Tracing Energy Flow in Stream Food Webs Using Stable Isotopes Of
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Freshwater Biology (2010) 55, 941–951 doi:10.1111/j.1365-2427.2009.02327.x Tracing energy flow in stream food webs using stable isotopes of hydrogen ,† ‡ † JACQUES C. FINLAY* , RICHARD R. DOUCETT AND CAMILLE MCNEELY *Department of Ecology, Evolution and Behavior, University of Minnesota, St Paul, MN, U.S.A. †St Anthony Falls Laboratory, National Center for Earth-surface Dynamics, University of Minnesota, MN, U.S.A. ‡Colorado Plateau Stable Isotope Laboratory, Merriam Powell Center for Environmental Research, Northern Arizona University, Flagstaff, AZ, U.S.A. SUMMARY 1. Use of the natural ratios of carbon and nitrogen stable isotopes as tracers of trophic interactions has some clear advantages over alternative methods for food web analyses, yet is limited to situations where organic materials of interest have adequate isotopic separation between potential sources. This constrains the use of natural abundance stable isotope approaches to a subset of ecosystems with biogeochemical conditions favourable to source separation. 2. Recent studies suggest that stable hydrogen isotopes (dD) could provide a robust tracer to distinguish contributions of aquatic and terrestrial production in food webs, but variation in dD of consumers and their organic food sources are poorly known. To explore the utility of the stable hydrogen isotope approach, we examined variation in dD in stream food webs in a forested catchment where variation in d13C has been described previously. 3. Although algal dD varied by taxa and, to a small degree, between sites, we found consistent and clear separation (by an average of 67&) from terrestrial carbon sources. Environmental conditions known to affect algal d13C, such as water velocity and stream productivity did not greatly influence algal dD, and there was no evidence of seasonal variation. In contrast, algal d13C was strongly affected by environmental factors both within and across sites, was seasonally variable at all sites, and partially overlapped with terrestrial d13C in all streams with catchment areas larger than 10 km2. 4. While knowledge of isotopic exchange with water and trophic fractionation of dD for aquatic consumers is limited, consistent source separation in streams suggests that dD may provide a complementary food web tracer to d13C in aquatic food webs. Lack of significant seasonal or spatial variation in dD is a distinct advantage over d13C for applications in many aquatic ecosystems. Keywords: energy flow, food webs, stable isotopes, subsidies, trophic interactions Introduction Correspondence: Jacques C. Finlay, Department of Ecology, Knowledge of the sources and fluxes of energy and Evolution and Behavior, University of Minnesota, 1987 Upper nutrients through food webs is integral to under- Buford Circle, St Paul, MN 55108, U.S.A. standing the productivity and diversity of consumers E-mail: jfi[email protected] and essential to any effort to understand their Present address: Camille McNeely, Department of Biology, ecological interactions. The sources of organic matter Eastern Washington University, 258 Science Building, Cheney, that fuel aquatic consumers are highly diverse in WA 99004-2440, U.S.A. space and time, a feature that has presented Ó 2009 Blackwell Publishing Ltd 941 942 J. C. Finlay et al. substantial challenges to understanding food web used to measure trophic position, d15N can provide a dynamics. Stable isotopes are increasingly used to complementary source tracer to d13C in some settings, trace energy flow and trophic structure in food webs such as at the marine–freshwater interface, and in because they integrate across spatial and temporal highly eutrophic ecosystems where source differences scales and thus provide important information that is are large (e.g. Delong & Thorp, 2006). Such applica- not otherwise accessible without very large expendi- tions are limited, however, by variable trophic frac- tures of research time and resources (Peterson & Fry, tionation by primary consumers (e.g. Goedkoop, 1987). Akerblom & Demandt, 2006) and temporal changes Most natural abundance isotope studies of diet in organic matter d15N because of variation in d15Nof sources use stable isotopes of carbon (i.e. d13C). dissolved inorganic nitrogen and microbial immobil- Tracing of sources using d13C in aquatic ecosystems isation of N onto organic matter (Finlay & Kendall, relies on isotopic differences between potential or- 2007). Sulphur stable isotopes (d34S) are increasingly ganic matter sources that arise from variation within used to complement d13C analyses in organic matter or among ecosystems in plant d13C, usually because of source tracing. A recent review found that d34S effects of inorganic carbon d13C and fractionation of distinguished organic matter sources in coastal inorganic carbon d13C during photosynthesis (Peter- marine ecosystems better than d15N (Connolly et al., son & Fry, 1987). After carbon is fixed by plants, there 2003). Within freshwater ecosystems, however, the are minor changes associated with aerobic decompo- sparse data available indicate relatively little differ- sition and trophic transfer so that d13C is an effective ence between major organic matter sources in d34Sin tracer of diet sources (Vander Zanden & Rasmussen, most ecosystems (Finlay & Kendall, 2007). 2001). While environmental variation or physiological Hydrogen stable isotopes (i.e. 2H and 1H, deute- differences among plants create useful separation rium : hydrogen, dD, or d2H) in organic materials are between source d13C in some streams and lakes (e.g. variable in the environment and could provide an Finlay, 2001; Grey, Jones & Sleep, 2001), there are alternative or complementary natural abundance iso- others where source d13C overlap occurs during some topic tracer to those of carbon, nitrogen and sulphur. or all of the year. Terrestrial plants show a somewhat dD is increasingly used to track movement and limited range of d13C values such that variation in migrations of animals (Hobson, 1999; Bowen, Was- algal d13C largely determines the degree of overlap senaar & Hobson, 2005) but has not been widely used between allochthonous and autochthonous sources in to distinguish organic matter sources and energy freshwaters (Finlay & Kendall, 2007). Algal d13C can flow pathways in food webs. Such use was consid- have a range that exceeds 15& within a site because of ered decades ago (Smith & Epstein, 1970; Estep & variation in water flow (France, 1995; Hecky & Dabrowski, 1980) but was not widely adopted because Hesslein, 1995; Trudeau & Rasmussen, 2003; Singer of methodological limitations and concern about et al., 2005), biomass (Hill & Middleton, 2006), dis- unexplained variability in dD (see Doucett et al., 2007). 13 solved CO2 concentrations and d C of dissolved Recent advances in stable hydrogen isotope meth- inorganic carbon (Finlay, 2004). In aquatic ecosystems ods have triggered new interest in dD as a tracer in where environmental conditions are highly dynamic, freshwater ecosystems. dD has been most commonly tracing of energy flow with d13C may not be possible analysed in specific compounds rather than bulk or may require a high intensity sampling effort. organic materials because of variation among biolog- Greater knowledge of environmental effects on ical tissues and methodological concerns. Improved variation in d13C values of sources and recognition analytical techniques (Wassenaar & Hobson, 2003) of the inherent complexity of many food webs have, however, addressed some of the methodological suggests a need for additional tracers of energy flow issues associated with analyses of bulk tissues. Fur- pathways in aquatic ecosystems. Use of multiple ther, a recent study suggests that effects of trophic tracers greatly increases the ability to resolve organic fractionation and exchange of isotopes between matter sources in food webs and ecosystems (Phillips organism and water are relatively small and may be & Gregg, 2003). The stable isotope tracer often used to predictable (Solomon et al., 2009). Finally, a study in complement d13C in natural abundance studies of rivers of the southwestern U.S.A. demonstrated a aquatic ecosystems is d15N. While most commonly large isotopic separation between non-exchangeable Ó 2009 Blackwell Publishing Ltd, Freshwater Biology, 55, 941–951 Hydrogen isotope tracing in food webs 943 dD in terrestrial and aquatic sources of organic matter Methods and their consumers (Doucett et al., 2007). Together, General approach these advances suggest the potential of dDasan effective tool to analyse energy flow in aquatic food The primary study sites were in the South Fork of the webs. Eel River catchment in the Coast Range of Mendocino There is, however, little information to determine County, CA. Previous studies of stream food webs at the general efficacy of source separation using dD. In this site have identified the controls over d13Cof plants, stable isotope ratios are determined by the d resources and invertebrate consumers (Finlay, Power value of inorganic nutrients and fractionation during & Cabana, 1999; Finlay, Khandwala & Power, 2002; photosynthetic uptake. Inorganic hydrogen incorpo- McNeely, Clinton & Erbe, 2006; McNeely, Finlay & rated into plant biomass is derived from water. While Power, 2007). Here, we examined dD source separa- dD of precipitation may be highly variable over short tion through a combination of dD measurements of timescales, ground and surface water are more tem- archived samples previously analysed for d13C and porally integrated and show more dampened