Oecologia (2000) 122:568–573
© Springer-Verlag 2000
S.E. MacAvoy · S.A. Macko · S.P. McIninch G.C. Garman
Marine nutrient contributions to freshwater apex predators
Received: 19 March 1999 / Accepted: 26 October 1999
Abstract Recent investigations into the nutrient cycling of coastal ecosystems have suggested that migratory or anadromous fish could be important vectors of marine nutrients. Anadromous fish have assimilated marine nutrients that would contribute to the nutrient budgets of freshwater systems by excretion, gamete release, or the decay of post-reproductive carcasses. However, the extent to which freshwater predators utilize marine material is not well understood. In systems where anadromous fish temporarily constitute a major portion of the fish community, they may contribute substantially to the diet of piscivorous fish and other predators. Here we show the contribution of anadromous blueback herring, shad, and alewife (Alosa) to diets of large, non-indigenous piscivorous catfish (Ictalurus furcatus) using δ34S and δ13C. The spawning anadromous Alosa, captured in tidal freshwater, had enriched δ34S and δ13C values compared to resident, native freshwater species. As a result of consuming the anadromous Alosa, the I. furcatus isotope signature shifted towards the marine signal. The isotope analysis revealed that anadromous fish contribute substantially to the diet of most captured I. furcatus. The percentage of anadromous Alosa carbon and sulfur that was incorporated into I. furcatus (≥38 cm total length) ranged from 0 to 84% and 10 to 69%, and had means (±SD) of 42 (±24) and 43 (±16)%, respectively. Although the δ15N signal of marine-derived biomass is enriched by approximately 3‰ relative to terrestrial or freshwater biomass, it was not as useful as δ34S and δ13C for nutrient source owing to trophic fractionation. This study demonstrates that anadromous fish may be a significant source of nutrients to tidal freshwater apex predators. S.E. MacAvoy (✉) · S.A. Macko Department of Environmental Sciences, University of Virginia, Charlottesville, VA 22903, USA e-mail:
[email protected] S.P. McIninch · G.C. Garman Center for Environmental Studies, Virginia Commonwealth University, Richmond, VA 23284, USA
Key words Isotopes · Anadromous fish · Ictalurus furcatus · Apex predators · Marine nutrients
Introduction Coastal streams have traditionally been viewed as avenues for transport of terrestrial or freshwater production to coastal offshore areas (Mulholland and Olsen 1992; Schlacher and Wooldridge 1996). Some studies have also shown that spawning anadromous fish may be vectors for marine contributions to freshwater nutrient budgets (Hesslein et al. 1991; Kline et al. 1990, 1993; Bilby et al. 1996; Garman and Macko 1998). They suggest that gamete release, excretion, and post-spawning mortality result in the deposition of marine nutrients that are then incorporated into the biomass of autotrophs. A few studies concerning the influence of migratory or anadromous fish upon coastal river nutrient cycles have focused on salmonids in western North America (Hesslein et al. 1991; Kline et al. 1990, 1993; Bilby et al. 1996; Ben-David et al. 1998) and in north-east England (Lyle and Elliott 1998). These studies showed that marine-derived nitrogen contributes 50–100% of autochthonous production in some Alaska streams. The investigation into salmonid import and export of nutrients along the coast of north-east England showed that adult anadromous fish contribute substantially to the total nutrient budget, delivering between 30.4 and 87.9 tons of carbon per year (Lyle and Elliott 1998). Bilby et al. (1996) found that nitrogen brought into the streams of Washington State by Oncorhynchus kisutch (coho salmon) contributed 17–30% of the total utilized nitrogen depending on trophic level. Ben-David et al. (1998) also found that Onchorhynchus contributed significant nitrogen and carbon to riparian plants on Chichagof Island, Alaska, and that the imported nutrients were incorporated into small mammals. Most of these marine nutrient tracer studies have used stable isotope ratios to quantify the degree of marine nutrient contribution to various components of the freshwater system. Marine-derived materials tend to be enriched
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in 15N, 13C, and, in particular, 34S, relative to freshwater or terrestrially derived material (with the exception of C4 plants that are enriched in 13C) (Peterson and Howarth 1987; Michener and Schell 1994). This fact offers an opportunity to trace marine inputs into freshwater systems (or vice versa) and, through mass balance equations, quantify relative contributions from the different sources to ecosystem components. Along the eastern seaboard of North America, anadromous fish of the genus Alosa are the greatest potential source of marine nutrients to freshwater. These fish have historically been highly abundant, and are an important commercial and recreational fishery (Garman 1992; Garman and Macko 1998). The potential carrying capacity of the James River system, Chesapeake Bay drainage, for anadromous clupeids is estimated to be 3.6×106, and this capacity can be considered typical for river systems flowing to the west side of Chesapeake Bay (Garman 1992). There is evidence suggesting that anadromous Alosa contribute to the nutrient budget of coastal freshwater through excretion or post spawning mortality (Garman 1992; Browder and Garman 1994). Additionally, Garman and Macko (1998) hypothesized, based on δ13C measurements on piscivores before and after the anadromous Alosa run, that freshwater piscivores may derive 35.6% of their biomass carbon from anadromous Alosa. Sharing the Virginia tidal freshwater streams with the spawning Alosa and native resident freshwater fish, is a large, introduced apex piscivore, the blue catfish Ictalurus furcatus. Recent gut content analysis of I. furcatus, captured in the tidal freshwater James River, Virginia, United States, has suggested that fish ≥50 cm total length (TL) may consume significant numbers of anadromous Alosa (Chandler 1998). I. furcatus is of particular ecological interest because it is a successful introduced species and has become an apex predator in a system with few native top predators. Longnose gar (Lepisosteus osseus) and bowfin (Amia calva) are the only large native piscivorous fish resident in the tidal freshwater of eastern Virginia. In this paper we quantify the contribution of marinederived biomass to the introduced, apex piscivore I. furcatus using stable isotopic analysis of muscle tissue. In the tidal freshwater systems these predators inhabit, the stable isotopes of sulfur and carbon, and to a lesser extent nitrogen, are useful for differentiating between nutrients derived from marine and freshwater sources. We found that marine carbon and sulfur contributions to individual I. furcatus were highly variable. The fact that marine-derived nutrients, as Alosa, contribute significantly to I. furcatus diets is important not only for the implications to nutrient flow models but also because Alosa are viewed as a natural resource and I. furcatus are an introduced species.
Methods In the spring of 1997 and 1998, coincident with the anadromous Alosa spawning run, fish were captured from the upper tidal freshwater reaches of the Rappahannock River in Virginia, United States, by boat electrofishing. All fish were captured 64–113 km upstream from where the Rappahannock meets the Chesapeake Bay. Representative native resident freshwater species [including: pumpkinseed (Lepomis gibbosus), eastern silvery minnow (Hybognathus regius), yellow perch (Perca flavescens), and creek chubsucker (Erimyzon oblongus)], anadromous Alosa [A. pseudoharengus (alewife), A. aestivalis (blueback herring), and A. sapidissima (American shad)] and piscivorous I. furcatus (≥38 cm TL) were targeted for collection. Samples of dorsal muscle tissue were dried at 60°C for 3 days and homogenized in preparation for analysis. A Carlo Erba elemental analyzer coupled to a Micromass Optima isotope ratio mass spectrometer (Fisons/VG/Micromass, Manchester, UK) was used to obtain δ13C, δ15N, and δ34S values. The δ13C and δ15N were determined concurrently and δ34S was determined during separate analysis runs. The isotope compositions are reported relative to standard material and follow the same procedure for all stable isotopic measurements, as follows: δxE=[(xE/yE)sample/(xE/yE)standard]–1)×1000
(1)
where E is the element analyzed (C, N, or S), x is the molecular weight of the heavier isotope, and y that of the lighter isotope (x=13, 15, 34, and y=12, 14, 32 for C, N, and S respectively). The standard materials to which the samples are compared are PDB for carbon, air N2 for nitrogen and CDT for sulfur. Reproducibility of all measurements was typically 0.3‰ or better. Twenty-five anadromous Alosa were analyzed for δ13C and δ15N. Fourteen were analyzed for δ34S. Eight native resident freshwater fish of similar trophic level were analyzed for δ13C and δ15N, and seven were analyzed for δ34S. Twenty two I. furcatus (between 38 and 82 cm TL) had δ13C, δ15N, and δ34S determined. Not all fish were analyzed for the three isotope ratios. Some fish had δ13C and δ15N determined and some had only δ34S determined. Isotopic mixing equations can be used to quantify nutrient source dependence in systems with isotopically distinct nutrient sources. The general form of the mixing equation used is: δxEcatfish–F=(δxEanad×fanad)+[(δxEfresh×(1–fanad)]
(2)
where fanad is the fraction of diet from anadromous fish, δxEanad and δxEfresh are the mean isotopic signatures of the anadromous Alosa and native resident freshwater fish respectively, and F is fractionation associated with consumption. In the tidal freshwater, these fish represent the isotope end members of the possible catfish diet. Both δ34S and δ13C were used in Eq. 2. The F corrects for trophic enrichment associated with isotopic analysis and is dependent on the isotope used in Eq. 2. In the case of δ13C, F was given a value of 1‰ which is typically the enrichment associated with δ13C. Sulfur isotopes do not significantly fractionate with trophic transfer (Michener and Schell 1994), therefore F=0 when using δ34S in Eq. 2. From the f variables in Eq. 2, the percentage of marine material (e.g., Alosa) that contributed to I. furcatus biomass could be estimated. There are two basic assumptions associated with using isotopic mixing equations. First, that fractionation effects are consistent and can be accounted for, and second, that the isotopic endmembers in the mixing equation are known. In this particular system both these assumptions are generally satisfied. The first assumption does not apply for δ34S because it does not fractionate with trophic level. For δ13C fractionation is generally accepted to be about 1‰, although small deviations from this value do occur (DeNiro and Epstein 1978; Doucett et al. 1996). Addressing the second assumption, there is no source of enriched δ13C or δ34S in this tidal freshwater area except marine biomass (Garman and Macko 1998; MacAvoy et al. 1998). An extensive survey of instream and near-shore plants in a stream similar to this one has
570 Table 1 Means ±SDs and n (in parentheses) of isotope ratios for the different species of anadromous and native resident fish used in this study δ13C Anadromous Alosa A. pseudoharengus A. aestivalis A. sapidissima
δ34S
δ15N
–18.0±1.4 (14) 18.4±1.1 (13) 12.8±0.6 (14) –19.0±0.7 (7) 19.3 (1) 13.2±0.3 (7) –20.2±0.7 (4) 12.6±0.4 (4)
Native resident freshwater species Lepomis gibbosus –26.1 (1) Hyboganthus regius –24.1±1.7 (3) Perca flavescens –26.1±2.9 (3) Erimyzon oblongus –28.1 (1)
2.5 (1) 4.9±2.0 (2) 5.3±1.1 (4)
13.4 (1) 11.2±1.2 (3) 12.9±2.5 (3) 10.9 (1)
Table 2 Means and standard deviations (in parentheses) for isotope ratios. Means with the different letters are significantly different (P≤0.05) as indicated by Kruskal-Wallis analysis and the Dunn procedure
Resident freshwater Anadromous Alosa Ictalurus furcatus
δ13C
δ34S
δ15N
–25.6 (2.3)a –18.6 (1.4)b –21.7 (1.8)c
4.8 (1.6)a 18.4 (1.1)b 10.6 (2.1)c
12.2 (1.7)a 12.9 (0.6)a 16.3 (1.7)b
shown constantly depleted δ13C values (–27 to –30‰; Garman and Macko 1998) and Alosa captured in this study and others have been significantly enriched in 13C whereas native resident fish have been consistently depleted (Garman and Macko 1998; MacAvoy et al. 1998). Likewise, resident freshwater fish captured in the tidal freshwater of Virginia have consistently been depleted in 34S relative to anadromous adults (MacAvoy et al. 1998). Carbon and sulfur isotopes were used in the mixing equation, however nitrogen isotopes were not used for two reasons. First, the trophic fractionation associated with δ15N is more variable than that of δ13C. The general fractionation factor assigned is 3.0–3.5‰; however slightly smaller and larger fractionation factors have been reported (Hansson et al. 1997; Hobson and Welch 1992). The variability in fractionation makes the assignment of F in Eq. 2 uncertain. Second, because the I. furcatus are apex predators they consume resident freshwater fish from several trophic levels. This makes the assignment of δxEfresh in Eq. 2 problematic for nitrogen. Kruskal-Wallis nonparametric procedures were used to test for differences in isotopic values among the three groups of fish (native resident freshwater, anadromous and I. furcatus) (α=0.05). The Dunn procedure was used to examine differences between groups (Rosner 1990). Statview SE+Graphics (Abacus Concepts, Inc.) and Microsoft Excel version 5.0 (Microsoft, Inc.) were used for statistical tests.
Results The mean δ13C value for the anadromous Alosa was –18.6±1.4‰ (n=25), ranging between –20.8 and –16.1‰ (Fig. 1a), reflecting marine phytoplankton. The native resident freshwater species had mean δ13C of –25.6±2.3‰ (n=8), a difference of 7‰ from the mean Alosa value. The range of native resident freshwater fish δ13C values was –28.6 to –22.9‰ (Fig. 1a). There was also a difference of >4‰ among the different species of resident freshwater fish (Table 1). I. furcatus had mean δ13C
Fig. 1a,b Stable isotope ratios for fish sampled in this study. a δ15N vs. δ13C. Anadromous fish species are Alosa pseudoharengus, A. aestivalis and A. sapidissima. Native resident freshwater fish species are Lepomis gibbosus, Hyboganthus regios, Perca flavescens and Erimizon oblongus. b δ34S vs. δ13C. Anadromous fish include A. pseduoharengus and one A. aestivalis. Native resident freshwater fish include H. regios, P. flavescens and E. oblongus. Not all the native resident freshwater fish that were analyzed for δ34S are shown, only the individuals that had both δ13C and δ34S determined
of –21.7±1.8‰ (n=22), ranging between –26.0 and –18.7‰, intermediate to the anadromous Alosa and the native resident freshwater fish (Fig. 1a). Kruskal-Wallis analysis and the Dunn procedure showed that each of these groups were significantly different from one another (P
