods, copepods, polychaetes

Sillaginodes punctata Errant polychaetes, amphipods and

copepods

Atherinamorus ogilbyi Benthic crustaceans, polychaetes

Pseudorhombus jenynsii Teleosts, decapods, mysids and errant

polychaetes

Aldrichetta forsteri Amphipods, green algae and copepods

Portunus pelagicus Bivalves, decapods, amphipods and

polychaetes


of the primary producers and the other prey species areconsistent with the fact that these invertebrates oftenpredate on smaller invertebrates or scavenge on deadanimals (Glasby et al., 2000), rather than directlyconsuming plant material.

In contrast to amphipods and calanoid copepods,harpacticoid copepods showed a significant spatialvariation in d13C values that resulted in a greater degreeof variability in the contributions of seagrasses to theseorganisms. While, overall, the mixing model indicatedthat the contribution of seagrasses to harpacticoidcopepods was likely to be low, this contribution waslikely to be high at one site. This site is relativelysheltered compared to the other sites, is in closerproximity to seagrass meadows and is known to havea relatively high organic content in the sediments(Whitehead and Hyndes, unpublished data). It ispossible, therefore, that the contribution of seagrassesto consumers at a site may reflect the proximity toseagrass and environmental factors that allow seagrassdetritus to accumulate at the site. Copepods feed on fineparticulate detritus or benthic microalgae (Coull, 1999),though our results for one site are consistent with someselection of seagrass detritus over other macrophytes.Furthermore, the similar d15N value of harpacticoidcopepods to benthic microalgae suggests that thedetritus of more depleted macrophytes (e.g. seagrass)make a considerable contribution to the N assimilatedby these invertebrates. Interestingly, polychaetes alsoexhibited a high degree of variability in their d13Cvalues, with seagrass shown to contribute to higherextreme of the d13C range. The current study, therefore,suggests that Amphibolis and Posidonia species can enterthe food web of unvegetated coastal areas largely asdetritus consumed by harpacticoid copepods and alsopolychaetes. However, spatially, this is likely to behighly variable. Similarly, Posidonia oceanica, appearsto enter the food web as detritus (Vizzini et al., 2002),while detrital Halodule uninervis and Halophila ovalis isconsidered to contribute considerably to prawn pro-duction in a north-eastern Australian estuary (Lone-ragan et al., 1997). The transportation of seagrassdetritus from distant coastal regions is likely tocontribute to the pelagic and benthic food webs in theoffshore region of south-eastern Australia (Thresheret al., 1992; Davonport and Bax, 2002).

The present study was carried out towards the endof the period (late spring to early autumn) when thejuveniles of numerous species recruit and remain in thenearshore waters for protracted periods (Hyndes et al.,1996; Hyndes, unpublished data). Harpacticoid cope-pods form a considerable part of the diet of smalljuveniles of species in this environment (Jenkins et al.,1995; Schafer et al., 2002). The assimilation of seagrassby harpacticoid copepods at some locations, and bysome polychaetes, therefore suggests that detrital

seagrasses can make a substantial indirect contributionto the production a range of fish species, albeit spatiallydependent. Since many of these fish species display anontogenetic shift away from consuming small prey, suchas copepods, to consuming larger prey, such asamphipods and then polychaetes, any contribution ofseagrass to fish production in unvegetated nearshoreareas is likely to alter as fish grow.

Since larger juveniles of the above species, as well asspecies such as Sillago schomburgkii and S. bassensisconsume prey other than harpacticoid copepods (seeTable 2), they are likely to assimilate C and N fromother sources such as brown and red algae. Similar toa range of seagrass species (Zieman et al., 1984), thed15N and d13C values of Amphibolis and Posidoniaspecies do not change during breakdown into finerparticulate material (Smit, unpublished data). Thisprocess is therefore unlikely to explain the lack ofcontribution of seagrasses to the food chain of the abovefish species in south-western Australia. It thereforeappears that macroalgae and possibly benthic micro-algae, contribute largely to invertebrate and fish pro-duction in those areas, a conclusion that concurs withstudies in seagrass systems, where epiphytic algae andbenthic microalgae contribute to the production ofconsumers (Fry et al., 1983; Fry, 1984; Kitting et al.,1984; Mallin et al., 1992; Newell et al., 1995).

With the exception of harpacticoid copepods at somelocations, and a small proportion of polychaetes, thelimited assimilation of C and N from seagrasses byinvertebrates in the present study may reflect thepreference of herbivores for algal material (Klumppet al., 1992), presumed to be related to the relativelypoor nutritional value and high lignocellulose content ofseagrasses. Re-entry into the foodweb of seagrassdetritus may therefore rely, more generally, on thebacterial decomposition process, which would bedifficult to detect using stable isotope analysis. Thephysical breakdown of seagrass material into detritusdoes not affect its isotopic signature (Zieman et al.,1984; Smit, unpublished data), but the bacterial de-composition of detached seagrass would result in theloss of any typical isotopic signature, making it difficultto trace using isotope analysis. Seagrass leaves de-compose relatively rapidly with the abundance ofmicrobes increasing over time (Peduzzi and Herndl,1991; Newell et al., 1995; Holmer and Olsen, 2002;Anesio et al., 2003). Attached bacteria enhance thedissolution of particulate seagrass, from which theproducts are either utilised by free bacteria in the watercolumn (Anesio et al., 2003), or become available foruptake by primary producers in the vicinity or furtheroffshore (Holmer and Olsen, 2002). The analyses used inthis study did not allow this pathway to be followed, andso we cannot discount that it is a mechanism for the re-entry of seagrass material into the foodweb.


In conclusion, our results suggest that seagrasses insouth-western Australia can enter the food web asdetritus, but this is likely to be limited. Any flow ofdetrital Amphibolis and Posidonia material into thefoodweb is being mediated by specific detrivores, such asharpactacoid copepods, rather than by all detritivores.Even in the case of harpactacoid copepods, thismediation appears to be spatially dependent. Inaddition, since harpactacoid copepods are consumedmainly by the small juveniles of a number of fish species,the entry of seagrass into the food web via these prey islikely to be restricted to the periods when fish firstrecruit into nearshore waters. However, since this studywas restricted to the late summer/early autumn, thoseother detritivores may rely on seagrass during othertimes of the year. Results from the current study suggestthat detrital brown algae, and possibly benthic micro-algae, provide substantial contributions to the food webin nearshore waters of south-western Australia.

Acknowledgements

We would like to thank A.J. Smit for his help in thefield and processing of the stable isotope samples, as wellhelpful discussions. We also appreciate the help of AlanKendrick for the processing of dietary samples and MatVanderklift for field support and constructive commentson the manuscript. Thank you also to Jason How forhelping with the Isosource analyses. This project wasfunded by the Australian Research Council small grantscheme.

References

Anesio, A.M., Abreu, P.C., Biddanda, B.A., 2003. The role of free and

attached microorganisms in the decomposition of estuarine

macrophyte detritus. Estuarine, Coastal and Shelf Sciences 56,

197e201.

Adin, R., Riera, P., 2003. Preferential food source utilization among

stranded macroalgae by Talitrus saltator (Amphipod, Talitridae):

a stable isotopes study in the northern coast of Brittany (France).

Estuarine, Coastal and Shelf Sciences 56, 91e98.

Ayvazian, S.G., Hyndes, G.A., 1995. Surf-zone fish assemblages in

south-western Australia: do adjacent nearshore habitat and the

warm Leeuwin Current influence the characteristics of the fish

fauna? Marine Biology 122, 527e536.

Benner, R., Maccubin, A.E., Hodson, R.E., 1984. Preparation,

characterization and microbial degradation of specifically radio-

labelled (14C) lignocelluloses from marine and freshwater macro-

phytes. Applied Environmental Microbiology 47, 381e389.

Cebrian, J., Duarte, C.M., Marba, N., Enrıquez, S., 1997. Magnitude

and fate of the production of four co-occurring Western

Mediterranean seagrass species. Marine Ecology Progress Series

155, 29e44.Clark, B.M., 1997. Variation in surf-zone fish communities across

a wave-exposure gradient. Estuarine, Coastal and Shelf Sciences

44, 659e674.

Connolly, R.M., 1994. A comparison of fish assemblages from

seagrass and unvegetated areas of a southern Australian estuary.

Australian Journal of Marine and Freshwater Research 45, 1033e1044.

Coull, B.C., 1999. Role of meifauna in estuarine soft-bottom habitats.

Australian Journal of Ecology 24, 327e343.Davonport, S.R., Bax, N.J., 2002. A trophic study of a marine

ecosystem off southeastern Australia using stable isotopes of

carbon and nitrogen. Canadian Journal of Fisheries and Aquatic

Sciences 59, 514e530.Ferrell, D.J., Bell, J.D., 1991. Differences among assemblages of fish

associated with Zostera capricorni and bare sand over a large

spatial scale. Marine Ecology Progress Series 72, 15e24.

Fry, B., Scalan, R.S., Parker, P.L., 1983. 13C/12C ratios in marine food

webs of the Torres Strait. Queensland. Australian Journal of

Marine and Freshwater Research 34, 707e715.

Fry, B., 1984. 13C/12C ratios and the trophic importance of algae in

Florida Syringodium filiforme seagrass meadows. Marine Biology

79, 11e19.

Gill, H.S., Potter, I.C., 1993. Spatial segregation amongst goby species

within an Australian estuary, with a comparison of the diets and

salinity tolerance of the two most abundant species. Marine

Biology 117, 515e526.

Glasby, C.J., Hutchings, P.A., Fauchald, K., Paxton, H.,

Rouse, G.W., Watson Russell, C., Wilson, R.S., 2000. Class

Polychaeta. In: Beesley, P.L., Ross, G.J.B., Glasby, C.J. (Eds.),

Polychates and Allies: The Southern Synthesis. Fauna of Australia:

Polychaeta, Myzostomida, Pogonophora, Echura, Sipuncula, vol.

4A, Australian Biological Resources Study, Canberra, pp. 1e296.Holmer,M., Olsen, A.B., 2002. Role of decomposition ofmangrove and

seagrassdetritus in sediment carbonandnitrogen cycling in a tropical

mangrove forest. Marine Ecology Progress Series 230, 87e101.Hyndes, G.A., Potter, I.C., Lenanton, R.C.J., 1996. Habitat partition-

ing by whiting species (Sillaginidae) in coastal waters. Environ-

mental Biology of Fishes 46, 21e40.

Hyndes, G.A., Platell, M.E., Potter, I.C., 1997. The relationship

between diets and body size, mouth morphology, habitat and

movements of six sillaginid species in coastal waters: implications

for resource partitioning. Marine Biology 128, 585e598.

Hyslop, E.J., 1980. Stomach contents analysis e a review of methods

and their application. Journal of Fish Biology 17, 411e429.

Jenkins, G.P., Wheatley, M.J., Poore, A.G.B., 1995. Spatial variation

in recruitment, growth, and feeding of postsettlement King George

whiting, Sillaginodes punctata, associated with seagrass beds of

Port Phillip Bay, Australia. Canadian Journal of Fisheries and

Aquatic Sciences 53, 350e359.

Kirkman, H., Kendrick, G., 1997. Ecological significance and

commercial harvesting of drifting and beach-cast macro-algae

and seagrasses in Australia: a review. Journal of Applied Ecology

9, 311e326.

Kitting, C.L., Fry, B., Morgan, M.D., 1984. Detection of inconspic-

uous epiphytic algae supporting food webs in seagrass meadows.

Oecologia 62, 145e149.

Klumpp, D.W., Salita-Espinosa, J.S., Fortes, M.D., 1992. The role of

epiphytic periphyton and macroinvertebrate grazers in the trophic

flux of a tropical seagrass community. Aquatic Botany 43, 327e349.

de Lestang, S., Platell, M.E., Potter, I.C., 2000. Dietary composition of

the blue swimmer crab Potunus pelagicus L. Does it vary with body

size and shell state and between estuaries? Journal of Experimental

Marine Biology and Ecology 246, 241e257.

Lavery, P.S., Vanderklift, M.A., 2002. A comparison of spatial and

temporal patterns in epiphytic algal assemblages of the seagrasses

Amphibolis griffithii and Posidonia coriacea. Marine Ecology

Progress Series 236, 99e112.

Lepoint, G., Nyssen, F., Gobert, S., Dauby, P., Bouquegneau, J.M.,

2000. Relative impact of a seagrass bed and its adjacent epilithic

algal community in consumer diets. Marine Biology 136, 513e518.

Lenanton, R.C.J., 1982. Alternative non-estuarine nursery habitats

for some commercially and recreationally important fish of


south-western Australia. Australian Journal of Marine and

Freshwater Research 33, 881e900.

Lenanton, R.C.J., Robertson, A.I., Hansen, J.A., 1982. Nearshore

accumulations of detached macrophytes as nursery areas for fish.

Marine Ecology Progress Series 9, 51e57.Loneragan, N.R., Bunn, S.E., Kellaway, D.M., 1997. Are mangroves

and seagrass sources of organic carbon for penaeid prawns in

a tropical Australian estuary? A multiple stable isotope study.

Marine Biology 130, 289e300.

Mallin, M.A., Burkholder, J.M., Sullivan, M.J., 1992. Contributions

of benthic microalgae to coastal fisheries yield. Transactions of the

American Fisheries Society 121, 691e695.Marba, N., Walker, D.I., 1999. Growth, flowering, and population

dynamics of temperate Western Australian seagrasses. Marine

Ecology Progress Series 184, 105e118.

Marguillier, S., van der Velde, G., Dehairs, F., Hemminga, M.A.,

Rajagopal, S., 1997. Trophic relationships in an interlinked

mangrove-seagrass ecosystem as traced by d13C and d15N. Marine

Ecology Progress Series 151, 115e121.Minagawa, M., Wada, E., 1984. Stepwise enrichment of 15N along

food chains: further evidence and the relationship between d15N

and animal age. Geochimica et Cosmochimica Acta 48, 1135e

1140.

Newell, R.I.E., Marshall, N., Sasekumar, A., Chong, V.C., 1995.

Relative importance of benthic microalgae, phytoplankton, and

mangroves as sources of nutrition for penaeid prawns and other

coastal invertebrates from Malaysia. Marine Biology 123, 595e606.

Orth, R.J., Heck, K.L., 1980. Structural components of the eelgrass

(Zostera marina) meadows in the lower Chesapeake Bay e fishes.

Estuaries 3, 278e288.

Peduzzi, P., Herndl, G.J., 1991. Decomposition and significance of

seagrass litter (Cymodocea nodosa) for the microbial food web in

coastal waters (Gulf of Trieste, Northern Adriatic Sea). Marine

Ecology Progress Series 71, 163e174.

Peterson, B.J., Fry, B., 1987. Stable isotopes in ecosystem studies.

Annual Review of Ecology and Systematics 18, 293e320.

Phillips, J., Kendrick, G., Lavery, P., 1997. A test of the functional

form group hypothesis for detecting disturbance in macroalgal reef

communities. Marine Ecology Progress Series 153, 125e138.

Phillips, D.L., Greg, J.W., 2003. Source partitioning using stable

isotopes: coping with too many sources. Oecologia 136, 261e269.Prince, J.P., Potter, I.C., Lenanton, R.C.J., Loneragan, N.R., 1982.

Segregation and feeding of atherinid species (Teleostei) in

southwestern Australian estuaries. Australian Journal of Marine

and Freshwater Research 33, 865e880.

Robertson, A.I., Lenanton, R.C.J., 1984. Fish community structure

and food chain dynamics in the surf-zone of sandy beaches: the role

of detached macrophyte detritus. Journal of Experimental Marine

Biology and Ecology 84, 265e283.

Robertson, A.I., Lucas, J.S., 1983. Food choice, feeding rates and the

turnover of macrophyte biomass by the surf-zone inhabitating

amphipod. Journal of Experimental Marine Biology and Ecology

72, 99e124.

Rolff, C., 2000. Seasonal variation in d13C and d15N of size-

fractionated plankton at a coastal station in the northern Baltic

proper. Marine Ecology Progress Series 203, 47e65.

Ruiz, G.M., Hines, A.H., Posey, M.H., 1993. Shallow water as

a refuge habitat for fish and crustaceans in non-vegetated estuaries:

an example from Chesapeake Bay. Marine Ecology Progress Series

99, 1e16.

Schafer, L.N., Platell, M.E., Valesini, F.J., Potter, I.C., 2002.

Comparisons between the influence of habitat type, season and

body size on the dietary compositions of fish species in nearshore

marine waters. Journal of Experimental Marine Biology and

Ecology 278, 67e92.

Sogard, S.M., Able, K.W., 1991. A comparison of eelgrass, sea lettuce

macroalgae, and marsh creeks as habitats for epibenthic fishes and

decapods. Estuarine, Coastal and Shelf Science 33, 501e519.

Staddon, P.L., 2004. Carbon isotopes in functional soil ecology.

Trends in Ecology and Evolution 19, 148e154.Thayer, G.W., Adams, S.M., La Croix, M.W., 1975. Structural and

functional aspects of a recently established Zostera marina

community. In: Cronin, L.E. (Ed.), Estuarine Research, vol. 1.

Academic Press, New York, pp. 518e540.Thresher, R.E., Nichols, P.D., Gunn, J.S., Bruce, B.D., Furlani, D.M.,

1992. Seagrass detritus as the basis of a coastal planktonic food

chain. Limnology and Oceanography 37, 1754e1758.Vizzini, S., Sara, G., Michener, R.H., Mazzola, A., 2002. The role and

contribution of the seagrass Posidonia oceanica (L.) Delile organic

matter for secondary consumers as revealed by carbon and

nitrogen stable isotope analysis. Acta Oecologia 277, 285.

Valentine, J.F., Heck Jr., K.L., Busby, J., Webb, D., 1997.

Experimental evidence that herbivory increases shoot density and

productivity in a subtropical turtlegrass (Thalassia testudinum)

meadow. Oecologia 112, 193e200.Valentine, J.F., Heck Jr., K.L., Kirsch, K.K., Webb, D., 2000.

Seagrass herbivory in the turtlegrass habitats of the Florida Keys.

Marine Ecology Progress Series. 200, 213e228.

Vanderklift, M.A., Ponsard, S., 2003. Sources of variation in

consumer-diet d15N enrichment: a meta-analysis. Oecologia 136,

169e182.

Zieman, J.C., Macko, S.A., Mills, A.L., 1984. Role of seagrass and

mangroves in estuarine food webs: temporal and spatial changes in

stable isotope composition and amino acid content during

decomposition. Bulletin of Marine Science 35, 380e392.

Does transported seagrass provide an important trophic link in unvegetated, nearshore areas?

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