Stable isotopes in subtidal food webs: Have enriched carbon ratios in benthic consumers been misinterpreted?

We examined the hypothesis that the d13C of benthic consumers is depleted in offshore, deeper waters where kelp and benthic microalgae are absent by conducting three analyses: (1) we analyzed d13C (and d15N) of consumers along a nearshore–offshore gradient in the field, (2) we analyzed d13C (and d15N) of consumers placed in cages at various depths and distances from shore, and (3) we reexamined published stable isotope values for consumers taken at various depths from studies around the world. In all three situations, we did not observe the predicted change in d13C values of benthic consumers. In both the literature and in our field measurements, the d13C values for consumers were on average separated from the values for suspended particulate organic matter by 4%, irrespective of depth, indicating that factors other than the feeding on 13C-rich benthic primary producers may explain the enriched carbon ratios in benthic consumers (e.g., selective feeding on enriched particles). The hypothesis that the high d13C ratio in suspension and deposit feeders reflects feeding on benthic primary producers is thus tenuous and requires further investigation. In coastal temperate and polar oceans, there exist three potentially important sources of primary production: phytoplankton, kelp, and benthic microalgae (microphytobenthos). Although it is generally acknowledged that phytoplankton are the main food source available to benthic consumers, productivity measurements suggest that kelp and benthic microalgae may also be an important food source. Kelps are among the most productive plants on the planet, and up to 90% of their net production may end up as detritus (Mann 1988), which can be ingested by suspension and deposit feeders (Duggins and Eckman 1997). In a review of benthic microalgae productivity measurements in coastal ecosystems, Cahoon (1999) showed that they also can markedly contribute to overall production in temperate regions (around 60 g C m22 yr21), even at depths of .20 m. For example, Glud et al. (2002) found that the net photosynthetic rate of benthic microalgae at depths ,30 m in a Greenland fjord was twofold greater than that of phytoplankton in overlying waters. Although certain studies have shown an increased growth rate of suspension feeders in the presence of kelp both in the field (Duggins et al. 1989) and in controlled feeding experiments (Duggins and Eckman 1997), direct evidence for the use of benthic algae by suspension and deposit feeders comes from the analysis of stable isotopes. Observations from more straightforward approaches, such as stomach content analyses, are difficult to obtain for these types of consumers. Marine primary producers typically have well-separated carbon isotope ratios, which are conserved in their respective consumers with an enrichment (i.e., an increase in heavy isotopes) ranging from 0.5% to 1.2% between trophic levels (Vander Zanden and Rasmussen 2001; McCutchan et al. 2003). In contrast, nitrogen isotope ratios are often similar in primary producers but are enriched by ,2.5% in herbivores and by 3.5% to 4.0% with further increases in trophic level (McCutchan et al. 2003). Consequently, carbon isotope ratios are mainly used to determine the sources of primary production, whereas nitrogen isotope ratios are used to identify the trophic level of organisms (Michener and Schell 1994). Kelp and benthic microalgae have a much heavier carbon isotopic ratio than phytoplankton because of the depletion of light carbon in the relatively thick boundary layer that develops around them, since they are attached to the bottom. Many studies have made use of this difference to evaluate the relative importance of the different benthic primary producers and phytoplankton in coastal food webs. Although most studies in subtidal systems focus on the importance of kelp (Duggins et al. 1989; Kaehler et al. 2000; Fredriksen 2003), a number also consider the importance of benthic microalgae (Takai et al. 2002; Kang et al. 2003). All of these studies show that most benthic consumers are rich in 13C, suggesting that benthic primary producers are major contributors to benthic food webs. They often appear to account for .50% of the carbon in benthic consumers. However, a few studies conducted in offshore waters, far removed from sources of kelp or benthic microalgae, also report enriched carbon ratios in benthic consumers (Fry 1988; Hobson et al. 1995). These observations suggest that 1 Corresponding author ([email protected]). Acknowledgments We are very grateful to Myles Thompson, Catherine Vallières, Isabelle Deschênes, Pierre Grondin, François Praira, JeanPhilippe Parent, Jean-Sébastien Roy, and Émilie Castonguay for their assistance with the field work, and to Ladd E. Johnson and Warwick F. Vincent for many good suggestions during the planning of the project and the preparation of the paper. We also thank Hugo Bourdages from Fisheries and Oceans Canada for his help in collecting offshore samples. We thank two anonymous reviewers for their constructive comments. This study was supported by an operating grant from the National Sciences and Engineering Research Council of Canada (NSERC) to J.H.H. and M.-O.N. received support from QuébecOcéan. Limnol. Oceanogr., 51(6), 2006, 2828–2836 E 2006, by the American Society of Limnology and Oceanography, Inc.