Mangrove forests are often a prominent feature ofthe coastline in the tropics and subtropics, and areincreasingly being exploited by humans. A thoroughunderstanding of the ecological functioning and oftheir interactions with adjacent ecosystems is impor-tant in providing a scientific basis for the managementand/or restoration of mangroves. Many aspects of car-
bon dynamics in mangrove and adjacent ecosystemsare still far from understood (e.g. Bouillon et al. 2004),and in view of the various settings in which mangroveforests may occur, it is imperative to obtain data from arange of contrasting mangrove ecosystems rather thangeneralizing conclusions from any particular site (e.g.Ewel et al. 1998).
Invertebrate communities in intertidal mangroveforests have access to a variety of carbon and nitrogen
Resource utilization patterns of epifauna frommangrove forests with contrasting inputs of
local versus imported organic matter
Steven Bouillon1,*, Tom Moens2, Inge Overmeer1, Nico Koedam3, Frank Dehairs1
1Department of Analytical and Environmental Chemistry, Mangrove Management Group, Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium
2Biology Department, Marine Biology Section, Ghent University, Krijgslaan 281/S8, 9000 Gent, Belgium3Department of General Botany and Nature Management, Mangrove Management Group, Vrije Universiteit Brussel,
Pleinlaan 2, 1050 Brussels, Belgium
ABSTRACT: Mangrove epifaunal communities have access to various carbon and nitrogen sourcesand we hypothesized that the degree of material exchange with the aquatic environment might influ-ence the overall use of different substrates by intertidal communities. Therefore, we analyzed C andN stable isotope ratios in primary producers, sediments and 245 samples of epifauna hand-collectedfrom 5 sites in India, Sri Lanka and Kenya (representing estuarine, lagoonal and basin-type man-grove forests). Several patterns emerged from this data set. First, epifaunal communities used a rangeof available food substrates at all sites studied, including mangrove-derived organic matter, localmicrophytobenthos and micro-epiflora, as well as imported C and N from the aquatic environment(i.e. phytoplankton- and/or seagrass-derived organic matter). Secondly, our data indicate that at siteswith significant inputs of aquatic sources, use of mangrove carbon is rather limited on a communitybasis, whereas in systems with less material exchange with adjacent waters, the relative importanceof mangroves is higher. Thus, despite the unquestionable impact some epifaunal species may haveon leaf litter dynamics, the dependency of the invertebrate community as a whole on mangrove litteris not ubiquitously large and varies according to the availability of local versus tidally importedsources. Precise quantification of the relative importance of different substrates with δ13C and δ15N is,however, not always straightforward due to the multitude of available sources and the overlap insource stable isotope signatures. Micro-epiflora on mangroves trees were remarkably depleted in 15Nin all systems (δ15N between –8.2 and –2.4‰) and thus form an example where δ15N is a useful sourceindicator, as low δ15N values of several gastropod species indicated substantial feeding on suchepiflora.
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sources: local inputs from mangroves as litterfall or aspart of the sediment organic matter pool, microphyto-benthos, a variety of epiflora and tidally importedsources such as phytoplankton- or seagrass-derivedorganic matter. The removal of large amounts of leaflitter by crabs observed in some systems (see Lee 1998)and the fact that some other well-studied mangroveinvertebrates (e.g. the gastropod Terebralia palustris)have been observed to feed extensively on mangroveleaves (e.g. Fratini et al. 2000) has nourished the stillprevalent view that ‘the great majority of the man-grove macrobenthos relies directly on the high produc-tion of the mangroves themselves, consuming eitherleaf litter or detritus composed of decaying leaves’ (e.g.Fratini et al. 2000, Ashton 2002). The observation thata significant proportion of leaf production is efficientlyremoved and/or consumed by some epifaunal species(e.g. Ólafsson et al. 2002) in some mangrove systems, isnot necessarily contradictory to the idea that mangroveepifaunal communities as a whole may not depend pri-marily on mangrove production as a direct food source.Recent results from stable isotope studies (e.g. Chris-tensen et al. 2001, Bouillon et al. 2002, Hsieh et al.2002) indeed suggest that only a limited number ofspecies may rely substantially on mangrove carbonand that a range of other carbon sources are used bythe invertebrate community. Nevertheless, the degreeto which such results can be generalized is not known.In particular, mangroves occur in highly variable geo-morphological settings, which greatly influence theavailability of potential C and N sources: where tidalexchange is significant, marine/estuarine sources suchas phytoplankton- or seagrass-derived organic mattercan be imported, but in low tidal amplitude settings,mangroves are the dominant source of carbon avail-able in the sedimentary pool (Bouillon et al. 2003).
The use of stable isotopes as tracers of the origin andassimilation of organic matter by faunal communitieshas become widespread, and is based on the assump-tions that (1) different sources (may) have differentδ13C and δ15N signatures, and (2) assimilation by con-
sumers results in little fractionation in the case of 13C(i.e. consumer δ13C values are close to those of theirdiet, with a slight enrichment typically between 0 and2‰), and somewhat higher for 15N (a value of ~3‰ isoften cited, but the actual degree of fractionationvaries as a function of taxonomy, food quality and envi-ronmental factors, see e.g. Vanderklift & Ponsard 2003for a recent review).
We hypothesized that the dependency of the epi-faunal community on mangrove-derived organic mat-ter would vary across different environmental settingsand that such differences would be related to the rela-tive availability of different potential sources. There-fore, we compared data on resource utilization pat-terns (as evident from δ13C and δ15N analyses) of avariety of epifaunal species from a number of contrast-ing mangrove sites (Table 1): (1) a seaward exposedsite and a more inland protected site with adjacent sea-grass beds in Gazi Bay (Kenya), (2) 1 site in theCoringa Wildlife Sanctuary (CWS), a large estuarinemangrove system without nearby seagrass beds in theGodavari delta (Andhra Pradesh, India), and (3) 2 smallmangrove sites along the coast of Sri Lanka: the basinforest of Galle and the lagoonal forest in Pambala.Whereas the sites in India and Kenya experiencemedium or high tidal amplitudes (spring tidal range of~2 and 3.2 m, respectively), the sites in Sri Lanka areboth characterized by a low tidal amplitude (typically≤0.20 m). We supplemented these data sets with acompilation of relevant literature data in an attempt tolook for general patterns in the origin of the carbonassimilated by different epifaunal groups acrossdifferent mangrove ecosystems.
MATERIALS AND METHODS
Description of study areas. Gazi Bay, Kenya: GaziBay (39° 30’ E, 4° 22’ S) is a shallow, tropical coastalwater system, located ~50 km south of Mombasa(Fig. 1a,b). The total area of the bay is approximately
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Site Forest type Dominant vegetation Tidal Adjacent seagrass or setting range (m) beds?
Gazi Bay (Kenya)Upstream site Estuarine Mixed: Rhizophora mucronata, ~3.2 Yes
Avicennia marina, Ceriops tagalSeaward site Estuarine Dominated by Sonneratia alba ~3.2 Yes
Galle (Sri Lanka) Basin Dominated by Rhizophora apiculata ≤0.20 No
Pambala (Sri Lanka) Lagoonal (fringe) Dominated by R. apiculata ≤0.20 Yes
Table 1. Overview of the main characteristics of the study sites. CWS: Coringa Wildlife Sanctuary, Andhra Pradesh
Bouillon et al.: Resource utilization patterns of mangrove epifauna
10 km2, with an additional 6 to 7 km2 covered bymangroves, mostly Rhizophora mucronata, Sonneratiaalba, Ceriops tagal, Bruguiera gymnorrhiza, Avicenniamarina and Xylocarpus granatum. The bay itself har-bors large areas (~70% of the total area) of often denseseagrass beds, which are dominated by Thalassoden-dron ciliatum (Coppejans et al. 1992). The bay is opento the Indian Ocean through a relatively wide andshallow entrance in the south. Besides a few tidalcreeks without freshwater inputs, the upper region ofthe bay receives freshwater from the Kidogoweni river,which cuts through the mangroves. Spring tidal rangein Gazi Bay is reported to be 3.2 m (Kitheka 1997). Twointertidal sites were selected for the sampling of flora,sediments and invertebrates in July 2003: (Site 1) amixed forest site located upstream along Kidogowenicreek, where vegetation consisted of R. mucronata, A.marina, C. tagal and a few X. granatum, and (Site 2) aseaward site predominantly vegetated by S. alba withsome R. mucronata and A. marina, which bordered theedge of the bay and is, therefore, more likely to beinfluenced by seagrass inputs (Fig. 1).
Coringa Wildlife Sanctuary, Andhra Pradesh, India:The Coringa Wildlife Sanctuary (CWS, between 82° 15’and 82° 22’ E, 16° 43’ and 17° 00’ N, Fig. 1a,c) is part ofthe mangrove-covered area between Kakinada bayand the Gautami branch of the Godavari river(Fig. 1a,c). The CWS is dominated by mangrove forests(covering ~150 km2) and tidal mudflats, the most abun-dant mangrove species being Avicennia marina, Avi-cennia officinalis, Excoecaria agallocha, Sonneratiaapetala, Rhizophora mucronata and Rhizophora apicu-lata (Satyanarayana et al. 2002). Seagrass beds areabsent from the areas adjacent to the mangroves.Tides are semidiurnal and spring tidal amplitude in thebay is ~2 m. Samples of vegetation, sediments and epi-fauna were collected in May and June 2001 in thenorthwestern part of the CWS, in an intertidal areadominated by A. officinalis, A. marina and E. agallochaalong Matlapalem creek (Fig. 1a,c).
Galle, Sri Lanka: The mangroves in Galle, southwestSri Lanka (06° 01’ N to 80° 14’ E) cover an area of about1.5 km2 and can be classified as a basin forest (sensuLugo & Snedaker 1974) (Fig. 1e). The forest is located
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Fig. 1. Geographical location of the different sampling sites. (a) Overview, and location of (b) the 2 sampling sites in Gazi Bay,Kenya, (c) the sampling areas in the Coringa Wildlife Sanctuary, India, and (d,e) the sampling sites in Galle and Pambala, SriLanka, respectively. Note that the black square in (c) indicates the areas where similar data were collected and presented inBouillon et al. (2002). The darkest areas represent the main mangrove-covered regions and the dotted area in (b) shows the
location of the main seagrass beds. See Table 1 for an overview of the main site characteristics
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approximately 600 m from the IndianOcean shoreline and is traversed by 2rivers, the Thalpe Ela and its tributary,the Galu Ganga. The forest at Galle isfurther characterized by a very irregulartopography due to the burrowing activityof the mud lobster Thalassina anomala,and large patches of the forest are per-manently inundated. This site experi-ences very low to no tidal influence andhence, limited exchange of organic mate-rial with adjacent environments, exceptduring exceptionally high water levels inthe river. The majority of samples forGalle were collected in an area predomi-nantly vegetated by Rhizophora apicu-lata in March 2002 (dry season). Someinitial samples were collected earlier inFebruary–March 2000; and some stableisotope data on vegetation and sedimentswere available from a previous study(Bouillon et al. 2003).
Pambala, Sri Lanka: Pambala-Chilawlagoon is situated in western Sri Lanka(07° 35’ N, 79° 47’ E) and is similarly char-acterized as a low tidal amplitude system(tidal range not exceeding 0.2 m, F. Dah-douh-Guebas pers. obs.), with ~3.5 km2
of fringing mangroves (Fig. 1d). Surfacewater salinity in the lagoon variesstrongly, between 0 and 55. All samplesfrom Pambala were collected in a Rhi-zophora mucronata-dominated area inMarch 2002, but some previous data onvegetation and sediments were available(Bouillon et al. 2003).
In conclusion, the different samplingsites represent a variety of geomorpho-logical settings (summarized in Table 1):(1) Pambala (Sri Lanka) as an example ofa low tidal amplitude lagoon with fring-ing mangroves, (2) Galle (Sri Lanka)being a basin forest with insignificanttidal influence, (3) the CWS (India) as anexample of a large estuarine mangroveforest with significant tidal influence butwithout seagrass inputs, and (4) 2 sites inthe smaller estuarine system of Gazi Bay(Kenya), 1 of which is located in the inte-rior part of the forest, the other site nearthe forest fringe and, therefore, moreexposed to inputs from the extensive sea-grass beds in the bay. The strongest tidalinfluence is experienced at Gazi Bay,Kenya.
Table 2. Overview of stable isotope data (average ± 1 SD) for flora, sediments and epifauna from Gazi Bay, Kenya (Sites 1 and 2, see Fig. 1b)
Bouillon et al.: Resource utilization patterns of mangrove epifauna
Sampling and analytical techniques. At all sites,samples of epifauna and flora were taken from a 20 mby 20 m area in order to avoid spatial variations in pro-ducer stable isotope signatures (e.g. Fry et al. 2000).Although our sampling design does not, therefore,consider potential spatial and seasonal variations inthe foodweb structure within sites, this should not limitour conclusions (see ‘Discussion’). Sampling effortswere concentrated on those intertidal species (mainlymollusks and brachyuran crabs) that were numericallyabundant in the area and, therefore, likely to play animportant role in the overall processing of organic mat-ter. Samples of vegetation and epifauna were collectedby hand, while benthic microalgae were obtained bygently scraping them off the sediment where theyformed a conspicuous layer; this was only the case inGazi Bay, although previous data were available fromthe CWS. Mangrove leaf samples were picked fromdifferent trees to avoid any bias in the resulting isotopesignatures. Typically, only surface sediments were col-lected, but for the 2 sites in Gazi, sediment cores weretaken in the framework of another study and parti-tioned into 0–1, 1–2, 2–4 and 4–10 cm layers. All fau-nal samples were kept in a cool box, transported to thefield laboratory, washed and dried at 60°C for at least48 h. For some of the smaller crab species (e.g. Ucaspp., smaller sesarmids) the gut and intestinal systemwere first removed and muscle tissue of the body wasused; for larger crab species, muscle tissue was takenfrom the chelae. For mollusks, tissues were removedfrom their shell and analyzed whole. All samples wereground to a fine powder and sub-samples for δ13C sub-sequently acidified with dilute (5%) HCl before ana-lysis to remove carbonates (except those of mangrovetissues). Sediment total organic carbon (TOC) and totalnitrogen (TN) were determined bycombusting pre-weighed samples in aThermoFinnigan Flash1112 elementalanalyzer. δ13C and δ15N analysis offlora, fauna and sediments was per-formed with the aforementioned ele-mental analyzer, coupled to a Ther-moFinnigan delta + XL via a Conflo IIIinterface, with a typical reproduci-bility of ±0.15‰ for both δ13C andδ15N. The samples from the CWS,however, were all measured on a dualinlet Finnigan Mat delta E off-lineafter cryogenic purification of the CO2
or N2, with a reproducibility of 0.2‰for both δ13C and δ15N. All stable iso-tope ratios are expressed relative tothe conventional standards (VPDBlimestone and atmospheric N2) as δvalues (‰), defined as:
where X = 13C/12C or 15N/14N in the case of δ15N.
RESULTS
Sedimentary organic matter
Sediment at the upstream Gazi site had δ13C values(–25.2 ± 0.2‰) somewhat more enriched than man-grove leaf tissues and showed relatively high TOC/TNratios (16.0 ± 1.3 atom, Fig. 2). At the seaward site,however, δ13C values of sediments were higher andmore variable, particularly in the surface layers (thelatter on average –23.0 ± 0.9‰). Sediments in Galleand Pambala showed consistently low δ13C values(–27.8 ± 1.1 and –27.5 ± 0.9‰, respectively), high con-centrations of organic carbon and high TOC/TN ratios(Fig. 2). Sediments in the CWS showed the highestδ13C values and had low TOC and TOC/TN ratios(Fig. 2).
Primary producer stable isotope signatures
Different mangrove species from the 2 sites in Gaziall showed typical δ13C signatures, with averages rang-ing between –27.0 and –31.2‰ (Table 2, Fig. 3). The 3mangrove species collected in the CWS had δ13C val-ues similar to those found previously in the area (seeBouillon et al. 2002), but 2 species had markedlyhigher δ15N values (Avicennia marina: +8.9‰ andExcoecaria agallocha: +8.8 ± 0.3‰, Table 3, Fig. 3).Mangrove leaf tissues from Pambala all showed rather
δ13 310C sample standard
standard=
−×
X X
X
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Fig. 2. Relationship between (a) sedimentary total organic carbon content (TOC)and δ13C of sediment organic carbon, and (b) sediment TOC/TN (total nitrogen)ratios (atom) and δ13C of sediment organic carbon, for the different systems/sitesstudied. Note that some additional data for Galle and Pambala, and all TOCand TOC/TN data for the CWS (Coringa Wildlife Sanctuary) were taken from
Bouillon et al. (2003)
a b
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low δ13C values, with averages ranging between –29.2and –31.2‰ for various mangrove species (Table 4,Fig. 3). The most depleted δ13C values for mangrovetissues, consistently lower than –30‰, were found inRhizophora apiculata and Bruguiera gmnorrhiza fromGalle (Table 4, Fig. 3). E. agallocha, however, whichmostly grows at slightly elevated patches in this area,had δ13C values in the usual range, averaging –28.6‰.In contrast to mangrove tissues, micro-epiflora grow-ing on mangrove stems (the composition of which wasnot studied) showed consistently low δ15N values in allareas studied: –8.2‰ in the CWS, –6.8‰ in both Galle
and Pambala, and –2.4‰ in Gazi. δ13C values for theseepiphytes were highly variable: –21.4‰ in the CWS,–24.2‰ in Gazi, –29.2‰ in Galle and –32.0‰ in Pam-bala (Tables 2 to 4, Fig. 3). It should be noted that alldata of micro-epiflora were gathered on pooled sam-ples and we have no indications of the variability inisotope signatures of this source. Due to difficulties insampling, we only have data for microphytobenthosfrom the upstream site in Gazi (δ13C: –22.0‰, δ15N:+1.8‰), but previous data from the CWS were avail-able (δ13C: –17.3 ± 1.7‰, δ15N: +1.7 ± 1.7‰, see Bouil-lon et al. 2002).
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Fig. 3. Plot of δ15N versus δ13C for epifauna from the 5 study sites. (a) Upstream site along Kidogoweni creek (Gazi Bay, Kenya),(b) the seaward site (Gazi Bay, Kenya), (c) Coringa Wildlife Sanctuary, India, (d) Galle, Sri Lanka and (e) Pambala lagoon, Sri
Lanka. Note the different scale of the y-axis in (c). See Table 1 for site characteristics
a b
c d
e
Bouillon et al.: Resource utilization patterns of mangrove epifauna
Consumer stable isotope signatures
Invertebrates from both sites in Gazi showed quitediverse stable isotope signatures, ranging overallbetween –30.3 and –16.4‰ for δ13C, and between 1.1and 7.2‰ for δ15N (Table 2, Fig. 3). However, δ13Cvalues were typically higher at the seaward site(Fig. 3). Our δ13C data on mangrove sesarmids are
highly variable both within andbetween different systems (overallrange: –30.3 to –18.9‰, with a fairlyeven distribution between these ex-tremes). In the CWS, for example(Table 3, Fig. 3), average δ13C valuesfor sesarmids were –25.4‰ (adultPerisesarma bengalensis and Epis-esarma versicolor), –24.0 (juvenile P.bengalensis), –23.8‰ (Parasesarmaasperum), and –19.5‰ (juvenile Pa-rasesarma plicatum). As previouslynoted for this area (Bouillon et al.2002), ocypodid crabs (3 Uca spp.)and Metaplax distinctus were foundat the more enriched end of the δ13Crange, and mollusks showed a diverseδ13C and δ15N pattern (Table 3,Fig. 3). With the exception of Ucalactea annulipes, invertebrates fromGalle all showed relatively uniformδ13C values (Table 4, Fig. 3), withaverages between –27.5 and –24.8‰.However, δ15N values ranged morewidely, with unusually low values forPythia plicata (–2.4 ± 0.7‰) and highvalues for the 2 bivalves examined(i.e. Polymesoda spp. and an uniden-
tified oyster, 5.7 ± 1.4 and 8.0 ± 0.2‰, Table 4, Fig. 3).Invertebrates from Pambala, with the exception ofCerithidea cingulata, similarly showed a fairly narrowrange of δ13C signatures, with averages between–28.5 and –24.3‰ (Table 4, Fig. 3). As in Galle, thefilter-feeding Polymesoda spp. showed distinctlyhigher δ15N values (8.4 ± 0.5‰) compared to otherinvertebrates (0.6 to 6.2‰).
Table 3. Overview of stable isotope data (average ±1 SD) for flora, sedimentsand epifauna from the Coringa Wildlife Sanctuary, Andhra Pradesh, India. Notethat additional data from this area (but different localities within the CWS)
can be found in Bouillon et al. (2002)
Fig. 4. Relationship between surface sediment δ13C values and those recorded in various species of (a) Sesarminae, (b) Uca spp.and (c) gastropods (data from all species at a specific site were pooled for c). Data were compiled from the 5 sites mentioned inthis study and additional literature data (data sources available on request). D: literature data; s: data from this study. Greyshaded areas show typical range of values for mangrove-derived organic matter. Literature data taken from Fry (1984), Rodelli
et al. (1984), France (1998), Thimdee et al. (2001), Bouillon et al. (2002) and Hsieh et al. (2002)
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DISCUSSION
Differences in sedimentary organic matter origin
The different sites in this study represent differentgeomorphological settings (i.e. estuarine, lagoonal andbasin forests, sensu Lugo & Snedaker 1974) with varyingtidal amplitude and, therefore, the relative importance oflocal vascular plant material and aquatic organic mattersources to the sedimentary pool varies significantly(Fig. 2). It has previously been shown (Bouillon et al.2003) that for the majority of systems, these parameters
reflect the balance between local inputsfrom mangroves (high TOC, highTOC/TN and low δ13C) and inputsfrom the water column (low TOC,low TOC/TN and higher but variableδ13C). Thus, our data show that both thefringing lagoonal mangroves in Pam-bala and the basin forest of Galle are‘retention’ sites, where mangrove car-bon accumulates and dominates thesedimentary organic matter pool. Forthe CWS and Gazi, however, a balanceexists between local mangrove inputsand tidally imported organic matter(see also Hemminga et al. 1994, Slim etal. 1996). Moreover, the data from theseaward site in Gazi show that seagrassinputs (with δ13C values in the areabetween –19.7 and –10.7‰, Hemmingaet al. 1994, authors’ unpubl. data) aremore important at this location than atthe upstream sampling site .
Consumption of different primaryfood sources by mangrove epifauna
Before discussing the differences inC and N sources for epifaunal commu-nities between different sites, we willfirst briefly examine the major primaryorganic matter sources for the 2 domi-nant groups of epifauna, i.e. brachy-uran crabs and mollusks, at thedifferent sites studied.
Brachyuran crabs
Brachyuran crabs and mollusks aretypically the dominant groups of man-grove epifauna and can attain veryhigh densities (e.g. Ashton & Macin-
tosh 2002). Their role in nutrient cycling (Lee 1998)and in sediment biogeochemistry, via bioturbation, istherefore considered to be large. Even though thefocus of most studies has been on the effect of sesarmidcrabs on leaf litter dynamics (e.g. Ashton 2002), severalstudies have stressed that different groups of man-grove crabs display a wide range of feeding prefer-ences. Although for several of the larger species δ13Cvalues were on average within ~4‰ of those of man-grove tissues (which indicates substantial inputs frommangrove litter, albeit with some contributions of otherdietary sources), several species showed consistently
Table 4. Overview of stable isotope data (average ±1 SD) for flora, sediments,particulate organic carbon (POC) and epifauna from Pambala and Galle,
Sri Lanka
Bouillon et al.: Resource utilization patterns of mangrove epifauna
high δ13C values tending towards those typical ofmicrophytobenthos (e.g. Perisesarma spp. from Gazi:–20.1 ± 0.5 and –22.1 ± 0.3‰, Parasesarma plicatumfrom the CWS: –19.5 ± 0.4‰). Thus, although somemangrove sesarmids undoubtedly rely substantially onmangrove carbon, this is clearly very species-specific.Secondly, when comparing sesarmid δ13C data from allthe sites studied here and with the inclusion of litera-ture data, we find (despite the species-specific varia-tion) a good overall correlation between the isotopesignature in sedimentary organic carbon and that insesarmids (Fig. 4a, Spearman rank correlation test: p =0.0057, R2 = 0.37). The latter confirms the idea thatmany sesarmids may spend more time feeding on thesediment surface than actively searching for fallenleaves (Skov & Hartnoll 2002) and indicates that the Cand N source for this group of epifauna will partiallydepend on the geomorphological settings of the sys-tem, as the latter is a primary determinant of the originof sedimentary organic matter (Bouillon et al. 2003).Such a correlation with sediment δ13C values is not sig-nificant (Spearman rank correlation test: p = 0.349, R2 =0.06) for the second major group of brachyurans foundin mangroves, ocypodid crabs (mostly Uca spp. andMacrophthalmus spp., see Tables 2 to 4). Ocypodidcrabs are typical deposit feeders which forage on thesediment surface. Stable isotope data presented earlier(e.g. Rodelli et al. 1984, Marguillier et al. 1997, France1998, Hsieh et al. 2002) and in this study consistentlyshow high δ13C values, ranging between –24.5 and–12.5‰, with an average of –18.9 ± 2.3‰, and with adistribution markedly different from that of sesarmids.These data indicate a clear selectivity for 13C-enrichedcarbon sources such as microphytobenthos. Amongthe other brachyuran crab taxa associated with man-groves, Eurycarcinus natalensis, Epixanthus dentatusand Metopograpsus thukuhar from Gazi Bay clusteredclose together and their stable isotope signatures (highδ13C and δ15N, Table 2) are suggestive of little directinputs from mangroves and of significant predation onlower trophic levels, consistent with literature data(e.g. Dahdouh-Guebas et al. 1999).
Mollusks
Most of the scarce, previously published stable iso-tope data for bivalves from intertidal mangrove habi-tats (Rodelli et al. 1984) point towards microalgal foodsources, but the data presented here show a morediverse pattern. Both the Polymesoda spp. (sampled inthe CWS, Galle and Pambala) and the unidentifiedoyster from Galle show consistently low δ13C signa-tures, close to those of mangrove tissues. However, thisresemblance does not necessarily indicate a strong
reliance on mangrove carbon, as aquatic microalgalproduction may be similarly depleted in 13C due to lowδ13C values in the dissolved inorganic carbon (DIC)pool (e.g. surface water δ13CDIC values in Galle rangedbetween –14.2 and –7.8‰, authors’ unpubl. data,whereas typical seawater values are close to 0‰). Thedata in Table 4 (see also Fig. 3) also show that thesebivalves were consistently enriched in 15N comparedto most other consumers in the ecosystem, despite sim-ilar δ13C values. For Galle, the only site with significantpermanently inundated sites, suspended organic mat-ter was similarly enriched in 15N compared to sedimentorganic matter. Thus, the situation for these bivalvespecies remains somewhat unclear, with strong contri-butions from either mangrove-derived material (aftermicrobial processing in the water column, which canresult in higher δ15N values, e.g. see De Brabandere etal. 2002) or from aquatic primary production. A specialgroup of bivalves are wood-boring species such as theTeredinidae (which were sampled in the CWS), knownto harbor symbiotic cellulolytic bacteria capable ofN2-fixation. Our δ13C data of Teredinidae (–24.6 ±0.4‰) are consistent with Avicennia wood (δ13C:–25.7‰) being the major C source, but the δ15N signa-tures of the Teredinidae (+5.8 ± 0.5) are only slightlyhigher than those of the log (δ15N: +5.1‰) in whichthey were collected, indeed suggesting an additionalinput of N2-fixation to the N-requirements of thesebivalves. Another bivalve from dead mangrove woodin Gazi, Trapezium cfr. sublaevigatum (which does nothave such a symbiotic relationship), showed δ13C andδ15N values markedly more distant from those of man-groves (Table 2, Fig. 3), suggesting additional inputsfrom aquatic C and N sources.
Two previous studies have found unexpectedly lowδ15N values in some mangrove mollusks (Christensenet al. 2001, Bouillon et al. 2002) and similar data wereobtained here, i.e. for Pythia plicata from Galle,Onchidium spp. from the CWS and to a lesser extentfrom Gazi, and for Littoraria scabra from Gazi (seeTables 2 to 4, Fig. 3), all of which are species typicallyfound grazing on mangrove roots or stems. The unusu-ally low δ15N values found here in micro-epiflora (δ15N= –6.8‰ in both Pambala and Galle, δ15N = –8.2‰ inthe CWS, –2.4‰ in Gazi Bay) offer a convincing expla-nation for these consumer δ15N values and indicate asignificant input of N from such a source. The δ15N val-ues of the epiflora are likely to reflect the importanceof atmospheric nitrogen (from precipitation and/orthrough N2-fixation) as their N source (see e.g. Hietz etal. 1999 for vascular epiphytes). It is worth noting thatsome other gastropods often found in large numberson mangrove stems, such as Cerithidea obtusa (foundin the CWS, see Table 3) or C. decollata (found in Gazi,see Table 2) do not show evidence of extensive feeding
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on 15N-depleted epiflora, but as these species are alsofound on the sediment surface, the isotope data sug-gest that these are more likely to feed on sedimentorganic matter and microphytobenthos. In conclusion,the δ13C and δ15N patterns (Fig. 3) indicate a diverserange of feeding preferences for mangrove-inhabitingmollusks.
Differences in C and N utilization between contrasting mangrove systems
In a previous study, we found no evidence for a dom-inant role of mangroves in sustaining epifaunal inver-tebrate communities (Bouillon et al. 2002). However, asthese data came from an estuarine system wheretidally imported organic matter was found to dominatethe sediment pool, we hypothesized that such a situa-tion may not be representative for other types of man-grove systems, in particular for those where exchangeof material with the aquatic environment is limited dueto low tidal action.
The data gathered in this study provide a first test ofthis hypothesis. First, as noted above, we found thatthe origin of sedimentary organic matter at least par-tially determines the overall dependency of sesarmidcrabs on different primary sources (Fig. 4a), despite theobvious fact that different species have different feed-ing specializations. In Fig. 4c, data for all gastropodspecies are presented per site with data from thisstudy, as well as those given in Rodelli et al. (1984) andBouillon et al. (2002). Again, despite their varyingfeeding specializations (some being selective forepiflora, microphytobenthos or mangrove litter, see‘Mollusks’ above), an analogous pattern as that foundfor sesarmids shows up for gastropods, i.e. a markedlylower direct use of mangrove carbon in estuarine foresttypes where inputs from the aquatic environment aresignificant (Spearman rank correlation test for the rela-tionship between sediment and gastropod δ13C: p =0.029, R2 = 0.86). It is worth mentioning that the slopeof the relationship between δ13C of consumers andsediments is markedly different for sesarmids (slopeof ~0.56) and gastropods (slope of ~1.0).
The same conclusions are also evident when compar-ing the panels in Fig. 3: much of the species data for thelow-amplitude sites in Sri Lanka cluster quite closelytogether in the range expected for species that assimilatesignificant mangrove-derived organic matter (from thesediment pool); for the upstream site in Gazi and for theCWS the data are more scattered; and at the seawardsite in Gazi, a clear trend towards much more enrichedvalues is evident. However, for both Pambala and Galle,our δ13C values for most mangrove tree species arerather low. Roggeman (2002) analyzed Rhizophora
mucronata leaves from both areas during the same sam-pling period and found typically higher δ13C values,ranging between –29 and –25‰. A clear relationshipwith tree age (as measured by the circumference of thetree crown or the height of the tree) was found, withyounger trees showing more negative δ13C values (be-tween –32 and –30‰). A generally more enriched δ13Csignature for mangrove leaf tissues at both Galle andPambala would be consistent with indications from sed-imentary TOC and TOC/TN data that the organic matterpool is derived primarily from mangrove tissues, and thesediment δ13C signatures (–27.5 ± 0.9‰ in Pambala,–27.8 ± 1.2‰ in Galle) are indeed closer to the data fromRoggeman (2002). In this interpretation, the trophicdependency of epifauna on mangroves in both Galle andPambala would overall be large, and likely to occur bothdirectly through feeding on mangrove leaves and indi-rectly through feeding on sediment organic matter(which is strongly enriched in N compared to senescentmangrove leaves, e.g. see Skov & Hartnoll 2002). Finally,it should be mentioned that our sampling design did notaccommodate potential seasonal and/or spatial varia-tions in the foodweb structure within sites. However,even if such variations were present, we do not see anyarguments to conclude that these would interfere withthe general patterns observed in Figs. 3 & 4.
Results of litter removal experiments and stableisotope analyses: how compatible are they?
The idea that much of the mangrove litter producedis removed and/or consumed by mangrove epifauna(at least in the Indo-Pacific, McIvor & Smith 1995 andeven there not in all forest zones alike or depending onthe tidal stage, see Slim et al. 1997 and Ólafsson et al.2002) seems to contrast with the stable isotope resultspresented and compiled in this study. They demon-strate that, from a community perspective, only a lim-ited number of species rely substantially and directlyon mangrove carbon, and that, when available, arange of other sources are used by the invertebratecommunity. There are several points which can beraised to reconcile these 2 superficially contrastingviewpoints. First, the fact that a large proportion of theleaf litter is removed and/or consumed by the localcrab fauna does not necessarily imply that mangroveleaves are the dominant item in their diet, as the popu-lation of sesarmids may consume even more of ‘some-thing else’. In this respect, the study of Skov & Hartnoll(2002) is particularly enlightening, as their field obser-vations clearly demonstrate that sesarmids spend con-siderably more time feeding off the sediment surfacethan collecting or eating leaves. Even though this doesnot necessarily imply that more sediment organic mat-
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ter is assimilated than mangrove leaves, it does indi-cate the importance of deposit feeding. Evidently, thesources of organic matter present in the sediment andthe degree of selectivity with which sesarmids feed onit (both of which may be highly variable) will furtherdetermine which carbon sources contribute to theirdiet and in which proportions. Secondly, much of thework on the trophic significance of different sourcesin mangrove ecosystems has focussed on a limitednumber of invertebrate groups or species, notablysesarmids and a disproportionate number of studies onTerebralia palustris (e.g. Slim et al. 1997). From a com-munity perspective, however, this may severely biasour view of the importance of mangrove litter, as theoften diverse invertebrate community apparently dis-plays a wide variety of feeding specializations.
Lastly, it should also be noted that in view of the sig-nificant differences in elemental ratios between differ-ent food sources available to intertidal consumers (e.g.mangrove leaves have a very low N content, micro-phytobenthos is much richer in N, etc.), the contribu-tions of C and N from any dietary source are not nec-essarily equal, but likely to be proportional to the C/Nratios of the substrates. The latter implies that thedependency in invertebrate communities on man-grove-derived N will generally be less than theirdependency on mangrove-derived C.
CONCLUSIONS
Our data strongly suggest that where multiple C andN sources are available, intertidal mangrove epifaunalcommunities exploit all available food resources withclear and consistent differences in utilization patternsbetween different taxa or species. Secondly, we haveshown a strong influence of the relative inputs of localand tidally imported carbon sources (as reflected insedimentary δ13C values) on the relative importance ofmangrove carbon to several groups of epifauna. Thisvariability shows strong similarities to the variablecontribution of different carbon sources to sedimen-tary microbial communities observed across variousmangrove sites (Bouillon et al. 2004).
Although δ15N was a poor source indicator except formicro-epiflora, which showed consistently low δ15Nvalues in all sites (–2.4 to –8.2‰), we can expect that theimportance of mangroves as a N source for invertebratesis less than for C, due to the low N content of mangrove-derived organic matter. Finally, it is worth pointing outthat the areal extent of ‘closed’ mangrove systems (i.e. inwhich mangroves appear to provide most of the carbonfuelling epifaunal and microbial communities) is ratherlimited on a global scale, as the largest mangrove-covered areas are found in estuarine and deltaic systems.
Acknowledgements. Funding for this work was provided bythe Fonds voor Wetenschappelijk Onderzoek (FWO-Vlaan-deren, contract G.0118.02) and by EC-INCO project contractERB IC18-CT98-0295. S.B. and T.M. are both postdoctoral fel-lows with the FWO-Vlaanderen. We are grateful to K. Ratnamfor help during fieldwork in India, to I. De Mesel, A. V. Borgesand the staff of the Kenya Marine and Fisheries ResearchInstitute (Mombasa) for fieldwork assistance in Kenya, to V.de Schuyter, M. Roggeman and A. Verheyden for help duringsample collection in Sri Lanka, to P. Davie (QueenslandMuseum, Australia) and D. P. Gillikin for their expertise inidentifying most of the crabs, and to A. Callea for his help inidentifying some of the mollusks from Kenya. The excellenthelp of J. Bosire and J. Kairo in organizing logistics in Kenyawas much appreciated. D. Gillikin and 3 anonymous refereesprovided very insightful and constructive comments to anearlier version of this manuscript.
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Editorial responsibility: Otto Kinne (Editor),Oldendorf/Luhe, Germany
Submitted: March 23, 2004; Accepted: June 8, 2004Proofs received from author(s): September 2, 2004
