N. R. Loneragan á S. E. Bunn á D. M. Kellaway

Are mangroves and seagrasses sources of organic carbonfor penaeid prawns in a tropical Australian estuary?A multiple stable-isotope study

Received: 21 January 1997 /Accepted: 13 August 1997

Abstract We used multiple stable-isotope analysis toinvestigate the importance of seagrasses, mangroves andother primary sources (macroalgae, seston) to the foodwebs supporting penaeid prawns in the Embley Riverestuary and adjacent o�-shore waters in the north-east-ern Gulf of Carpentaria, Australia. Mangroves, seagrassand macroalgae/seston were well separated on the basisof their d13C values in both the dry and the wet seasons.In contrast, only macroalgae and seston (phytoplanktonand zooplankton), which had similar d13C values, wereseparated by their d15N values. The primary source ofcarbon supporting food webs of several species of ju-venile penaeid prawns clearly depended on the locationwithin the estuary. The d13C values of juvenile prawns(Penaeus esculentus, P. semisulcatus and Metapenaeusspp.) in seagrass beds were close to those of seagrass andseagrass epiphytes, particularly in the dry season. Thiswas despite the proximity of the seagrass to mangrovesand the presence of mangrove detritus in the seagrassbeds. Juvenile prawns (P. merguiensis, P. semisulcatus,and Metapenaeus spp.) in an upstream mangrove creekhad d13C values that were midway between those ofmangroves and seagrass, and close to those of macro-algae and seston during the dry season. Mangrovescould have made a signi®cant contribution to the carbonassimilated by juvenile prawns at this site, but only if it isassumed that the remainder of the carbon is ultimatelyderived from a seagrass source. The d13C values ofadults of three species of prawns in o�shore waters were

very similar and were much higher than those of man-groves. The considerable amount of mangrove/terres-trial carbon exported from tropical Australian estuariesduring the wet season is therefore unlikely to contributeto o�shore food webs supporting adult prawns. Fur-thermore, the contribution of mangrove/terrestrialsources to the food webs of juvenile prawns appears tobe limited to a very small spatial scale ± within themangrove fringe of small creeks and mainly during thewet season.

Introduction

Mangroves are conspicuous features of many tropicalcoastal systems, where they stabilise banks and sedi-ments, take up nutrients, and provide habitats for ju-venile crustaceans and ®sh (Hatcher et al. 1989;Robertson and Blaber 1992). Mangroves also producelarge amounts of organic matter via litterfall, and thiscan be exported far o�shore (Robertson et al. 1991). Thefate of this material is not certain: does this ``outwelling''of carbon and nutrients form the basis of coastal foodwebs, or does it simply accumulate as inert matter in thesediments (Robertson et al. 1992; Lee 1995)? Recentstudies of prawn food webs in mangrove systems usingstable-isotope analyses have shown that mangroves donot make a major contribution to coastal food webs(Stoner and Zimmerman 1988; Newell et al. 1995; Pri-mavera 1996). However, the seasonal dynamics of thesesystems and associated potential changes in the primaryfood sources (as measured by stable-isotope analysis)were not considered, and the replication of samples,both within and between habitats, was limited. Fur-thermore, these systems were ones in which mangrovesare the dominant macrophyte and seagrasses were notimportant.

In northern Australia, the very marked summer wetseason, in which 80 to 90% of the annual rainfall occurs,has a major in¯uence on estuaries and coastal systems.In this region, mangroves provide the critical nursery

Marine Biology (1997) 130: 289±300 Ó Springer-Verlag 1997

Communicated by G.F. Humphrey, Sydney

N.R. Loneragan (&)CSIRO Division of Marine Research,Cleveland Marine Laboratories, P.O. Box 129,Cleveland, Queensland 4163, Australia

S.E. Bunn á D.M. KellawayCentre for Catchment and In-Stream Research,Faculty of Environmental Sciences, Gri�th University,Nathan, Queensland 4111, Australia

habitat for the postlarvae and juveniles of the bananaprawn (Penaeus merguiensis), while seagrasses andmacroalgae are the nursery habitats for tiger prawns(P. esculentus and P. semisulcatus) (Staples et al. 1985;Haywood et al. 1995). Previous studies of the stomachcontents of these species have found considerableamounts of detritus in P. merguiensis (Robertson 1988)and plant material in P. esculentus (O'Brien 1994).However, it is not known whether this detritus and plantmatter is assimilated by the prawns and, indeed, whetherthese sources support prawn food webs.

We used stable-isotope analysis (carbon, nitrogenand sulphur) to investigate the contribution of sea-grasses, mangroves and macroalgae to the food webs ofjuvenile penaeid prawns in the Embley River estuary,north eastern Gulf of Carpentaria, Australia (Fig. 1).The contribution of mangroves to prawn food webs wasexamined: (1) within small mangrove-lined creeks;(2) within seagrass beds about 200 m from the mangrovefringe; and (3) in o�shore waters, 20 to 50 km frommangrove forests. We also determined whether the pri-mary food sources of penaeid prawns changed under thein¯uence of the tropical wet season.

Materials and methods

Study area

The Embley River estuary (12°40¢S; 141°50¢E: Fig. 1) containsseveral large (>3 ha) intertidal beds of seagrass (Enhalus acoroides,Halodule uninervis and Halophila ovalis) and smaller ('1 ha) sub-tidal beds of algae (mostly Caulerpa spp.) (Haywood et al. 1995).For much of its length, the estuary is lined with mangrove-forestcommunities, each dominated by Rhizophora stylosa, Ceriops tagalvar. australia, or Avicennia marina var. eucalyptifolia (Long et al.1992). The tidal amplitude at the mouth of the Embley River is�3.0 m on spring tides and �2.4 m on neap tides.

Two intertidal ``seagrass'' sites and two ``mangrove sites'', be-tween 11 km (Sg1) and 15 km (Mn2) from the mouth of the Em-bley River estuary, were sampled (Fig. 1). The inner edge of theseagrass at Sg1 is �200 m from the fringing mangroves, while thatat Sg2 is �1 km from the nearest mangroves at Mn1. Sparse sea-grass beds are located �2 km upstream of Mn2.

Mean monthly water temperatures at night ranged from 27.5 inthe pre-wet season (September) to 31.5 °C early in the wet season(December) at Sg1 and Mn2 in 1991/1992 (Fig. 2). The ®rst rainfallduring 1991/1992 at Weipa airport, 10 km east of the mouth of theEmbley River estuary, was recorded in November (61 mm: Fig. 2).Monthly rainfall was highest in February (584 mm) and March(348 mm) and decreased markedly in April and May (<25 mm).The rainfall during the summer wet season (December to March)accounted for 93.5% of the total rainfall between September andMay (1703 mm). Mean monthly salinities at both Sg1 and Mn2exceeded 36& between September and December, then declined tominima in March (18.9 at Sg1 and 12.9& at Mn2) associated withthe heavy summer rainfall. Salinities increased to >30& in April atSg1 and May at Mn2.

Juveniles of ®ve species of commercially important penaeidprawns (Penaeus merguiensis, P. esculentus, P. semisulcatus, Meta-penaeus endeavouri and M. ensis) and several non-commercialspecies (Trachypenaeus spp., M. moyebi, M. conjunctus, M. ebo-racensis) have been recorded from the Embley River estuary (Sta-ples et al. 1985).

Sample collection

In most cases, at least three samples of the major primary pro-ducers, prawns and other consumers were collected from all sites inNovember 1991 (dry season) and March 1992 (wet season). Sea-grass leaves and algae were collected by hand or grab from at leastthree locations at Sg1 and Sg2. Algae were also collected from Mn2during the dry season. Mangrove leaves were collected from thegrowing tips of di�erent trees in mangrove forests near each site,except Sg2. There is virtually no change in the d13C values ofmangrove and seagrass leaves during decomposition (Zieman et al.1984). At least three sediment samples of the top 10 cm of substratewere taken by grab from each site. Di�erent size fractions ofbenthic organic matter were sieved from the sediment samples (seenext subsection) and the stable-isotope values of the benthic or-ganic matter were determined.

Fig. 1 Location map of mangrove (Mn) and seagrass (Sg) samplingsites in Embley River estuary, north-eastern Gulf of Carpentaria,Australia (Stippled area extent of intertidal seagrass along southernbank of Embley River estuary)

Fig. 2 a Mean water temperature at mangrove (Mn2) and seagrass(Sg1) sites in Embley River estuary; b monthly rainfall for Weipaairport between September 1991 and May 1992

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Samples of seston were collected by towing a 250 lm net in thetop 0.5 m of the water column for 2 min during the night in deeperwater near each site, and at the mouth of the Embley River estuary.During the wet season, because the nets very quickly clogged withseagrass leaves and other coarse organic matter, only a few samplesof seston were obtained. To provide an additional indication of thestable-isotope signatures for seston, barnacles and oysters werecollected from mangrove prop roots and channel markers near thefour sites. No live barnacles or oysters were found during the wet-season collecting trip.

Juvenile prawns were collected at the four sites in the EmbleyRiver estuary in a small beam trawl (1 ´ 0.5 m mouth with 2 mmmesh in the body and 1 mm mesh in the cod-end). Wherever pos-sible, prawns were identi®ed to species and sorted into di�erentsize-groups: <3 mm carapace length (CL); 3 to 5.9 mm CL; 6 to9.9 mm CL; and ³10 mm CL. Juveniles in the genus Metapenaeus(mostly M. moyebi, with some M. endeavouri and M. ensis) weredi�cult to separate into species in the ®eld. (Statistical analysesshowed that there were no signi®cant di�erences in d13C and d15Nvalues between species in the genus Metapenaeus, so juveniles inthis genus were therefore considered as a single taxon.)

Samples of prawns were also obtained in the o�shore waters ofAlbatross Bay from a commercial ®shing vessel and were identi®edto species. Three regions were trawled: 20 km from the mouth of theEmbley River estuary (10 to 15 m deep); 30 to 40 km o�shore (15 to30 m deep); and about 50 km o�shore (30 to 40 m deep). To de-termine the maximum range of values likely to be found for prawnso�shore, only two size groups of prawns were considered: 15 to25 mm CL (juveniles and subadults); and ³35 mm CL (adults).

Sample preparation

Samples of seagrass leaves and macroalgae were rinsed in fresh-water to remove detritus and loose epiphytes. Epiphytes were ob-tained only from the large strap-like leaves of the seagrass Enhalusacoroides ± they were removed by gently scraping with a scalpelblade. The seagrass leaves and algae were not bathed in acid as hasbeen done in the past because this procedure can a�ect d15N values(Bunn et al. 1995). The epiphytes from E. acoroides were washed indistilled water and collected on Whatman glass-®bre (Type GF/C)®lters. Their biomass was very low, particularly in the wet seasonwhen no samples of epiphytes were obtained. Mangrove leaveswere rinsed in distilled water.

Sediment samples were washed through four sieves (4, 1, 0.5and 0.25 mm). Benthic organic matter was then elutriated from the0.25 to 0.5 mm and 0.5 to 1 mm inorganic sediment size-fractions.Seston samples were also sieved into 0.25 to 0.5 mm and 0.5 to1 mm size-fractions.

The tissue of barnacles and oysters was removed from theirshells. A sample of the abdominal muscle tissue of juvenile (³3 mmCL) and adult prawns was taken after the exoskeletons and di-gestive tracts had been removed. In virtually all cases, the stable-isotope values were determined for individual barnacles, oystersand prawns, which gives a much better estimation of the within siteand season variation in stable-isotope values than is possiblethrough pooling individuals for analysis.

All samples were frozen and stored at )20 °C before stable-isotope analysis.

Stable-isotope analysis

All samples were oven dried at 60 °C for 24 h. Small volumes ofdried plant material and all animal tissue were ground with amortar and pestle. Larger volumes of plant material were ground ina rotary vane mill.

Dried and weighed samples (�5 to 10 mg for plant matter, 3 to5 mg for animal matter) were oxidised, and the resultant CO2 andN2 were analysed with a continuous ¯ow±isotope ratio mass spec-trometer (Europa Tracermass, Crewe, England). Ratios of 13C:12Cand 15N:14N were expressed as the relative per mil (&) di�erence

between the sample and conventional standards (Pee Dee Belem-nite carbonate and N2 in air) as follows:

dX � Rsample=Rstandard ÿ 1� �� 1000�&� ; �1�

where X = 13C or 15N, and R = 13C:12C or 15N:14N.Initially, samples were processed in dual isotope mode to

obtain values for their C and N content and d13C. Samples werethen reanalysed in single isotope mode to obtain more accurateestimates of d15N. Some preliminary samples of mangroves, sea-grass and prawns collected in January 1991 (i.e. early in the wetseason) were sent to the Waikato Stable Isotope Laboratory,Hamilton, New Zealand, for d34S analysis, in addition to d13Cand d15N.

Data analyses

Before testing for di�erences in stable-isotope ratios of prawnsbetween sites and seasons, di�erences in stable isotope values be-tween size classes of juvenile prawns were tested with one-wayanalyses of variance (ANOVAs, with Tukey's HSD multiple-rangetest) for each site and season. This process was followed, ratherthan three-way ANOVAs (size, site, season) because not all size-classes were caught at each site in each season. Although six of the15 ANOVAs for d13C showed signi®cant di�erences between size-classes, these di�erences were usually small (<2&) compared withdi�erences between sites and seasons. Size was a signi®cant factorin only one of the 15 tests for d15N. Means were therefore calcu-lated for juveniles of each species of prawn ignoring size-class, anddi�erences in stable-isotope values between species, sites and sea-sons were tested using three-way ANOVAs and Tukey's HSDmultiple-range test, ignoring size.

The possible contributions of mangrove, seagrass and sestoncarbon to the assimilated carbon in penaeid prawns were calculatedfrom the following simple mixing model:

PA � �d13CConsumerÿfÿd13CsourceB�=�d13CsourceAÿd13CsourceB� ; �2�where PA = proportion of source A; and f = isotopic fractiona-tion (&). An isotopic fractionation of 1 was used (see Peterson andFry 1987). The mixing model calculates the contribution of eachprimary source assuming that only two sources are contributing tothe isotope signature of the consumers. By using di�erent endpoints, the range of possible contributions of di�erent primarysources can be estimated.

Three di�erent pairs of end points were used in the mixingmodel: mangroves and seagrass; mangroves and seston; and sea-grass and seston. Each of these was applied to the overall mean datafor the seagrass sites in each season and to the mean data for o�-shore prawns. Since seston values were obtained from only a fewsites in the wet season, the mean for seston, pooled over all sites andsizes, was calculated in each season and used in the mixing models.Because of di�erences in consumer signatures between mangrovesites, data for each mangrove site were analysed separately.

Results

Primary sources

The marked di�erences in mean d13C values among themajor primary sources of organic matter (mangroves,seagrass, macroalgae and seston), pooled over di�erentsites, are clearly shown in Fig. 3; the means �95%con®dence limits for each macrophyte category do notoverlap. Although macroalgae and seston had similard13C signatures, seston had higher d15N values (Table 1,Fig. 3). The mean d13C for epiphytes on Enhalus acor-

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oides in the dry season ()13.3&) was 4& lower than thatfor the seagrass host (Table 1).

Amongst the seagrasses, the mean d13C values forHalodule uninervis and particularly Halophila ovalis werehigher in the dry season than in the wet season. Theconverse was true for their mean d15N values (Table 1,Fig. 3). The mean d13C values of Enhalus acoroides werehigher than those of the other seagrasses and, togetherwith the mean d15N values, showed little variation be-tween seasons.

Caulerpa spp. at Mn2, and other macroalgae (in-cluding species of Gracilaria, Tolydonia, Hypnae andEuchuma) at the seagrass sites, had lower d13C valuesthan those of the seagrass (Table 1, Fig. 3). As withseagrass, the mean d13C value for algae at Sg1 and Sg2was higher in the dry season than in the wet season. Themean d15N values of algae were similar to those recordedfor seagrass and were higher in the wet than in the dryseason.

Mangroves had much lower mean d13C values(range = )28.7 to )27.0&) than the macroalgae andespecially the seagrass. There was also less variationbetween species and seasons in mangrove d13C values,than with the seagrasses and macroalgae (Table 1,Fig. 3).

Seston values for d13C were similar in magnitudeamong sites, and between seasons and size fractions,with values ranging from )23.2 to )18.8& (Table 1).Seston also had mean d15N values that were similaramong the sites in the dry season (range = 5.3 to 6.6&).Microscopic examination of the di�erent size-fractionsindicated that virtually all the seston consisted of livingplankton.

Benthic organic matter

Fine benthic organic matter (0.25 to 0.5 mm) had meand13C and d15N values that varied between sites andseasons, much like the coarser material (0.5 to 1 mm)(Fig. 3a). The benthic organic matter at mangrove siteshad similar d13C and d15N values to those of mangroves

Fig. 3 Stable carbon (d13C) and nitrogen (d15N) isotope values forbenthic organic matter in dry and wet seasons (a), and individualbarnacles (b) and individual oysters (c) in dry season, at mangrove andseagrass sites in Embley River estuary, 1992/1992 (Symbols as inFig. 1; small and large symbols data for 250 to 500 lm and 500 to1000 lm benthic organic matter, respectively; dashed boxes 95%con®dence limits for major primary sources; Enhalus = E. acoroides;Hal. combined data for Halodule uninervis and Halophila ovalis)

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(Fig. 3a). The d13C values were lower at the mangrovethan at the seagrass sites, where they were highly vari-able (Fig. 3a). At the seagrass sites, the d13C values werehigher in the dry than in the wet season. In general, thed15N values of benthic organic matter di�ered littleamong sites and between seasons.

Barnacles and oysters

In the dry season, the d13C values of barnacles andoysters at Sg1, Sg2 and Mn1 were similar in magnitudeto those for macroalgae/seston (Fig. 3b,c). At Mn2, thed13C values were lower than at the other sites and wereintermediate between the mean d13C values for macro-algae/seston and mangroves.

At mangrove sites, in all except one case, the d15Nvalues for barnacles were lower than those at the sea-grass sites (Fig. 3). The d15N values of barnacles wereclose to those of seston, and higher than those of oys-ters.

Juvenile prawns

In the dry season at mangrove sites, the d13C values ofPenaeus merguiensis were very similar in magnitude tothose for P. semisulcatus and Metapenaeus spp.(range = )22.0 to )16&, Fig. 4a). The d13C values ofprawns at the mangrove sites were close to those formacroalgae/seston, and were 5 to 11& higher than thoseof mangroves.

In the dry season at the seagrass sites, the d13C valuesfor Penaeus esculentus, P. semisulcatus andMetapenaeusspp. were within the range )13 to )8.5&, which is muchhigher than for the last two species at mangrove sites(range = )23.2 to )10.5&), particularly Mn2 (Fig. 4b,c, d). The d13C values for prawns at the seagrass sitescorresponded to those for seagrass and epiphytes onEnhalus acroides (Fig. 4, Table 1).

In the dry season at the seagrass sites, the d15N valuesof Metapenaeus spp. were generally higher than thosefor Penaeus esculentus and P. semisulcatus (Fig. 4)(P. merguiensis were not found in seagrass during thisseason). They were also higher for P. semisulcatus at themangrove than at the seagrass sites. In the wet season,

Table 1 Mean stable-isotoperatios (�1 SE) for d13C andd15N for major primary sourcesin November 1991 (dry season)and March 1992 (wet season) inEmbley River Estuary, north-eastern Gulf of Carpentaria,Australia (Values in parenthesesnumber of stable-isotopevalues; ± no data)

Source and site d13C d15N

dry wet dry wet

MangrovesRhizophora stylosaMn2 )28.7 � 0.42 (3) )28.2 � 0.71 (4) 1.9 � 0.72 (3) 3.4 � 0.83 (4)Mn1 )28.3 (1) )28.8 � 0.45 (3) 3.7 (1) 1.3 � 0.04 (3)Sg1 )27.0 � 0.77 (2) ± 3.6 � 0.57 (2) ±

Ceriops (Mn2) )27.4 � 0.77 (3) )27.9 � 0.39 (2) 2.3 � 1.19 (2) 2.8 � 0.25 (2)

SeagrassEnhalus acoroidesSg2 )9.7 (1) ± 0.34 (1) ±Sg1 )9.3 � 0.19 (3) )10.5 � 0.19 (4) 1.9 � 0.66 (3) 1.7 � 0.26 (4)

Halodule uninervisSg2 )12.1 � 0.40 (4) )15.0 � 0.72 (3) 3.0 � 1.55 (3) 3.3 � 1.05 (3)Sg1 ± )13.3 � 0.37 (4) ± 5.7 � 0.96 (3)

Halophila ovalisSg2 )10.7 � 0.18 (4) )15.4 � 0.18 (4) 3.1 � 0.08 (3) 6.5 � 0.85 (3)

EpiphytesSg1 )13.3 � 0.91 (6) ± 2.4 � 1.72 (3) ±

AlgaeCaulerpa (Mn2) )23.0 � 0.51 (3) ± 0.3 � 0.43 (3) ±Sg1 and Sg2 )20.1 � 0.26 (12) )22.8 � 0.46 (8) 1.7 � 0.56 (11) 4.0 � 0.56 (7)

Seston(250±500 lm)Mn1 )22.0 � 0.57 (2) ± 5.3 � 0.28 (2) ±Sg2 ± )21.7 (1) ± ±Sg1 )19.3 � 0.19 (2) ± 5.7 � 0.08 (2) ±Embley entrance ± )23.2 � 0.27 (3) ± ±

(500 lm±1 mm) ±Mn2 )19.1 � 0.73 (4) ± 5.9 � 0.47 (3) ±Mn1 )21.9 � 0.44 (2) ± 5.4 � 0.05 (2) ±Sg2 )19.3 (1) )19.6 (1) ± 6.1 (1)Sg1 )18.8 � 0.26 (5) )19.3 (1) 5.7 � 0.48 (5) ±Embley entrance )20.1 � 0.47 (7) ± 6.6 � 0.47 (6) ±

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the d15N values for P. merguiensis, P. esculentus andP. semisulcatus were generally higher than in the dryseason, while those forMetapenaeus spp. were similar inthe two seasons.

Fig. 4 Stable carbon (d13C) and nitrogen (d15N) isotope values forindividual juveniles of Penaeus merguiensis (a), P. esculentus (b),P. semisulcatus (c), andMetapenaeus spp. (d) in dry and wet seasons atmangrove and seagrass sites in Embley River estuary, 1991/1992(Symbols, abbreviations and boxes as in Fig. 3)

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In the wet season at the seagrass sites, the d13C valuesof all species of juvenile prawns were lower and morevariable than in the dry season (Fig. 4). For Penaeusesculentus, P. semisulcatus and Metapenaeus spp., thedi�erence between seasons was signi®cant (dry seasonmean = )9.8&; wet season mean = )16.5&; F1,139= 378.5, p < 0.001), and they were generally in therange of seagrass or intermediate between seagrass andseston/macroalgae. A three-way ANOVA (species, sea-son, site) of the data for these three species at the sea-grass sites showed that the d13C values did not di�eramong species (F2,139 = 0.34, p = 0.71) or betweenseagrass sites (F1,139 = 1.88, p = 0.17). The d13C valuesof P. merguiensis were the lowest recorded at the sea-grass sites in the wet season, and were almost identical tothose recorded for this species from the mangrove sitesat the same time (Fig. 4a).

Sulphur values

At the start of the wet season in 1991, the d34S values forPenaeus esculentus (13.6 to 14.5&) from Sg1 were verysimilar to those for the seagrass Enhalus acoroides(14.9&), while those for P. merguiensis and P. semis-ulcatus at mangrove sites (6.9 to 9.7&) were betweenthose for E. acoroides and the mangrove Ceriops tagalvar. australia (6.9&) (Fig. 5). Although no d34S valueswere obtained for macroalgae or seston, the followingvalues are summarised in Newell et al. (1995, theirTable 2): 5.4 and 14.3& for benthic diatoms in the ®eld,18.8& for worldwide phytoplankton (Peterson andHowarth 1987), and 6.5& for macroalgae in a mangrovecreek.

O�shore prawns

During the dry season, most d13C values for 15 to25 mm carapace length CL and ³35 mm CL Penaeusmerguiensis, P. esculentus, and P. semisulcatus caughto�shore ranged from only )17 to )14& (Fig. 6), whichis intermediate between macroalgae/seston and seagrassfrom the estuary (Fig. 6).

In the wet season, the d13C values for subadult andadult prawns o�shore, unlike those of juvenile prawns inthe estuary, tended to be higher than in the dry season.They were closer to (and in some cases were higher than)the d13C values of seagrass in the estuary than to anyother potential primary source of carbon (Fig. 6). Thetwo small Penaeus merguiensis with very low d13C valuesin the wet season ()23 and )21&: Fig. 6) were bothcaught in shallow trawls, within 20 km of the mouth ofthe Embley River estuary. The o�shore d13C values ofsmall P. merguiensis in this season were lower than thoseof most small P. esculentus and P. semisulcatus.

The d13C values of o�shore prawns were signi®cantlyhigher in the wet (mean = )14.4&) than the dry season(mean = )15.9&, F1,78 = 13.8, p < 0.001), and in

large ()14.6&) than in small prawns ()15.8&, F1,78= 12.1, p < 0.001). Tukey's HSD test showed that themean d13C value of Penaeus merguiensis ()15.5&) wassigni®cantly lower than the means for P. esculentus()14.5&) and P. semisulcatus ()15.0&).

The d15N values for o�shore prawns ranged from 5.2to 10.0& and did not show any marked trend withseason or size-class of prawn (Fig. 6). The d15N values oflarge Penaeus merguiensis were lower than those ofP. esculentus or P. semisulcatus in the dry season but notin the wet.

Contribution of mangroves and seagrassto prawn food webs

The estimated contribution of mangroves to prawn foodwebs from the mangrove/seagrass model was greater atthe mangrove than at the seagrass sites and greater atMn2 than Mn1. The model suggests that mangrove

Fig. 5 Stable carbon (d13C), nitrogen (d15N) and sulphur (d34S)isotope values for juvenile prawns and some of their potential primaryfood sources at start of wet season at mangrove and seagrass sites inEmbley River estuary, 1991 (For prawns, open symbols = prawnscaught at seagrass sites; black symbols = prawns caught at mangrovesites; Ceriops = C. tagal var. australia; Rhizopora = R. stylosa; otherabbreviations as in Fig. 3)

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carbon could constitute up to 64% of the assimilatedcarbon of prawns at Mn2 in both seasons for Penaeusmerguiensis, and up to 83% for Metapenaeus spp. in thewet season (Table 2). However, this assumes that sea-grass was the other source of remaining carbon.

Since the d13C and d15N values of the juvenile prawnsfollowed those of the seagrasses Halodule uninervis andHalophila ovalis more closely than those of Enhalusacoroides, means for the ®rst two species were calculatedfor the seagrass sites and used as the seagrass end pointin the mixing models. At the seagrass sites, the potentialcontribution of mangroves to the carbon in food webssupporting Penaeus esculentus, P. semisulcatus, andMetapenaeus spp., estimated from the mangrove/sea-grass mixing model was 0% in the dry season, and only20% in the wet season (Table 2). In the wet season,however, P. merguiensis could have obtained up to 50%of its carbon from a mangrove source at the seagrass

sites. Again, this assumes that the remaining carbon wasderived from seagrass.

O�shore, the contribution of mangroves to the car-bon assimilated by subadult and adult Penaeus mer-guiensis, P. esculentus and P. semisulcatus, estimatedfrom the mangrove/seagrass mixing model, could be atmost 30 to 36% in the dry season, and 0 to 34% in thewet season.

The potential contributions of mangroves estimatedfrom the mangrove/seston mixing model were muchlower than those from the mangrove/seagrass model

Table 2 Potential contribution(%) of mangroves and sea-grasses to carbon assimilated bypenaeid prawns in the EmbleyRiver estuary and o�shore re-gions in the dry and wet sea-sons. Values were calculatedusing simple mixing model andfractionation of 1& (CL car-apace length; ± no prawnscaught)

Habitat and species Mangrove/seagrass Mangrove/seston Seagrass/seston(% mangrove) (% mangrove) (% seagrass)

dry wet dry wet dry wet

Mangrove (Mn2)Penaeus merguiensis 64 64 26 24 0 0Penaeus semisulcatus 63 ± 23 ± 0 ±Metapenaeus spp. 62 83 22 65 0 0

Mangrove (Mn1)P. merguiensis 40 66 0 30 38 0P. semisulcatus 12 1 0 0 82 99Metapenaeus spp. 16 44 0 0 75 30

Seagrass (Sg1 and Sg2)P. merguiensis ± 50 ± 15 ± 0P. esculentus, P. semisulcatus,and Metapenaeus spp.

0 20 0 0 100 50

O�shore (15±25 mm CL)P. merguiensis ± 34 0 0 ± 35P. esculentus, P. semisulcatus 36 7 0 0 23 87

O�shore (�35 mm CL)P. merguiensis 30 4 0 0 34 100P. esculentus, P. semisulcatus 32 0 0 0 30 100

Fig. 6 Stable carbon (d13C) and nitrogen (d15N) isotope values forsubadult and adult prawns in Albatross Bay, o�shore from EmbleyRiver estuary, in dry and wet seasons of 1991/1992 [Symbols for prawnspecies as in Fig. 5; small symbols 15 to 25 mm carapace length (CL);large symbols �35 mm CL; dashed boxes 95% con®dence limits formajor primary sources in estuary; abbreviations for seagrass species asin Fig. 3]

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(Table 2). In the mangrove/seston model, mangrovesonly contributed to the assimilated carbon of prawns inthe following cases: in the dry season, only at Mn2('25% for Penaeus merguiensis, P. semisulcatus andMetapenaeus spp.); in the wet season for Metapenaeusspp. at Mn2 (65%) and P. merguiensis at all sites (15 to30%) (but not in the o�shore prawns).

The seagrass/seston model estimated that at the sea-grass sites, seagrass would contribute all of the carbonassimilated by prawns during the dry season and 50% ofthe carbon of Penaeus esculentus, P. semisulcatus andMetapenaeus spp. in the wet season, and none of thecarbon of P. merguiensis (Table 2). At the mangrovesites, seagrass could contribute major quantities of car-bon to prawns only atMn1, particularly in the dry season.O�shore, the potential contribution of seagrass carbon tolarge P. merguiensis and to small and large P. esculentusand P. semisulcatus was �30% in the dry season and�100% in the wet season (Table 2). In contrast, thecontribution of seagrass carbon to subadult P. mer-guiensis was only �35% in the wet season (Table 2).

Discussion

Importance of mangroves to estuarine food webs

The carbon-isotope signatures of juvenile prawns at mostsites in the Embley River estuary showed that the con-tribution of mangroves to the prawn food web was in-signi®cant. The only possible exception was in a small,mangrove-lined creek, but even there, mangrove carboncan only have made a signi®cant contribution if it is as-sumed that the other source is seagrass. This seems un-likely given the absence of seagrass from this site. Despitethe obvious presence of benthic organic matter derivedfrom mangrove/terrestrial sources in seagrass beds only200 m from the fringing mangrove forest, little was as-similated by juvenile prawns (cf. Figs. 3 and 4). This in-dicates that the contribution of mangrove carbon to thefood web of juvenile prawns is limited to an even smallerarea than suggested by previous stable-isotope studies oftropical mangrove systems (Stoner and Zimmerman1988; Primavera 1996). Benthic algae, phytoplankton orboth were thought to be larger contributors to the carbonassimilated by juvenile prawns than mangrove-derivedmaterial in both these cases. Benthic microalage have alsobeen suggested as amajor source of carbon assimilated byjuvenile prawns in tropical mangrove creeks in Malaysia(Newell et al. 1995). A recent stable-isotope study of ®shin a mangrove±seagrass ecosystem also found that man-groves made little contribution to the carbon assimilatedby ®shes, despite the movement of some species of ®shesbetween mangroves and seagrasses (Marguillier et al.1997).

Because of di�erences in the habitats where juvenileprawns are found (Staples et al. 1985), mangrove carbonis likely to be more important for Penaeus merguiensisthan the tiger prawns or species in the genus Meta-

penaeus. Although mangrove detritus can be a signi®-cant component of the gut contents in P. merguiensis(Chong and Sasekumar 1981; Robertson 1988), the ac-tivity of bacteria in guts of juvenile P. merguiensis isrelatively low (14%), which suggests that the probablesources of prawn protein are tissues of live prey ratherthan microorganisms from the detritus (Moriarty andBarclay 1981; Dall et al. 1990). The main dietary itemsof juvenile P. merguiensis include copepods, gastropods,and in some cases diatoms and algae (Chong andSasekumar 1981; Robertson 1988; Wassenberg and Hill1993). The e�ciency with which juvenile P. merguiensisassimilates mangrove material is also relatively low('13%, Newell et al. 1995). Our work, together with arecent stable-isotope study of Malaysian mangrovecreeks (Newell et al. 1995), con®rms that juvenileP. merguiensis are likely to obtain only a small propor-tion ('10%) of their nutrition from mangrove detritus,either directly or indirectly.

Although mangrove material appears to have hadlimited input to the food web of juvenile prawns in theestuary, mangroves are important habitats for the ju-venile stages of both prawns and ®shes. Banana prawnsare found only along mangrove-lined mudbanks, par-ticularly those in small creeks (Staples et al. 1985; Vanceet al. 1990), and the density of small ®shes is higher inmangrove creeks than other nearby habitats, includingseagrass (Robertson and Duke 1987). Mangrove mate-rial at the bottom of creeks can provide habitat for ju-venile prawns and increased densities of smallcrustaceans and polychaetes (Daniel and Robertson1990; Robertson and Blaber 1992). A high proportion ofthe fallen mangrove leaves can be consumed within theforest by sesarmid crabs, whose larvae reach high den-sities at certain times of the year. These larvae are im-portant prey for ®shes, and mangrove material cantherefore contribute to the food chain of ®shes throughthis pathway (Robertson and Blaber 1992).

Mangroves also provide some escape from predation,since the postlarvae and juveniles of banana prawnsmove into the forests as they are inundated on the ¯oodtide while large predatory ®shes are restricted tothe mangrove fringe (Vance et al. 1996). In addition, thestructure provided by mangroves is likely to decrease thee�ciency of some prawn predators (Robertson andBlaber 1992).

Importance of seagrass to estuarine food webs

In contrast to mangroves, seagrass could be a majorcontributor to the carbon of juvenile prawns in the estu-ary. However, we were not able to separate the contri-butions of living seagrass, their epiphytes and seagrassdetritus, to the carbon assimilated by juvenile prawns. Ingeneral, epiphytes are thought to more important to thefood web than their hosts (e.g. Thayer et al. 1978; Kittinget al. 1984). Epiphytes are often more palatable thanseagrasses, particularly those species containing noxious

297

sulfated phenolic compounds (Kitting et al. 1984; Bell andPollard 1989). In some cases, the greater importance ofalgae than seagrass to consumers has been supported bythe d13C values of the consumers (e.g. Fry 1984). How-ever, the seeds and starch bodies of seagrass are verynutritious, with similar energy contents for copepods andamphipods (O'Brien 1994). These components of seagrassform a signi®cant part of the diet of juvenile Penaeusesculentus in subtropical Moreton Bay, Australia, at cer-tain times of the year (Wassenberg 1990; O'Brien 1994).

The seasonal trends in the d13C and d15N values ofjuvenile prawns in seagrass followed more closely thoseof the small seagrasses (Halodule uninervis andHalophilaovalis) than those of the much larger Enhalus acoroides.These ®ndings suggest that if juvenile prawns are as-similating carbon from seagrass directly, Haloduleuninervis or Halophila ovalis are the most likely sources.The small H. ovalis is also the preferred seagrass ofdugongs and turtles, two important herbivores in trop-ical seagrass systems (Lanyon et al. 1989).

The fact that juvenile prawns have similar isotopevalues to seagrass does not necessarily imply that theyassimilate their carbon directly from seagrass. The d15Nvalues of consumers have been used to interpret theirposition in the food web, with a change of �3& indi-cating that the consumer belongs to another level in thefood chain (e.g. Peterson and Fry 1987). Because thed15N values of juvenile prawns were only slightly higher(in general <5&) than those of seagrass, only one, or atmost, two trophic levels are likely to separate the pri-mary sources and juvenile prawns. Studies of the diet ofsmall juvenile Penaeus esculentus and P. semisulcatushave shown that they feed mainly on copepods, ostra-cods, gastropods and diatoms (O'Brien 1994; Healeset al. 1996). Filamentous algae and seagrass can also bea signi®cant component of the gut contents of juvenileP. esculentus (O'Brien 1994). It is likely that both plantand animal material are important for the nutrition ofjuvenile prawns: e.g. juvenile P. aztecus and P. setiferusgrow faster on a mixed diet of diatoms (Skeletonemacostatum) and brine shrimp (Artemia sp.), than on eithersource alone (Gleason and Zimmerman 1984; McTigueand Zimmerman 1991).

Seasonal patterns in carbon dynamics in the estuary

Despite the potential outwelling of mangrove/terrestrialcarbon during the pronounced wet season, it's contri-bution to the food web increased only slightly at thistime. At the end of the dry season, there was relativelylittle variation in the d13C values of juvenile prawns inthe Embley River estuary, particularly in the seagrassbeds. This low variation in the d13C values of juvenileprawns within-sites, indicates that they had been resi-dent for some time and all had taken on the value of theprimary carbon source in the area.

In contrast, the d13C values of juvenile prawns inseagrass at the end of the wet season were lower and

much more variable than those in the dry season. Thisbroad range of values suggests that, in the wet season,individuals in the seagrass beds had di�erent feedinghistories i.e. some prawns may have only just becomeresident consumers in the seagrass. It should be notedthat juvenile prawns in the wet season belong to a dif-ferent cohort from those in the dry season. The low d13Cvalues for Penaeus merguiensis in seagrass in the wetseason, similar to those at mangrove sites, suggest thatvirtually all individuals of this species at the seagrasssites were recent emigrants from mangrove creeks. Thishypothesis is also supported by the fact that rainfallstimulates the emigration of P. merguiensis from man-grove creeks to nearshore marine environments (Staplesand Vance 1986), and that juvenile P. merguiensis arenot usually found in seagrass (Staples et al. 1985).

O�shore food webs

The d13C values for prawns in the waters o�shore fromthe Embley River estuary varied less, both within andbetween species, than those for juvenile prawns in theestuary. The d13C values for o�shore prawns were sub-stantially higher than those recorded for mangroveleaves and mangrove benthic organic matter in the es-tuary, and are similar to values reported for o�shoreprawns in the Torres Straits, northern Australia (Fryet al. 1983), Malaysia (Rodelli et al. 1984; Newell et al.1995), and the Gulf of Mexico (Fry 1983). O�shoreprawns in our study had higher, rather than lower d13Cvalues at the end of the wet season after mangrove/ter-restrial material had been exported from the estuary,which is contrary to what would be predicted if man-grove/terrestrial sources were important. In Malaysia,although sediments 5 km from the mangroves had d13Cvalues indicative of a mangrove/terrestrial origin, therewas little evidence that this source was utilised by theo�shore prawns (Rodelli et al. 1984; Newell et al. 1995).Similarly, in Florida and southern Brazil, there was littleevidence that mangrove/terrestrial sources of carbonenter the coastal food web directly (Fleming et al. 1990;Matsura and Wada 1994).

The higher d13C values of subadult and adult prawnsat the end of the wet season is consistent with seagrassdetritus becoming more important in the food chain ofo�shore prawns at this time. Seagrass detritus wasproposed as a likely major source of carbon for pelagic®sh larvae (blue grenadier) in Tasmania, southern Aus-tralia (Thresher et al. 1992). However, the d13C values ofo�shore prawns are also consistent with the primarysource being benthic microalgae (see Newell et al. 1995),which are thought to be an important source for marinefood webs (Fry and Wainwright 1991; Mallin et al.1992), or a mixture of seagrass and plankton.

The results from both the juvenile prawns in the es-tuary and, particularly, adult prawns o�shore, con®rmthat mangrove/terrestrial carbon makes a minor con-tribution to the food web supporting prawns in coastal

298

waters. Thus, although large amounts of mangrove andterrestrial carbon may be exported from the EmbleyRiver estuary, very little is assimilated by prawns inhabitats away from the mangrove creeks, either innearby seagrasses, or further away in o�shore areas (seealso Rothlisberg et al. 1994). Our study has emphasisedthe importance of seagrass beds as a major source ofenergy supporting the food web of prawns in estuaries,although further work is required to resolve the relativeimportance of seagrasses and their epiphytes.

Acknowledgements We thank R. Diocares for assistance with sta-ble-isotope analyses and M. Kempster, M. Grey, C. Marshall,M. Haywood and R. Kenyon for helping to collect samples in the®eld. P. Crocos and T. van der Velde provided samples of prawnsfrom the o�shore waters in Albatross Bay. T. Haystead analysedsamples for sulphur, and R. Connolly, N. Preston, G. Fenton, andJ. Primavera provided helpful comments on the manuscript.Rainfall data were provided by the Bureau of Meteorology, andsalinity and temperature data by D. Vance. This project was sup-ported by funds from the Fisheries Research and DevelopmentCorporation (FRDC 92/45), the CSIRO Division of Marine Re-search, and the Australian Research Council small-grant scheme atGri�th University.

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