Relative importance of CO2 recycling and CH4 pathways in lake food webs along a dissolved organic carbon gradient

Terrestrial ecosystems export large quantities of dissolved organic carbon (DOC) to aquatic ecosystems. This DOC can serve as a resource for heterotrophic bacteria and influence whether lakes function as sources or sinks of atmospheric CO2. However, it remains unclear as to how terrestrial carbon moves through lake food webs. We addressed this topic by conducting a comparative lake survey in the northeastern U.S. along a gradient of terrestrial-derived DOC. We used naturally occurring carbon stable isotopes of CO2, particulate organic matter (POM), and crustacean zooplankton, as well as gas measurements and culture-independent assessments of microbial community composition to make inferences about the flow of terrestrial carbon in lake food webs. Stable isotope ratios of POM and zooplankton decreased with DOC and were often depleted in 13C relative to terrestrial carbon, suggesting the importance of an isotopically light carbon source. It has been proposed that the incorporation of biogenic methane (CH4) into plankton food webs would account for such trends in stable isotope ratios, but we found weak evidence for this hypothesis, on the basis of relationships of CH4, methanogenic archaebacteria, and methanotrophic bacteria in our lakes. Instead, our results are consistent with the view that phytoplankton increase their use of heterotrophically respired CO2 with increasing concentrations of terrestrialderived DOC. The effect of this CO2 recycling can be detected in the stable isotope composition of crustacean zooplankton, suggesting that the direct transfer of terrestrial DOC inputs to higher trophic levels may be relatively inefficient. Freshwater, estuarine, and marine ecosystems receive large inputs of terrestrial carbon in the form of dissolved organic carbon (DOC). In addition to altering numerous physical and chemical attributes, DOC has a strong influence on the metabolic functioning of aquatic ecosystems (Hanson et al. 2003). However, for a number of reasons, the flow of terrestrial-derived DOC in lake food webs is less clear. First, a large percentage (85–90%) of the total DOC pool is biologically recalcitrant (Søndergaard and Middelboe 1995), whereas the remaining percentage is restricted to consumption primarily by aquatic bacteria. Second, planktonic bacteria have relatively low growth efficiencies and respire 35–99% of consumed DOC as CO2 (del Giorgio and Cole 1998). Finally, terrestrial carbon flow in lake food webs may be influenced by the limited ability of some zooplankton functional groups to graze on DOC-subsidized bacteria (Jürgens 1994). Despite these trophic constraints, some studies report that .50% of the carbon in particulate organic matter (POM), zooplankton, and fish may ultimately be derived from terrestrial ecosystems (Grey et al. 2001; Pace et al. 2004; Carpenter et al. 2005). The DOC concentration in lakes varies across the landscape (Canham et al. 2004) and may influence the degree to which aquatic food webs are subsidized by terrestrial carbon. This hypothesis has been addressed using naturally occurring stable isotope ratios, with the prediction that zooplankton should converge upon the isotopic signature of terrestrial carbon with increasing concentrations of DOC (Jones et al. 1999). Zooplankton stable isotope ratios decrease with DOC concentration and also tend to be depleted in 13C relative to both POM and terrestrial-derived carbon (Jones et al. 1999; Karlsson et al. 2003). Although these observations reveal that DOC inputs 1 To whom correspondence should be addressed. Present address: W.K. Kellogg Biological Station and Department of Microbiology & Molecular Genetics, Michigan State University, Hickory Corners, MI 49060 ([email protected]).