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Stable isotopes of nitrogen and carbon in an aquatic food web recently invaded by Dreissena polymorpha (Pallas)
Myron J. Mitchell, Edward L. Mills, Nasser Idrisi, and Robert Michener

Abstract: The carbon and nitrogen concentrations and the stable isotopic compositions ( 13C and 15N) of major abiotic and biotic constituents were determined in Oneida Lake, New York. This lake was invaded by the zebra mussel (Dreissena polymorpha) in 1990 and there have been concomitant changes in various biotic and abiotic lake properties. The C (46-49%) and N (12%) concentrations and C:N ratios (3.9-4) of zebra mussel flesh were similar to those reported for other lakes. Trophic positions were reflected in the 15N values for which walleye> gizzard shad and yellow pereh > Daphnia spp. and zebra mussel flesh > seston and sediment. There was an average increase of 3.6 1 5N per the 13C analysis suggest that Daphnia spp. were using a distinct source of organic carbon whereas zebra mussel were using the entire seston resource. Only yellow perch showed a significant shift in 13C values (1.1.), possibly reflecting a shift in food source and diet from 1992 to 1993.

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Use of stable isotopes of carbon (C) and nitrogen (N) is a powerful tool in evaluating trophic relationships in limnetic food webs (Peterson and Fry 1987; Fry 1991; Yoshioka et al. 1994). When observational data involving diets and trophic interactions prove difficult to interpret, stable isotopes can provide useful insights into the feeding relationships of organisms within a given food web (Gu et al. 1994). Analyses of stable isotopes of C and N have also been used to evaluate the contributions of various C sources to the energy flux of limnetic systems (Bunn et al. 1989; Hamilton et al. 1992). Often the C isotopic compositions of animals correspond closely to those of their food sources. It is possible to ascertain the relative importance of allochthonous versus autochthonous C sources, because they generally have distinctive C isotopic ratios (exReceived April 19, 1995. Accepted December 13, 1995. J12878 M.J. Mitchell1 and N. Idrisi. College of Environmental Science and Forestry, State University of New York, 1 Forestry Drive, Syracuse, NY 132102788, U.S.A. E.L. Mills. Cornell Biological Station, 900 Shackelton Point Road, Bridgeport, NY 13030, U.S.A. R. Michener. Department of Biology, Boston University, 5 Cummington Street, Boston, MA 02215, U.S.A.

Author to whom all correspondence should be addressed. e-mail:mitchell@mailbox.syr.edu

pressed as 13C) (Hamilton et al. 1992; Peterson et al. 1994). The actual isotopic values of the trophic components, however, may vary among lakes and over time because of the many processes that affect the C isotopic composition (Fry and Sherr 1989). There is also a direct correspondence between diet, trophic position, and the stable isotopic composition of N. This is mainly due to the preferential catabolism and excretion of the lighter form of 14N, resulting in increased 15N values of approximately 35 for each trophic transfer along a food chain (Peterson and Fry 1987; Cabana and Rasmussen 1994). North Americas Great Lakes have recently been invaded by the zebra mussel (Dreissena polymorpha), the origin of which was most likely eastern Europe and Russia (e.g., Ludyanskiy 1993; Spidle et al. 1994). The zebra mussel was first sighted in the western basin of Lake Erie in 1986 (Hebert et al 1989) and has spread rapidly born the Great Lakes eastward through the Erie-Barge Canal and the Mohawk and Hudson river systems and southward through the Mississippi River drainage. Infestation of lakes by zebra mussels may have marked impacts on aquatic food webs. Zebra mussels feed on algal particles removed from the water column and deposit feces and unwanted particulate matter in the form of pseudofeces onto sediments. Such filtering activity may have strong effects on lakewide phytoplankton biomass because of the typically high densities of zebra mussels (more than 300000 individuals/m 2 in Lake Erie; Leach 1993) as well their high individual filtering rates (Kryger and Riisgard 1988). Because of their high densities and ability to filter large quantities of 1996 NRC Canada

Can. J. Fish. Aquat. Sci. 53:1445-1450 (1996).

1446 Fig. 1. The major components of the Oneida Lake food web.
Adult Walleye

Can. J. Fish. Aquat. Sci. Vol. 53, 1996 from about 25C in August to 1C under winter ice cover. Water chemistry is strongly influenced by nutrient-rich streams that flow from the south over outcropping of Onondaga limestone and through the fertile Lake Ontario plain. Oneida Lake waters are alkaline with a mean pH of 8.0 and alkalinity of 87 mg CaCO3/L, and mean concentrations of NO3- in the summer generally range between 150 and 200 g/L. Trophic relationships in the Oneida Lake food web including the zebra mussel are shown in Fig. 1. Review of a 14-year data set prior to the invasion of the zebra mussel (19751988) indicated that mean annual chlorophyll and total phosphorus concentrations from May through August ranged from 5.6 to 11.7 g/L and from 23 to 58 g/L, respectively (McQueen et al. 1992). Over 60 species of fish inhabit the lake. The walleye (Stizostedion vilreum) is the most abundant predator and walleye predation controls recruitment of yellow perch (Perca flavescens) and strongly influences the species and size composition of the fish community. Walleye and yellow perch share the limnetic region with white perch (Morone americana) and gizzard shad (Dorosoma cepedianum), a clupeid in which vast schools of young have been observed since 1984. The dominant cladoceran grazers in the lake are Daphnia pulicaria and Daphnia galeata mendotae. the abundance of which is closely tied to the abundance of young planktivorous fish (Mills and Forney 1981). Since colonization of Oneida Lake by Dreissena polymorpha, the clear-water phase has been extended by as much as 3040 days, the lake has experienced unprecedented cyanophyte blooms of Aphanizomenon flos-aquae, and summer Secchi disc readings are among the highest ever recorded for this lake. Yet when A. flos-aquae appears, water clarity declines to the lowest levels recorded. Sampling Samples were collected at a site 0.4 km northeast of Shackleton Point at 11 m depth. Suspended particulate samples were collected on 5 days from 2 July to 18 August, 1992, and on 6 days from 18 June to 12 July, 1993. The water samples were collected with an 11-m integrated Tygon tube (2 cm i.d.). Particulate were filtered onto a glass-fiber filter (Whatman 934-AH) precombusted at 550C for 30 min. After filtering, the filters and particulates were dried to a constant weight at 60C and frozen. Control filters were made with distilled water. Sediment samples were collected in triplicate in August 1992 and 1993 using a Kajak-Brinkhurst corer. The upper 5 cm of the samples was removed from the coring tube and frozen until further analyses. Daphnia spp. were collected by towing a 752-m mesh net at the same site on 29 June 1992 and 14 June 1993. Daphnia spp. were allowed to evacuate their guts for 36 h (evaluated using microscopic examination) in a series of baths with glass-fiber filtered water. When evacuation was complete, Daphnia spp. were concentrated and frozen. Microscopic examination indicated that in 1992 Daphnia galeata mendotae comprised >99% of the animals in the sample and Daphnia pulicaria comprised >99% in 1993. A minimum of 1000 animals was composite for each isotopic and elemental analysis. Zebra mussels attached to shells of unionid clams were collected by SCUBA on 23 July 1992 and 22 July 1993 near Shackleton Point. Zebra mussels were allowed to evacuate overnight in filtered Oneida Lake water to remove algal and detrital particles. Mussels were opened and soft tissues were removed and frozen. At least 100 individuals were composite for each analysis. Young-of-the-year yellow perch and gizzard shad were collected and allowed to evacuate for 25 h in water cleared of zooplankton. Yellow perch were collected with a beach seine at Shackleton Point on 30 June and 27 July 1993. Gizzard shad were collected using a surface trawl on 21 July 1992. At least 50 individual yellow perch or gizzard shad were composited for each analysis. Adult walleye were collected on 2 July 1993 by bottom trawl. Lateral muscle samples of walleye were taken from nine individuals (295 to 472 mm total length). All fish were frozen for later analyses. 1996 NRC Canada

Adult Yellow Perch

Young-of-the-Year Fish (e.g., Yellow Perch and Gizzard Shad) Benthic Macroinvertebrates Pseudo feces Zooplankton (e.g., Daphnia)

Benthic Algae


water (Reeders et al. 1989: MacIsaac et al. 1991) zebra mus-

sels enhance water clarity (Leach 1993), decrease phytoplankton abundance (Stanczykowska et al. 1975; Nichols and Hopkins 1993), and may shunt nutrients and energy from the pelagia to the benthos, leading to an increase in benthic production (Walz 1979; Stanczykowska and Planter 1985; Stewart and Haynes 1994). Long-term studies of ecological systems are vital if we are to attain an accurate perception of ecological dynamics and to differentiate natural variability from impacts of exotics such as zebra mussels. Few long-term data sets exist for aquatic ecosystems but in the case of Oneida Lake, New York, ecological research has been conducted since the beginning of this century (Adams and Hankinson 1916; Baker 1916) and sub-

stantial charges in the biota and chemistry of the lake have been documented over this period (see reviews in Mills et al. 1987; Mills and Forney 1988). One major change in the biota has been the infestation of the lake by zebra mussels (Dreissena polymorpha). Zebra mussels likely invaded the lake in 1990 and by 1993, densities on hard substrate shoals (comprising 2030% of the lakes surface area) were high and generally ranged between 30 000 and 100 000 individuals/m2. Because these mollusks feed by removing particles from the water column and deposit their wastes on the lake bottom, they are key elements in the coupling of benthic and pelagic food pathways (Kautsky and Evans 1987; Lauritsen 1986; Murphy and Kremer 1985: Olafson 1989). As a result, the zebra mussel is likely inducing food web changes in this well-studied ecosystem, making it an ideal location for examining how changes in the trophic structure may be reflected in the isotopic composition of its abiotic and biotic constituents. Consequently, the objectives of this study are to present the elemental (C and N) and stable isotopic composition ( 13C and 15N) of some major constituents of the Oneida Lake food web and to use this information to evaluate trophic changes associated with the invasion of the zebra mussel.

Field site description Oneida Lake (7555W, 4312N; Onondaga County, New York) is a naturally eutrophic (mean depth, 6.8 m; flushing rate, 1.6 year-l), warm water lake covering 20 700 ha on the Lake Ontario plain of central New York (Mills et al. 1978). Oneida Lake is generally well mixed during the ice-free months with water temperatures ranging

Mitchell et al. Table 1. Carbon and nitrogen concentrations of representative ecosystem constituents of Oneida Lake. Year Sediment Zebra mussel shell Zebra mussel flesh Daphnia spp. Yellow perch Gizzard shad Walleye 1992 1993 1992 1993 1992 1993 1992 1993 1992 1993 1992 1993 1993 C(%) 4.8 + 0.0 (6) 4.4 + 0.4 (6) 12.4 + 10.0 (3) 12.7 + 0.0 (2) 46.2 + 0.2 (2)* 48.8 + 0.5 (2)* 43.0 + 0.5 (6)* 46.5 + 0.1 (4)* 42.8 + 0.3 (2) 44.8 + 0.0 (2) 43.6 + 0.2 (2)* 47.1 + 0.4 (2)* 48.4 + 0.0 (2) N (%) 0.48 + 0.01 (6) 0.49 + 0.05 (6) 0.29 + 0.02 (3) 0.29 + 0.01 (2) 11.68 + 0.16 (2) 12.46 + 0.15 (2) 8.95 + 0.04 (6)* 8.84 + 0.02 (4)* 11.83 + 0.05 (2) 12.24 + 0.07 (2) 11.98 + 0.04 (2)* 12.83 + 0.13 (2)* 12.74 + 3.01 (2) Sediment Seston Zebra mussel shell Zebra mussel flesh Daphnia spp. Yellow perch Gizzard shad Walleye Table 2. Carbon and nitrogen stable isotopic composition of representative ecosystem constituents of Oneida Lake. Year 1992 1992 1993 1992 1993 1992 1993 1992 1993 1992 1993 1992 1993 1993


15N ()

Note: Values are given as the mean+ SE, with N in parentheses. *Significant difference between years by t test at p < 0.05. Preparation and analyses All samples, except water, were freeze dried and pulverized to ensure sample homogeneity. Replicate samples were analyzed for C and N using a Perkin-Elmer 2400 CHN analyzer. Isotopic analyses of C and N were done at the Stable Isotope Laboratory at Boston University using a Finnigan Delta-S isotope ratio mass spectrometer. The isotopic composition of samples was expressed using the 13C and 15N notation defined as follows:

26.2 + 0.5 (4) 25.6 + 0.3 (3) -29.8 + 0.6 (4) -30.7 + 0.4 (10) -6.4 + 0.0 (2) -8.1 + 0.1 (3) -31.3 (1) -32.7 + 0.9 (2) -33.6 + 0.2 (3) -33.6 (1) 30.8 + 0.1 (2)* 31.9 + 0.2 (2)* -32.0 (1) -31.7 + 0.3 (2) -28.3 + 0.1 (2)

7.5 + 0.5 (4) 7.3 + 0.0 (3) 7.5 + 0.2 (4) 6.0 + 0.43 (10) na 7.7 (1) 8.1 + 0.3 (2) 8.8 + 0.6 (3) 8.3 (1) 12.5 + 0.l (2) 12.3 (1) 13.4(1) 12.4 + 0.O (2) 15.7 (1)

Note: Values are given as the mean + SE. with N in parentheses. Data for zebra mussel shel1 are for inorganic carbon only. na, not available. *Significant difference between years by t test at p + 0.05. 9% (C in sediment). This latter high value reflected spatial variation in the sediment of Oneida Lake. The C concentrations were similar, but N concentrations were lower for zebra mussel flesh from Lake St. Clair in Michigan (ranged from 44.0 to 48.8% and from 8.8 to 10.5%, respectively: Nalepa et al. 1993) compared with mussels from the present study (Table 1). These elemental differences resulted in C:N ratios of 3.94.0 that were lower than the 4.45.7 ratios for zebra mussels from Lake St. Clair. Ratios of 3.6 and 5.3 have been reported for zebra mussels in Lake Mikolajskie, Poland (Stanczykowska and Lawacz 1976), and Lake Constance, Switzerland (Walz 1979), respectively. Isotopic composition The isotopic composition of the samples reflected their trophic positions (Table 2). This is evident in the 15N values where walleye > gizzard shad and yellow perch > Daphnia spp. and zebra mussels > seston and sediment. There was an average increase of 3.6h 15N per trophic level among zooplankton (Daphnia spp.), zooplanktivores (gizzard shad and yellow perch), and piscivores (walleye). This value agrees very well with previous studies that have shown that the 15N values can be used to predict trophic position (Minegawa and Wada 1984; Peterson and Fry 1987; Cabana and Rasmussen 1994). The 15 N values of Dahnia spp. tend to be slightly greater, but not significantly (p > 0.05) different from the 15N values of zebra mussel flesh or seston (Fig. 2). Therefore, zebra mussels and Daphnia spp. occupy similar trophic positions in Oneida Lake. Phytoplankton comprised 5.4% of the seston sampled (M. Hogan, Cornell University, Ithaca, N.Y., personal communication) and represented a food source for both the benthic zebra mussels and zooplankton such as Daphnia spp. The variability in isotopic composition of the seston was likely due to differences in the algal and detrital components that may have distinctive isotopic characteristics (Hamilton and Lewis 1992; France 1995a). In our study no separation of these two components was attempted. The only significant difference (p< 0.05) in isotopic composition between 1992 and 1993 was a 1.1 1996 NRC Canada

where is parts per thousand and 13C/12C and 15N/14N are the atomic ratios of the number of atoms in the sample or standard. The international standards for C and N are PeeDee Belermnite and the Earths atmosphere, respectively. Front-ended to the mass spectrometer were a Heraeus C and N analyzer and a Finnigan CT-box for cryogenic separation of gases. Typical analytical precision was + 0.2 for both 13C and 15N determinations. Comparisons among samples were evaluated using paired t tests (p = 0.05 and 0.01) and Pearson correlation (Sokal and Rolf 1981).

Results and discussion Elemental composition The results of the elemental analysis for abiotic and biotic constituents of Oneida Lake are presented in Table 1. Concentrations of C and N were lower in sediments and zebra mussel shells, compared with the other constituents, which were rich in proteins and thus high in both C and N. The lower N concentrations in Daphnia spp. reflect the contribution of its polysaccharide, chitinous exoskeleton. The zebra mussel shell had intermediate C concentrations and very low concentrations of N, reflecting the predominance of inorganic C. Some statistical differences in elemental concentrations were found between samples taken in 1992 and 1993 at p < 0.05, but not at p < 0.01. The percent relative differences in the elemental compositions were generally small and ranged from less than 1% (N concentration in zebra mussel and walleye flesh) up to

1448 Fig. 2. Isotopic composition ( 13C and 15N) of samples of selected food web constituents of Oneida Lake for 1992 and 1993. The 13C value for zebra mussel shell is for inorganic carbon only.

Can. J. Fish. Aquat. Sci. Vol. 53, 1996

suggesting that cladocerans were using a distinctive C source. A possible explanation for the lower d13C values of Daphnia spp. is the utilization of recycled dissolved organic carbon (DOC) and particulate organic carbon (POC) within the pelagic zone (Hamilton et al. 1992). C derived from the microbial breakdown of DOC is lighter than DIC imported into the system (Peterson et al. 1994). This explanation does not seem likely because of the highly mixed nature of Oneida Lake, exposing both zooplankton and zebra mussels to the same DOC and POC sources. A more plausible explanation for the lower 13C of Daphnia spp. may be the utilization of the smaller size fractions (pico- and nano-plankton, <50 m) of the seston by Daphnia spp., which have lower 13C values than net plankton (Fry and Sherr 1989). Zebra mussels maybe utilizing most of the particles in the seston as evidenced by the corresponding 15C and 15N values of zebra mussel flesh and the seston. The similarity in 13C values for yellow perch and gizzard shad shows clearly that these two planktivores were using the same food. This correspondence can be contrasted with that of walleye, for which the 13C values were higher. If combined with the 15N data, these results show that the walleye were the top carnivores and were feeding on age0 yellow perch and gizzard shad (Fig. 1).
Stable isotopes and the response of food webs to


increase in 13C for yellow perch, possibly reflecting either variation in isotopic composition among populations in our samples or an actual shift in food source and diet (Table 2). C isotope ratios varied widely between the sediment and seston (Table 2, Fig. 2). This pattern of 13C distribution has been documented in other systems (Fry and Sherr 1989) and can be attributed to different C sources. The relatively heavy 13C value of the sediments maybe due to the preferential loss of the lighter 12C isotope during sediment catabolism. It might be expected that the temporal variability in 13C in Oneida Lake would be dampened because of the high concentrations of dissolved inorganic carbon (DIC) with distinctive isotopic cornposition or it may reflect inputs of terrestrial organic C. The 13C values of Oneida Lake sediment are greater than those (25.8 to 30.6) reported for Lake Memphremagog, Quebec (LaZerte 1983). The 13C value of DIC in Oneida Lake was found to be 6.9, which agrees closely with the average value of -7.2 for the inorganic C in zebra mussel shells (Table 2). If we assume a 2223 fractionation by the phytoplankton, the 13C value for the seston indicates that it is primarily autochthonous organic matter. Among animals, 13C values are typically within + 2 of those of their food sources (Fry and Sherr 1989). The 13C values for seston and zebra mussel flesh were similar (Fig. 2), suggesting that these mollusks were using the entire seston C 13 source. In contrast, the C values for Daphnia spp. were lower than those for seston and the flesh of zebra mussels,

Dreissena polymorpha An ecological concern in freshwater lakes is that the zebra mussel, through its filter-feeding activities, will shift the C flow in the food web from the pelagia to the benthos. However, zooplankton also feed on natural seston; so the question arises, is the phytoplankton decline an effect of Daphnia spp. or zebra mussels? In Lake Erie, Wu and Culver (1991) concluded that Daphnia grazing effects were more important than zebra mussel effects on phytoplankton. On the other hand, Nichols and Hopkins (1993) concluded that the decline of Lake Erie phytoplankton was due to the filtration activity of zebra mussels. Evidence for zebra mussel effects on Lake Erie phytoplankton was the observed proportional decline in all major groups of algae, including large and small forms, which is consistent with our own assessment that Dreissena polymorpha is capable of utilizing most sestonic particles. Other studies support the hypothesis that recent reductions in Lake Erie phytoplankton are in response to grazing by zebra mussels (Leach 1993; MacIsaac et al. 1992; Holland 1993). In the present study, the lower food web components of Daphnia spp., zebra mussels, and natural seston are linked. Whereas sediment, seston, zebra mussel flesh, and Daphnia spp. showed small differences in 15N, these same trophic components were separated by their 13C values. The positioning of isotopic ratios of C indicated that zebra mussels have a greater reliance on natural seston for food than Daphnia spp. but neither Daphnia spp. nor zebra mussels were associated with the sediments (Fig. 2). Consequently, it appears that stable isotopes of C provide one more piece of evidence linking zebra mussel grazing with increasing water clarity and decreasing algal concentrations in freshwater lakes (Hebert et al. 1991; MacIsaac et al. 1992; Griffiths. 1993; Leach 1993). The stable isotopes of C and N can help elucidate trophic structure and energy sources in various populations of aquatic food webs (McConnaughey and McRoy 1979; Kling et al. 1992; Hamilton et al. 1992). Analysis of isotopic variability
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Mitchell et al. among individuals may also be useful in evaluating changes in feeding patterns (France 1995b). A possible impact of zebra mussels on the Oneida Lake food web is a shunting of more production into the benthos. A concomitant decline in pelagic zooplankton and an increase in benthic macroinvertebrates could force age0 planktivorous fish to shift to benthos at an earlier age. The isotopic data collected in 19921993 (Fig. 2), however, suggest that during that period the dominant food source for age0 yellow perch was still zooplankton. Further increases in water clarity and decreased phytoplankton abundance may force zooplankton to feed more on bacteria and use a greater proportion of C as food from the microbial loop. In addition, changes in light availability may alter the 13C values by affecting the13rate of photosynthesis and the kinetic discrimi-nation against C (Herczeg and Fairbanks 1987). If recruitment of age0 yellow perch and gizzard shad declines in response to a decline in pelagic zooplankton, walleye may become cannibalistic by feeding on their own young. Consequently, we might expect changes in stable isotope composition to be manifested along with possible changes in the Oneida Lake food chain as the impact of zebra mussels increases. Further isotopic analyses in Oneida Lake as the impact of the zebra mussel intensifies will help us to ascertain both the magnitude and the direction of these changes. Acknowledgments This work was supported by the New York Sea Grant Institute. We appreciate the help of Marty Hogan and Bryan Lantry in sample collection. Jeff Owen and Qin Qin Xu helped in sample preparation and elemental analyses. Don Stewart provided helpful comments on the manuscript. This is contribution No. 173 of the Cornell Biological Field Station. We also appreciate the useful comments of Dr. Robert France and an anonymous reviewer on an earlier version of the manuscript. References Adams, C.C., and Hankinson, T. 1916. Notes on Oneida Lake fish and fisheries. Trans. Am. Fish. Soc. 45: 155166. Baker, F.C. 1916. The relation of mollusks to fish in Oneida Lake. Tech. Publ. State Univ. Coll. For. Syracuse Univ. No. 4. pp. 1366. Bunn, S.E., Barton, D. R., Noel Hynes, H. B., Power, G., and Pope, M.A. 1989. Stable isotope analysis of carbon flow in a tundra river system Can. J. Fish. Aquat. Sci. 46: 17691775. Cabana G., and Rasmussen, J.B. 1994. Modelling food chain structure and containment bioaccumalation using stable nitrogen isotopes. Nature (London), 372: 255257. France, R.L. 1995a. Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Mar. Ecol. Prog. Ser. 124: 307-312. France, R.L. 1995b. Differentiation between littoral and pelagic food webs in lakes using stable carbon isotopes. Limnol. Oceanogr. 40: 13101313. Fry, B. 1991. Stable isotope diagrams of freshwater food webs. Ecology, 72: 22932297. Fry, B., and Sherr, E.B. 1989. 13C measurements as indicators of carbon flow in marine and freshwater ecosystems. In Stable isotopes in ecological research. Ecological studies No. 68. Edited by P.W. Rundel, J.R. Ehleringer, and K.A. Nagy. Springer-Verlag, New York. pp. 196229. Griffiths, R.W. 1993. Effects of zebra mussel (Dreissena polymor-

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