Changes in Food Web Structure Under the Influence of Increased Anthropogenic Nitrogen Inputs to Estuaries

MARINE ECOLOGY PROGRESS SERIES I Vol. 168: 259-271,1998 1 Published July 9 Mar Ecol Prog Ser

Changes in food web structure under the influence of increased anthropogenic nitrogen inputs to estuaries

James W. McClelland*, I. Valiela

Boston University Marine Program, Marine Biological Laboratory. Woods Hole. Massachusetts 02543, USA

ABSTRACT: Anthropogenic nitrogen loads to shallow coastal waters have been linked to shifts from seagrass- to algae-dominated communities in many regions of the world, yet the influence that these shifts have on the structure of nearshore food webs remains unclear. We used stable C and N isotope ratios to assess the relative importance of phytoplankton, macroalgae, and eelgrass Zostera marina as food sources to consumers in estuaries of Waquoit Bay, Massachusetts, USA, that receive low versus high nitrogen loads from their surrounding watersheds. We found that, in general, the diets of herbivores, suspension feeders, and detritlvores (collectively referred to as primary consumers) in the Waquoit Bay estuaries are influenced by the dominant forms of production that they are exposed to. Phytoplankton and macroalgae are the major food sources of primary consumers under both low and high N loading conditions, but eelgrass is also an important food so'urce where N loading is low Most of the primary consumers at the estuary with low N loading have between 10 and 16 % eelgrass in their diets. Some species, however, appear to have no eelgrass in their diets, while others have diets consisting of as much as 31 % eelgrass. Eelgrass C and N are passed on to benthic as well as pelagic secondary consumers. With losses of eelgrass as a consequence of nitrogen loading, an important pathway through which land-derived nitrogen enters food webs in the Waquoit Bay estuaries is eliminated. This fundamental change probably affects the rate at which land-derived nitrogen is cycled within estuaries, as well as its ultimate fate.

KEYWORDS: Nitrogen loading . Estuanes . Food webs . Coastal watersheds . Urbanization

INTRODUCTION In some shallow temperate waters, eelgrass Zostera marina dominates production under oligotrophic condi- Anthropogenic nutrient loads from coastal water- tions, but is replaced by proliferations of phytoplankton sheds to nearshore waters are dramatically altering and macroalgae as eutrophication progresses. This shift aquatic habitats (GESAMP 1990, National Research occurs because eelgrass production is light-limited, Council 1994). In estuarine and coastal marine waters, whereas phytoplankton and macroalgal production are increased nitrogen loads stimulate eutrophication nutrient-limited (Duarte 1995). Increased nitrogen (Kelly & Levin 1986, Nixon 1986, Galloway et al. 1995). availability promotes algal growth, and as a result, eel- As a consequence, the assemblage of primary produc- grass is lost due to shading (Valiela et al. 1997a). A ers found in these waters often changes (Orth & Moore well-studied example of this phenomenon comes from 1983, Sand-Jensen & Borum 1991, Costa et al. 1992, the Waquoit Bay system on Cape Cod, Massachusetts, Duarte 1995, Short & Burdick 1996, Valiela et al. USA (Fig. 1). In the 1950s eelgrass grew throughout 1997a). Waquoit Bay and the estuaries adjoining it (Valiela et al. 1992). Over the past 40 yr, however, nitrogen loading has increased phytoplankton and macroalgal production, causing eelgrass production to decrease as a secondary effect (Valiela et al. 1997a).

0 Inter-Research 1998 Resale of fullarticle not permitted 260 marEcol Prog Ser 168: 259-271, 1998

studled recelve relatively low (Sage Lot Pond), high '/i\ \ I ;, I (Quashnet River), and higher (Childs Rlver) n~trogen L,' - I \ loads (Table 1) In Sage Lot Pond, eelgrass is an irnpor- tant source of production, but at Quashnet Rlver and /FL Chllds River, production is dominated by macroalgae /I r X (Table 1) By maklng comparisons among estuaries I I I I within the Waquoit Bay system, we galn a better I I h I I I understanding of changes that take place in estuanes I I I I l as u~ban~iationof coastal watersheds Increases Thls I I \ approach IS referred to as a space-for-time substttut~on I I \ I I \ * (Pickett 1991) Of course, many factors are not con- \ I I ' h trolled In a quasi-expenment such as thls, addlng some 1 3 \\ 4 l I uncertainty to data Interpretation Worklng at the scale I I I I of whole watersheds, however, reveals novel ~nforma- I I 11 , tion about ecosystem function that cannot be learned I I by worklny at smaller scales Hence, the added uncer- I \ talnty Inherent to lnterpretatlon of data from cross-sys- ten corr,peir:socs 1s oztwe:ghed by the scaic-spcc:fic 1) \ information gained w~ththis approach \ N I \ Although it IS clear that pnmary producer assemblages \ \ change in response to nutrient loadlng, the Influence of --P lkm - such changes on the strl~ctlireof ~st~~iirin~food WP~S 1s / / poorly understood If all producers were equally edtble I I " (and accessible), then consumers would s~mplyeat them I / 4". 0 'f In proportion to their productlon, and the diets of con- J I I ' Waquo~t / A<-- 1-h / /- sumers would change as the mix of producers changed I 1 Bay /' - 7 ',/ /' I -5. /.: - ZCP '/ In fact, however, d~fferencesin chemlcal composition I -- -< < L'---/ \ ,' ._- - - , and morphological charactenstics among producers make them differ In edibility (Cebnan & Duarte 1994) V~neyardSound For example, nutnent-poor structural tissues in eelgrass make it less desirable as a food source than phytoplank- Fig. 1 The Waquolt Bay xvatershed-estuary system, Cape ton and macroalgae. Edibility also varies wldely among Cod, Massachusetts, USA. Dashed lines separate the Waquo~t Bav watershed into catchment basins associated xvith dlffer- macroalgal species (NicOtn lg80, Heckscher et lgg6). ent estuanes surrounding Waquoit Bay Each catchment These differences in edtbility make it difficult to predict basln is named for the estuary that it empties into: 1 = T~mms how and to what extent nutrient-loading-lnduced Pond, 2 = Eel Pond, 3 = Childs River, 4 = Quashnet River, changes in producer assemblages in coastal 5 = Hamblin Pond, 6 = Jehu Pond, 7 = Sage Lot Pond waters affect food web structure.

The Waquo~tBay system consists of Table 1 Nitrogen loads to the Sage Lot Pond, Quashnet Rlver, and Childs Rlver estuanes of Waquoit Bay, and percentages of primary product~oncontnbuted 7 shallow estuaries (maximum depth by phytoplankton, macroalgae, and eelgrass wlthin these estuaries N-load~np of 3 m, and average depth of 1 m at and percentage primary product~onestimates are based on Waquoit Bdy Land mean low water) that receive fresh- b4argin Ecosystems Research (WBLMER) measurements (D'Avanzo et a1 1996, water inputs from separate catchment Peck01 & Rlvers 1996, WBLMER unpubl data) basins within the Waquoit Bay watershed (Fig. 1). Freshwater enters the Estuary estuaries almost exclusively via Sage Lot Pond Quashnet River Childs R~ver groundwater flow, and with it land- 1Nitrogen load (kg N ha.' yr-l) 64 520 624 1 derived nitrogen is conveyed to the % of pnmary production by. estuaries (Val.iela et al. 1992). The Phytoplankton 26 nitrogen loads delivered to each estu- Macroalgae ary differ according to land use on the Cladophora vayabunda 19 surrounding watershed (Valiela et al. Gracrlana t~kvahiae 19 Eelgrass 3997b). The 3 estuanes of Waquoit Zostera marina 3 7 Bay that have been most extensively McClelland & Valiela: Chalnges in food web structure 26 1

An effective means to elucidate food web structure is In this paper, we use stable C and N isotope ratios to examine the stable carbon and nitrogen isotope together to investigate how changes in primary pro- ratios (expressed as 613C and 6I5N) of producers and ducer assemblages brought about by increased waste- consumers within a community (for reviews see Fry & water N loads influence the diets of consumers in Sherr 1984, Peterson & Fry 1987, and Lajtha & Mich- Waquoit Bay. In particular, we assess the relative ener 1994). This is because different producers often importance of phytoplankton, macroalgae, and eel- have unique stable isotope ratios that make them iden- grass as food sources to the consumers. We focus our tifiable in mixes of particulate organic matter (Haines work on the Sage Lot Pond, Quashnet River, and 1977, Gearing 1988, Canuel et al. 1995) and in the tis- Childs River estuaries, addressing 3 main questions: sues of consumers (Zieman et al. 1984, Peterson et al. (1) What are major primary producers contributing to 1985, Fry 1991). particulate organic matter (POM) in each estuary? Use of 613C and F15N in food web studies relies on (2) What are the major food sources of consumers in the assumption that the isotopic composition of a con- estuaries with low versus high N loads? (3) How do sumer (or mixture of particulate organic matter) is pathways of C and N flow through estuarine food webs equal to the weighted average of the isotopic compo- change as eutrophication intensifies? sitions of its food sources (Gannes et al. 1997). For example, if an amphipod eats 2 food sources in equal proportions, it is expected to have a 613C value METHODS (whole body) that is intermediate to those of the 2 food sources. Where there are multiple food sources, Sample collection. Biota and POM in Sage Lot Pond, plots of 6I3C versus 615N provide a 2-dimensional Quashnet River, and Childs River were sampled for view of the diets of consumers. As carbon and nitro- stable isotope analysis in November 1993, July 1994, gen from producers are passed from one troph~clevel May 1995, July 1995, and June 1996. These dates were to the next, their 6I3C and F15N values tend to chosen to cover spring, summer, and fall conditions increase due to differential use of heavy and light iso- within the estuaries, and to allow an interannual com- topes during metabolism (Fry & Sherr 1984, Peterson parison within the summer season. Samples were not & Fry 1987, Lajtha & Michener 1994). There is also a collected during winter months because of low animal ---fiw;n-3." day 5&y of ex.ri.l,ence the! steb!e isotope rltics sbur?d.-nce. Samples were col!ected from regions can change during decomposition (Benner et al. 1987, within each estuary characterized by a vertically Currin et al. 1995). These factors must be considered mixed water column with salinity between 25 and in order to clearly interpret stable isotope data in food 30 PSU. Producers (except phytoplankton, see below) web studies. and POM were sampled from all 3 estuaries, and con- Previously published nitrogen stable isotope data sumers were sampled from Sage Lot Pond and Childs from the Waquoit Bay system (McClelland et al. 1997) River. shows that differences in 615N values of biota among We could not use suspended POM as a proxy for the estuaries of Waquoit Bay are strongly correlated phytoplankton isotope values-as is often done in with differences in nitrogen loading from wastewater. open ocean .waters-because suspended POM in the As the percentage of wastewater contributing to total estuaries of Waquoit Bay has a large non-phytoplank- N loading increases among estuaries, the 6'" values ton (mainly detritus and amorphous organic aggre- of estuarine biota increase. A second paper (McClel- gates) conlponent. However, dense populations of land & Valiela in press) defines the relationship phytoplankton with minimal detrital and aggregate between wastewater inputs to watersheds and the 6I5N particles were available from the 'controls' of an ongo- of dissolved inorganic nitrogen (DIN) in groundwater, ing experiment on nutrient limitation of phytoplankton and explicitly links groundwater 615N with producer in Childs River (Tomasky & Valiela 1995). We mea- 6I5N in the different estuaries of Waquoit Bay. The 615N sured the C and N stable isotope values of these 'con- values of groundwater nitrate within the Waquoit Bay trols'. Samples were collected for isotope analysis after watershed increase from -0.9 to +14% as wastetvater a July 1996 run of the experiment. Based on the fact contributions increase from 4 % to 86% of the total that the 613C values of other primary producers within nitrogen pool. As a result, the average 615N of DIN the Waquoit Bay system differed little among estuaries (nitrate + ammonium) received by different estuaries (data presented in this paper), we estimated the of around Waquoit Bay increases from +0.5%0to +9.5%o. phytoplankton in Quashnet River and Sage Lot Pond to This Increase is paralleled by the FI5N of eelgrass, be the same as phytoplankton in Childs River. Simi- while macroalgae, salt-marsh cordgrass, and sus- larly, based on consistent differences in macroalgae pended particulate organic matter increase to a lesser 615N among estuaries (McClelland et al. 1997, McClel- degree among estuaries. land & Valiela in press, and data presented in this 262 Mar Ecol ProgSer 168:259-271, 1998

paper) we estimated the 615N of phytoplankton in The standard used for stable nitrogen isotope analysis Quashnet River by subtracting l from the Childs was N, in air, and the standard used for stable carbon River value, and we estimated the 615N of phytoplank- isotope analysis was Vienna Peedee belemnite. 613C ton at Sage Lot Pond by subtracting 2% from the and 615N values, expressed as %, were calculated as Childs River value. [(Rs,,ple/R,t,,d,,d)-l] X 103, with R equal to 15N/14N or Other producers and consumers were sampled as I3C/l2C. Precision of replicate analyses was *0.2% for follows: Suspended POM was sampled by collecting 2 1 nitrogen and +0.3X for carbon. bottles of sea water from a depth of 0.5 m below the surface at 3 locations within each estuary. Benthic POM was sampled by collecting bare sediment (ben- RESULTS AND DISCUSSION thic microbial and microalgal mats are not a prominent feature in the estuaries of Waquoit Bay) to a depth of In the sections below, we first examine the stable 1 cm at 10 locations within each estuary. Sediment carbon and nitrogen isotope values of primary produc- type in all 3 estuaries is a mixture of sand, silt, and clay. ers in Sage Lot Pond, Quashnet River, and Childs Benthic macrophytes were sampled from 15 locations River. We then discuss the relationship between iso- within each estuary. Benthic invertebrates were sam- tope values of POM, and isotope values of dominant pled with an Ekman dredge from 15 locations within producers in each estuary. Finally, we use stable car- Sage Lot Pond and Childs River Dredge contents were bon and nitrogen isotope values to compare the food, rinsed through a 1 mm sieve and invertebrate species webs in Sage Lot Pond and Childs River, and discuss retained on the sieve were sorted by species. Fish were changes in the flow of land-derived nitrogen into food col.lected from Sage Lot Pond and Childs River by webs as eutrophication intensifies. Although we focus seine. our analysis on the producers that contribute most to Sample preparation. To prepare samples for stable production within the estuaries of Waquoit Bay isotope analysis, phytoplankton and suspended POM (Table l),we acknowledge that a variety of less promi- were filtered from water samples onto precombusted nent producers must also contribute to POM and to the (490°C) Gelman A/E glass fiber filters with a low pres- diets of consumers. sure vacuum pump, macrophytes were gently cleaned of epiphytic material, and animals were held in filtered sea water for 24 h to allow their guts to clear. Both Stable isotope values of primary producers macrophytes and animals were then rinsed with deion- ized water, and all samples were dried at 60°C. When The 613C values of primary producers (except for the dry, samples were ground (filters with POM were kept macroalga Gracilaria tikvahiae, see below) change whole) into a homogenous powder, and combined to little among estuaries, while the 6"'N values of pri- make single composite samples of each species per mary producers consistently differ among estuaries estuary per sampling date. Whole organisms were (Table 2). The similarity of producer 613C is reasonable used in all cases except for Mya arenaria and Geuken- because the 613C of dissolved inorganic carbon (DIC) sia demissa, the shells of which were removed. Sepa- largely depends on salinity (Fogel et al. 1992), and pro- rate composites consisting of 15 to 250 individuals ducers were sampled from waters of the same salinity (depending on the size of the species collected) were range at all estuaries. As discussed in the introduction, prepared for stable isotope analysis from each estuary differences in 615N values of producers among estuar- for each season. Samples for stable carbon isotope ies are linked to differences in N loading from waste- analysis were acidified to remove inorganic carbon, water (McClelland et al. 1997, McClelland & Valiela in then dried and ground a second time. press). Both 615N and 6I3C of producers change little Stable isotope analysis. Samples were analyzed in among seasons (Table 2), suggesting that the isotope the Boston University Stable Isotope Laboratory using values of DIN and DIC, and the fractionation associ- a Finnigan Delta-S isotope ratio mass spectrometer. All ated with their use, do not vary much throughout the samples (except filters, see below) were weighed and year within the Waqu.oit Bay system. loaded into tin capsules and combusted in a Heraeus Unlike the other producers, the 6'" of Gracilaria element analyzer. The resulting combustion gases tikvahiae in Sage Lot Pond is substantially lower were cryogen.ically separated and purified in a Finni- than at the other 2 estuaries (Table 2).The reason for gan CT-CN trapping box before introduction into the this anomaly is unclear. Perhaps increased nitrogen mass spectrometer. Filters were acidified with PtC12, availability in Childs River and Quashnet River dried, then combusted using the Dumas combustion allows G. tikvahiae to incorporate carbon m.ore effi- technique. Combustion gases were again separated ciently than in Sage Lot Pond, so that fractionation of and purified before analysis (Lajtha & Michener 1994). DIC during uptake by this species becomes sma.ller McClelland P1Valiela: Changes in food web structure 263

Table 2. Primary producer and POM isotope values ("L) of composite samples collected spring, summer, and fall between 1993 and 1996 from Sage Lot Pond. Quashnet River, and Childs River (average t 3 SE). Values in parentheses are number of seasons sampled. Values in italics are estimates of phytoplankton isotope values based on measured values at Childs River

Sage Lot Pond Quashnet River Childs River 6I3c 615~ 6' '(1 6I5N 613C 6%

POM (Suspended) -18.4 * 1.4 (5) 3.7+ 0.3 (S) POM (Benthic) -15.2 t 0.5 (2) 2.4 + 0.3 (2) Pnrnary producers Phytoplankton -21.1 5.1 Macroalgae Cladophora vagabunda -15.3 * 0.3 (4) 3.4 * 0 1 (4) Cracilana tikvahiae -19.5 * 0.6 (4) 5.1 t 0 6 (4) Enteromorpha sp. -19.1 * 2.1 (2) 4.9 * 0.3 (2) Eelgrass Zostera marina -7.1 +0.5 (4) 0.2 +0.6 (4)

under higher N loading conditions (B. Peterson pers. assumption that 20% of net aerial production (total comm.). organic carbon) by S. alterniflora typically makes it Although the stable isotope values of phytoplankton into the open waters of salt-marsh estuaiies (Taylor & in Waquoit Bay were determined from populations Allanson 1995). In fact, however, the hydrology and grown up under artificial conditions (see 'Methods'), geomorphology of the Waquoit Bay system are such the values are typical of those measured for marine that inputs from S. alterniflora may even be smaller. phytoplankton in many locations around the world The low tidal amplitude in Waquoit Bay is conducive to (Gearing 1988). In fact, our estimate of phytoplankton salt-marsh banks that drop off vertically from the 613C in Waquoit Bay (-21.1%0) is almost identical to the marsh surface into the water. As a consequence, creek sversge FI3C va!ue of phytop!ankton (-21.3 * !.l":.-) ir! ba~kswith the tal! form of S. a!terr?iflor8 (that get nearby Narragansett Bay, Rhode Island (Gearing et al. flooded twice daily) are almost non-existent. The sur- 1984). Rased on this similarity, we conclude that any face of the marsh is only flooded infrequently, and thus non-phytoplankton particles in our 'phytoplankton' remains uncoupled from the estuary much of the time. samples did not measurably influence the isotope val- This situation is consistent with the finding of Deegan ues of these samples. & Garritt (1997) that salt-marsh production does not contribute significantly to subtidal food webs in estuaries with low tidal amplitudes. Composition of POM

The 613C values of POM fall between those of phytoplankton and macroalgae at all of the Waquoit Bay estuaries (Fig. 2), indicating that these 2 producer Phyto...... ----.-...---., Macroalgae types are the dominant contributors to POM throughout the system. It is apparent from the higher 6'" val- : SL- ues of POM in Sage Lot Pond compared to the other 2 estuaries (Fig. 2), however, that eelgrass makes an important contribution to POM in Sage Lot Pond in addition to phytoplankton and macroalgae. Salt-marsh cordgrass Spartina alterniflora is more abundant at Sage Lot Pond that at the other 2 estuaries. It is therefore possible that inputs from S. alterniflora (6I3c = -12.5%) contribute to the higher 6'" values of POM In Sage Lot Pond (Fig. 2). We estimate the influence of S. alterniflora to be small, however, Fig. 2. 6I3C values of suspended (0) and benthic (m)POM in Sage Lot Pond (SL), Quashnet River (QR),and Chllds River because the proportion of primary production in Sage (CR) compared to those of phytoplankton (Phyto.), macroal- Lot Pond coming from S. alterniflora is only about 10% gae, and eelgrass in Waquoit Bay. Dashed lines indicate the (WBLMER unpubl. data). This estimate is based on the ranges of SI3C values for each producer type 264 Mar Ecol Prog Ser 168: 259-271, 1998

Table 3 Percentage of POM and pnmary conwmer d~etsconsisting of eel- eelgrass 6I3C and the 8°C of POM at grass Zostera manna w~thlnthe Sage Lot Pond estuar) (average 2 1 SD) chllds River represents a 100% loss of eel- Estimates are calculated from the difference In 6°C of consumers (and grass Thus, the slope term In the above POM) llving In Ch~ldsRtver and Sage Lot Pond Sp spring, Su summer, F. ~AII equatlon is 100 divided by the difference between eelgrass &':'C and the 6I3C of POM at Childs River There is no y-intercept Seasons In average Percent eelyrass I term because the 6I3C values of POM at Suspended POM F., Su., Su,Sp Sage Lot Pond and Childs River are Benth~cP0k1 Su.Su expected to be the same if POM at Sage Lot Suspens~onfeeders Pond contains no eelgrass. Geukens~adem~ssa SP. ,klya arenarla Su. Su Our estimates of the percentage of eel- Depos~t/detntusfeeders grass ln POM (Table 3) are probably con- Sclerodactyla bnareus F , SLI.,SLI , Sp. servative, because the larger contributlon Palaemonetes vulgans Su. to production by Cladophora vagabunda Le~toscoloplosfraglhs Su. in Childs River compared to Sage Lot Leptosynapta sp S u Herbivores Pond (Table 1) counters the decrease in Cypnnodon vanegatus F. Su., Su 6I3C of POM caused by a loss of eelgrass. Cvmadusa compta Su., Su. Nonetheless, our ~stimirt~sfor Sage 1.0t Gdlnfnarus rnucrona tub Su. Pond are quite similar to estimates by Er~chsonellafLOform~s Su., Sp. fvl~crodeutopusgrj/llotalpa Su.,SLI. Thayer et al. (1978) for benthic (29%) and suspended (18%) POM in the Newport River Estuarv, North Carolina (also based on 6I3C). The consistently lower 6'" values of suspended Contributions by eelgrass (8'" = --7%0)to POM in POM compared to benthlc POM at all 3 estuaries Sage Lot Pond appear to change seasonally (Fig. 3, top (Fig. 2) indicate that suspended POM contains a larger panel). The &':'C of suspended POM is highest dunng proportion of phytoplankton than does benthic POM. summer months, when eelgrass biomass peaks within This is not surprising, given that phytoplankton pro- the estuary, and lowest in the fall and spring, when duction takes place in the water column. What is more eelgrass biomass is relatively low. In the other 2 estu- interesting, however, is that suspended POM at all of aries, where eelgrass is virtually absent, 613C values of the estuaries contains organic matter from benthic pro- POM change little among seasons (Table 2). Using ducers. Benthic macrophytes may be contributing to Eq. (l), we find that contributions of eelgrass to sus- suspended POM (1) as sloughed particles, (2) as resus- pended POM are undetectable during fall and spring, pended detritus from the sediments or (3) as organic but that in summer (when eelgrass biomass peaks in aggregates formed by bacteria in association with Sage Lot Pond), suspended POM consists of approxi- macrophyte-derived dissolved organic matter (Alber & mately 34 % eelgrass (Table 4). The timing of the rela- Valiela 1994). In any case, the 6°C data for POM 1.n the tionship between eelgrass biomass and suspended Waquoit Bay estuanes highlights the importance of POM in Sage Lot Pond suggests that release of eel- benthic-pelaglc coupling in shallow estuaries. grass-derived organic matter into the water column is Based on the decrease in 613C between Sage Lot closely coupled to active growth of eelgrass. Formation Pond and Childs River (Fig. 21, we estimate that (as an of organic aggregates from DOM released by eelgrass annual average) benthic POM is 23% eelgrass and (Alber & Valiela 1994) is probably an important mech- suspended POM IS 17% eelgrass in Sage Lot Pond anism behind this coupling. (Table 3).These percentages were calculated from the As with 6I3C, differences in the 6"N values of POM equation among estuanes are consistent with differences in eelgrass contributions; the 615N values of POM are lower % eelgrass = at Sage Lot Pond than at the other 2 estuaries (Table 2). Differences in the 6''N values of pnmary producers among estuaries (as a result of dlfferences in waste- where CR and SL represent Childs River and Sage Lot water inputs), however, make it difficult to quantify the Pond respectively, and POM is either benthic or sus- relationship between eelgrass contributions and POM pended particulate organic matter This equation 6I5N At most, we deduce from the different responses expresses a simple linear relationship between % eel- of 6'"C and 615N In POM to seasonal contributions of grass and the decrease in 6I3C of POM between Sage eelgrass (Fig. 3) that nitrogen from eelgrass makes a Lot Pond and Childs River. The difference between smaller contribution to POM than does carbon from McClelland & Valiela. Changes in food web structure 265

SAGE LOT POND +15 Jul 94

QUASHNET RIVER

15 Apr 96

",1'1'1'1'1

Z m

I"""""'"

-.__ -----4' CHILDS RIVER 6 Phyt. ------S-___ .. m '".C 0 Z m 4 I'-'OM B.POM C v.

Eelgrass b~ornass(g dry wt. m -2)

Fig. 3. Biomass of eelgrass Zostera marina versus 613C (top) Fig 4 6I3C versus &'"h of POM (0) compared to 6IJC versus and 615N (bottom) of suspended POM at various times of year FI5N of the dominant pnmary producers (0) at Sage Lot Pond, in Sage Lot Pond Estimates of eelgrass biomass are from Quashnet Rlver, and Childs Rlver Phyt = phytoplankton, G t monthly samples (n = 10) collected with an Ekman dredge. = Gracjlar~atrkvahlae, C v = Cladophora vagabunda, Z m = Eelgrass blades were removed from rhizomes, cleaned of epi- Zostera manna, S-POM = suspended POM, B-POM = benthlc phytic material, rinsed wlth fresh water, dried at 60°C, and POM Dashed llnes connect the donlinant producers with~n weighed. Averages i 1 SD were then calculated for each each estuary (Table l) Areas enclosed by the dashed lines month lndicate where points for POM are expected to fall when POM conslsts of a mix of the dominant producers eelgrass. This is reasonable, giwn the higher C:N of Hanson 1984) may also uncouple the 615N signal from eelgrass compared to phytoplankton and macroalgae the 613C signal of eelgrass. Zieman et al. (1984),how- (Duarte 1992). immobilization of inorganic nitrogen by ever, found that the 615N values of 2 seagrass species in heterotrophic bacteria associated with detritus (Rice & Florida did not change during early decomposition. In dual isotope plots (613C VS 615N), points for POM consistentlv fall below the area Table 4 Seasonal comparison of the percentage of eelgrass Zostera where they are pred;cted to fall based on a manna contributing to suspended POM and to the diets of sea cucum- be~sSclerodactyla brjareus, sheeps head minnow Cypnnodon van- the dominant producers In each estu- egatus, and isopods Er~chsonellahllformls at Sage Lot Pond Averages i ary (Fig 4) This suggests that the 615N of 1 SE are reported where samples were collected durlng more than producers decrease by a small but consistent one season amount during decomposition. Currin et al. (1995) found that the 6I5N of standing dead Season Percentage eelgrass contributing to: cordgrass decreased by about 2.4%0 over a Susp POM S briareus C. vanegatus E. filiformis 10 mo period. The extent to which stable iso- -- - tope values of algae change during decom- 30 + 8 Summer 34 + 7 25 r 6 39 + 5 position have received less study. Based on our data from Childs River (where over 80% 266 Mar Ecol Prog Ser 168: 259-271, 1998

Table 5. Consumer isotope values (%D)of composite samples collected in spring, summer, and fall between 1993 and 1996 from Sage Lot Pond, and Childs River (average * 1 SE). Values in parentheses are number of seasons sampled. B: bivdlv~;P: polychaete; C: crustacean; H: holothurian; F: fish

Sage Lot Pond Childs River Si3C 6I5N 6I3c 6I5N

Primary consumers Suspension feeders Geukensia demissa, B -19.0 (l) 7.3 (1) -18.5 (l) 9.1 (1) Mya arenaria, B -16.0 * 0 5 (2) 5.3 k 0.4 (2) -17.1 t 0 2 (2) 7.9 + 0.0 (2) DeposiUdetritus feeders Cirratulus grandis, P -14.7 + 0.2 (2) 5.1 r 0.3 (2) - Leitoscoloplos fragilis, P -13.5 + 0.3 (2) 4.5 i 0.6 (2) -14.4 (l] 7.5 (1) Palaemonetes vulgaris, C -12.6 (l) 5.8 (1) -13.6 (l] 8.8 (1) Leptosynapta sp., H -13.4 (l) 6.1 (1) -14.7 (l) 9.4 (1) Sclerodactyla briareus, H -13.4 + 0.2 (4) 6.7 r 0.1 (4) -16.0 * 0 2 (4) 10.3 + 0.4 (4) Herbivores Cyprinodon variegatus, F - 11.5 T 0.9 (3) 5.2 * 0.5 (3) -14.0 + 0.5 (3) 9.8 + 0.3 (3) Cymadusa cornpta, C -14.4 + 0.3 (2) 4.1 2 0.2 (2) -16.0 + 0.4 (2) 7.6 + 0.2 (2) Gammarus mucronatus. C -14.2 (l) 5.1 (1) -14.8 + 0.4 (2) 7.8 * 0.3 (2) Erichsonella filiformis, C -13.6 + 1.8 (2) 4.3r 1.0(2) -14.5 + 0.6 (2) 7.7 + 0.8 (2) Microdeutopus gryllotalpa. C -13.4 + 0.1 (2) 3.8 r 0.1 (2) -14.8 * 0.4 (2) 6.6 + 0.1 (2) Secondary consumers Menidia menjdia, F -16.5 * 0.5 (4) 9.8 * 0.4 (4) -17.7 + 0 8 (4) 11.6+0.3 (4) Gasterosteus aculeatus. F -16.9 (1) 9.0 (1) -15.4 * 0.4 (3) 12.3 * 0.4 (31 Fundulus heteroclitus, F -14 * 0.4 (3) 8.3 * 0.2 (3) -14.6 + 0.5 (3) 11.3 + 0.3 (3) Pseudopleuronectes americanus, f. - -13.1 (1) 10.7 (1) Podarke obscura, P -12.7 + 0.2 (4) 7.1 r 0.1 (4) -14.9 * 0.2 (4) 10.7 + 0.3 (4)

of production comes from phytoplankton and Clado- tracted from 6I3C, and 3.0%0was subtracted from 6I5N. phora vagabunda; Table l), it appears that decomposi- These values reflect an average fractionation effect of tion has decreased the F1'N of algae by about 1%0.This a trophic step based on a broad range of consumer decrease in 815N may be due to uptake of inorganic types (Peterson & Fry 1987, Michener & Schell 1994). nitrogen by bacteria associated with detritus (Rice Primary consumers. The positions of primary con- 1982). Rice & Hanson (1984) demonstrated that bacte- sumers compared to those of producers in 613C versus rially mediated N accumulation in cordgrass detritus 6I5N plots for Sage Lot Pond (Fig. 5) and Childs River was greater than N accumulation in macroalgal (Fig. 6) indicate that the dominant producers found in (Gracilaria foliifera) detritus. This would explain the each estuary are important food sources. Primary con- larger difference in 615N between llve and decom- sumers in Sage Lot Pond (Fig. 5) eat phytoplankton, posed cordgrass observed by Currin et al. (1995) than macroalgae, and eelgrass, whereas primary consumers between live and decomposed algae observed in this in Childs River (Fig. 6) subsist on phytoplankton and study (Fig. 4). macroalgae alone. The presence of eelgrass in the diets of primary consumers in Sage Lot Pond is confirmed by shifts in 6I3c Food sources of consumers values of primary consumers between Sage Lot Pond and Childs River (Fig. 7). Shifts in the 615N values of Before comparing the stable isotope values of con- consumers between Sage Lot Pond and Childs River sumers with those of potential food sources within the (Table 5) also reflect differences in eelgrass abundance Waquoit Bay estuaries, we corrected for fractionation between estuaries, but these shifts are confounded by tha.t occurs as organic matter passes from one trophic shifts in producer 6I5N (Table 2) as a result of differ- level to the next. This was done by subtracting litera- ences in N loading from wastewater (McClelland et al. ture values for trophic fractionation from the measured 1997, McClelland & Valiela in press). We therefore isotope values of consumers presented in Table 5. focus on shifts in 6I3C between Sage Lot Pond and 1.0% was subtracted from the 613C and 615N values of Childs River to estimate the proportions of primary amphipods (and one isopod) to account for the troph~c consumer diets derived from eelgrass in Sage Lot fractionatlon measu.red by Macko et al. (1982) for these Pond. We use Eq. (l),but substitute 'consumers' for consumers. For all other consumers, 1.0% was sub- 'POM' and '(6I3Ce1g,,, + 1)' for '613CEe,,,,, '. We add 1 to McClelland & Valiela: Changes in food web structure 267

SAGE LOT POND CHILDSRIVER I

tS-POM C v. +B-POM S2.

Fig. 5. 6'" versus 6'" of primary consumers (with adjust- Fig. 6. SI3C versus 615N of primary consumers (with adjust- ment for trophic fractionation, see below) compared to 6I3C ment for trophic fractionation, see below) compared to 6l3C versus SI5N of POM and the dominant producers in Sage Lot versus ST5Nof POM and the dominant producers in Childs ?@.'d. Suspension feeders. S1 = Getlkprlia TI~mic~a,S2 = Mya R~ver.Suspension feeders: S1 = Geukensia demissa. S2 = Mya arenaria. Herbivores: H1 = Cypnnodon variegatus, H2 = arenaria. Herbivores: H1 = 'Cyprinodon variegatus, H2 = Cymadusa compta, H3 = Gammarus mucronatus, H4 = Erich- Cymadusa compta, H3 = Gammarus mucronatus, H4 = Erlch- sonella filiformis, H5 = Microdeutopus gryllotalpa. Deposit/ sonella filiformis, H5 = Microdeutopus gryllotalpa. Deposit/ detritus feeder: D1 = Cirratulus grandis, D2 = Leitoscoloplos detntus feeder: D2 = Leitoscoloplos fragilis, D3 = Palae~non- fragilis, D3 = Palaemonetes vulgaris. D4 = Leptosynapta sp., etes vulgaris, D4 = Leptosynapta sp., D5 = Sclerodactyla D5 = Sclerodactyla briareus. Phyt. = phytoplankton, G. t. = briareus. Phyt. = phytoplankton, C. t. = Gracilaria tikvahiae, Gracilaria tikvahiae, C. v. = Cladophora vagabunda, Z. m. = C. v = Cladophora vagabunda, 2. m. = Zostera marina, Zostera mal-jna, S-POM = suspended POM, B-POM = benthic S-POM = suspended POM, B-POM = benthic POM. Dashed POM. Dashed llnes encompass the areas where polnts for pri- lines encompass the areas where points for primary con- mary consumers are expected to fall when their diets consist sumers are expected to fall when thelr dlets consist of a mix of of a mix of the dominant producers in Sage Lot Pond. 1 has the dominant producers in Childs River. To correct for trophic been subtracted from the stable C and N isotope values of fractionation, 1% was subtracted from the stable C and N iso- small crustacean grazers to correct for trophlc fractionation. tope values of small crustacean grazers. l'?;;* and 3%. were 1 %" and 3%0have been subtracted from the S1'C and 6"N val- subtracted from the Fl3C and 6l5N values respectively of all ues respectively of all other consumers other primary consumers

the 6I3C value of eelgrass to account for trophic frac- mussel Geukensia demissa has no detectable eelgrass tionation. in its diet (Table 3). Sage Lot Pond: Using Eq. (l), we estimate that eel- The difference in diet between the ribbed mussel grass makes a relatively small contribution to the diets and the soft-shell clam in Sage Lot Pond (Table 3), of most consumers in Sage Lot Pond (typically less than even though they are both suspension feeders, is likely 16 %), and yet its presence in the food web of Sage Lot a result of the different locations within the estuary Pond is pervasive (Table 3).Furthermore, it is apparent where each species lives. Ribbed mussels in Sage Lot that eelgrass is more important in the diets of some Pond live embedded in the salt-marsh bank at the consumers than others; the sea cucumber Sclero- estuary's edge, just below the marsh surface. In this dactyla briareus and the sheepshead minnow Cypnn- location, they can only feed near high tide, and thus odon variegatus stand out as having particularly large have diets dominated by phytoplankton (Fig. 5). On proportions of eelgrass in their diets, while the ribbed the other hand, soft shell clams in Sage Lot Pond live 268 Mar Ecol Prog Ser 1

Phyto...... ~.~...... Macroalgae Eelgrass..... dition, S bnareus inay consume eelgrass detntus that , ,. spans several (even many) seasons from day to day m : a: 0 D5 j I SA ; , . Our findlng that eelgrass makes an important contri- m m :+H j; 3 : , * bution to the food web in Sage Lot Pond is conslstent -m I +:U H2 j m : wlth other stable isotope studies of eelgrass communi- C : 0 H5 i : m : * , . 0 D4 : ties In North Carolina (Thayer et a1 1978) and Alaska Z :. , . - ; (McConnaughey & McRoy 1979), suggesting that use 2 i a+; S2 :, . of eelgrass by consumers IS a : .O D3 common Stephenson et a1 - . .; Sm : . . : .G D2 : ; (1986),in contrast, found that eelgrass does not make a m, , , 1 c. - V H4 j j s~gnif~cantcontribution to consumers In an eelgrass V) : mJ , , m. -0 H3 j j commun~tyin Nova Scot~a,Canada Where eelgrass is . , ti IS c : : 0. S1 j j an important food source it probably consumed , , , , more as detntus than as live mater~al(Thayer et a1 , , 1975, Zieman 1975) Live eelgrass IS less nutritious -22 -20 -18 -16 -14 -12 -10 -8 -6 than algae, but microbially mediated processes during decomposit~on make it (with assoclated bacteria) a more favorable food source with time (Tenore et a1 Fig 7 6I3C values of pnmarv consumers ilvlthout ad~ustm~nt 1982) for troph~cfractionatlon) at Sage Lot Pond (0) and Childs Childs River:In Ch~ldsRiver, where eelgrass IS vlr- Rtver (a) compared to those of phytoplankton (Phyto ) tually absent, the stable isotope data show that herbi- macroalgae, and eelgrass in Waquoit Bay Dashed hnes indicate the ranges of 6I3C values for each producer type Sus- vores and detntus/deposit feeders eat a mix of Gracl- penslon feeders S1 = Geukensla dernissa S2 = Mvaarenarla lana hkvahlae and Cladophora vaqabunda (Fiq 6) Herbivores H1 = Cypnnodon vanegatus H2 = Cymadusa Four herbivores (Cymadusa compta, Gammarus mu- compta, H3 = Garnmarus rnucronatus,H4 = Er~chsonellaf111- cronatus, Enchsonella filiform~sand Cyprlnodon var- forms, H5 = ~V~crodeutopusgryllotalpa Deposit/detntus iegatus) fall Intermediate between G t~kvah~aeand C feeder D2 = Le~toscoloplosfrag~l~s, D3 = Palaemonetes vul- vagabunda In Fig 6, indicating that they eat similar gans, D4 = Leptosynapta sp , D5 - Sclerodactyla bnareus Prl- mary consumers are ordered from the bottom to the top of the quantities of the 2 macroalgal species The herb~vore flgure according to increasing d~fferencein S13C between M~crodeufopusgryllotalpa falls close to C vagabunda estuar~es alone, indicating that it special~zeson C vagabunda The w~derscatter of points for deposlt/detrltus feeders compared to herbivores in Fig 6 suggests that the diets largely subtidally on the bottom of the estuary and of depos~t/detr~tusfeeders vary more among species their d~etshave a large benthic component (Fig 5), than do the diets of herbivores It is more likely, how- Including a contribution from eelgrass (Table 3) Peter- ever, that vanat~onsin C and N stable ~sotopevalues son et a1 (1985) similarly suggest that the different among deposit/detrltus feeders reflect taxon-speciflc subhabitats of rlbbed mussels compared to quahogs differences in fractionation of C and N during assimila- ~Clercenanarnercenana are responsible for the larger tion of organic matter (DeNlro & Epstein 1978, 1981 proport~on of phytoplankton found in the diets of Mlnagawa & Wada 1984),since the species included In ribbed mussels compared to hard-shell clams wlthin the deposit/detrltus feeder group belong to 3 different Great Slppewissett Marsh Cape Cod Massachusetts phyla Where we had suff~c~entdata we also looked for The positions of the rlbbed mussel Geukensla seasonal differences in the percentage of eelgrass In demjssa and the soft-shell clam Mya arenaria in Fig 6 the d~etsof prlmary consumers As with suspended indicate that these suspension feeders subsist on a mlx POM the sheepshead mnnow Cypnnodon vanegatus of phytoplankton and macroalgae Cladophora vaga- and the isopod Er~chsonellafihformis are Influenced bv bunda through the consumpt~on of POhZ in Childs eelgrass more In summer than wlnter months (Table 4) River As observed for Sage Lot Pond, the nbbed mus- This seasonality suggests that these herbivores feed at sel gets a larger proport~onof ~tsd~et from phytoplank- least partially on live eelgrass The sea cucumber Scle- ton than does the soft-shell clam rodactyla bnareus, on the other hand, shows no sea- Secondary consumers. The pos~tions of mummi- sonal shift in the percentage of eelgrass contnbuting to chogs Fundulus heterochtus, winter flounder Pseudo- ~tsd~et (Table 4) This is conslstent with the detntus pleulonectes amencanus, and the polychaete Podarke feeding habit of S bnareus Eelgrass detntus becomes obscura In Fig 8 imply that these organisms feed on more edible as ~tdecays (Tenore et a1 1982), and thus benthlc fauna In contrast, st~cklebacksGasterosteus seasonal inputs of live eelgrass are temporally sepa- aculeatus and silversldes Menldia rnenld~aappear to rated from the detntus pool used by S bnareus In ad- consume both benth~cfauna and zooplankton We do McClelland & Valiela: Chalnges in food web structure 269

not assign specific organisms to the diets of each sec- Shifts in stable isotope values of secondary con- ondary consumer because, although the primary consumers from Sage Lot Pond to Childs River (Fig. 8) are sumers we chose for this study are diverse, they rep- difficult to clearly attribute to a loss of eelgrass, since resent only a fraction of the species found in Waquoit secondary consumers are 2 trophic steps away from Bay. Other isotopic investigations of marine food webs eelgrass. Because most of the primary consumers in also identify organisms that use planktonic and ben- Sage Lot Pond get a portion of their diet from eelgrass thic food sources within the same community (Fry & (Table 3), however, it is reasonable to assume that eel- Parker 1979, Fry et al. 1983, Simenstad & Wissmar grass carbon and nitrogen are making it into sec- 1985, Peterson et al. 1986, Thomas & Cahoon 1993, ondary consumers at this estuary. France 1995, Deegan & Garritt 1997). Deegan & Gar- ritt (1997) in particular, however, emphasize the mix- ing of benthic and planktonic food sources in the diets Conclusions of consumers in estuarine waters. Our stable isotope data on secondary consumers (and also suspension Isotopic examination of subtidal food webs in differ- feeders) in the Waquoit Bay estuaries support this ent estuaries of Waquoit Bay shows that diets of pri- perspective. mary consumers are influenced by the dominant forms of production that they are exposed to. Phytoplankton SAGE LOT POND and macroalgae are the major food sources of primary I consumers under both low and high N loading conditions, but eelgrass is also an important food source where N loading is low. Seasonal changes in the percentages of eelgrass in the diets of some primary consumers suggest that they feed on live eelgrass or organic aggregates rapidly formed from eelgrass exudates. Other primary consumers have relatively constant contributions by eelgrass to their diets throughout the year, suggesting that they feed on eel- --. t l grass detritusstored in the sedimnntz. F~lr~rassC and &3~'"""1'"1'""' N are passed on to benthic as well as pelagic sec- z L0 ondary consumers. - CHILDS RIVER O0I I With losses of eelgrass as a result of nitrogen loading, an important pathway through which land- derived nitrogen enters food webs in the Waquoit Bay system is eliminated. The ecological implications of this fundamental change have not been defined, but the rate at which land-derived nitrogen is cycled within estuaries, as well as its ultimate fate, must be influenced by the path of nitrogen flow through estuarine food webs. When eelgrass is replaced by algae, it is llkely that detrital nitrogen becomes available to estuarine consumers at a faster rate. This is because algal detritus starts out as a nutritious food source to consumers, whereas eelgrass detritus must be microbially altered before it can be used by many consumers Flg 8 613C versus 6"N of secondary consumers (with adjust- (Tenore et al. 1982). As a consequence of faster nutri- ment for trophic fractionation, see below) compared to 6I3C ent cycling. through the detrital pathway, detritivores versus 6% of benthic fauna (B) and zooplankton (Z) in Sage may become more closely coupled to annual produc- Lot Pond (lop panel)and Childs River (bottom panel).The sta- tion cycles. Levinton (1972) hypothesized that detritus- ble isotope signature of the ribbed muscle is used as a proxy for that of zooplankton, because ~tsdiet is dom~natedby based benthic communities are more stable than com- phytoplankton. Common names for secondary consumers munities that feed on plankton directly because the (open triangles) are: silversides. Menidia menidia; stickle- food supply to detritus-based communities is relatively back, Gasterosteus aculeatus;mummichog, Fundulus hetero- constant. Shifts from eelgrass- to algae-dominated pro- clitus; winter flounder, Pseudopleuronectes americanus; car- duction brought about by anthropogenic nitrogen nivorous polychaete, Podarke obscura. To correct for trophic fractionation, 1 ?L and 3%owere subtracted from the 6'" and loading may similarly result in less stable communities S5Nvalues respectively of each secondary consumer in shallow estuarine waters. 270 Mar Ecol Prog Ser 168. 259-271, 1998

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Editoi7a1 responsibility: Otto Kinne (Editor), Submitted: December 16, 1997; Accepted: April 3, 1998 Oldendorf/Luhe, Germany Proofs received from a uthor(s): June 3, 1998