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

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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 Published July 9 Mar Ecol Prog Ser 1 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 herbi- vores, 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 consist- ing 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 estuar- ies, as well as its ultimate fate. KEY WORDS: 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 load- ing has increased phytoplankton and macroalgal pro- duction, causing eelgrass production to decrease as a secondary effect (Valiela et al. 1997a). 0 Inter-Research 1998 Resale of full article not permitted 260 mar Ecol Prog Ser 168: 259-271, 1998 \ studled recelve relatively low (Sage Lot Pond), high \ I '/i ;, I L,' \ - I (Quashnet River), and higher (Childs Rlver) n~trogen 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 ' J I In proportion to their productlon, and the diets of con- Waquo~t / A<-- I 1-h / /- sumers would change as the mix of producers changed I 1 Bay /' - 7 ',/ /' I -5. /.: , '/ In fact, however, d~fferencesin chemlcal composition - ZCP 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 (NicOtnlg80, 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 water- shed (Fig. 1). Freshwater enters the Estuary estuaries almost exclusively via Sage Lot Pond Quashnet River Childs R~ver groundwater flow, and with it land- Nitrogen load (kg N ha.' yr-l) 64 520 624 derived nitrogen is conveyed to the 1 1 % 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.
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