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Using Stable Isotopes and C:N Ratios to Examine the Life‐History

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Using Stable Isotopes and C:N Ratios to Examine the Life‐History Journal of Fish Biology (2016) 88, 638–654 doi:10.1111/jfb.12858, available online at wileyonlinelibrary.com Using stable isotopes and C:N ratios to examine the life-history strategies and nutritional sources of larval lampreys T. M. Evans* and J. E. Bauer The Ohio State University Aquatic Biogeochemistry Lab., Department of Evolution, Ecology, and Organismal Biology, The Ohio State University, 300 Aronoff Laboratory, 318 W. 12th Avenue, Columbus, OH 43210-1293, U.S.A. (Received 15 June 2015, Accepted 5 November 2015) Natural abundance stable-isotope analysis (13Cand15N) and C:N ratios were used to study the ammocoete phase of two common non-parasitic lamprey species (least brook lamprey Lampetra aepyptera and American brook lamprey Lethenteron appendix) in two tributaries of the Ohio River (U.S.A.). The C:N ratios suggest that each species employs different lipid accumulation strategies to support its metamorphosis and recruitment into an adult animal. Ammocoete 13C values generally increased with increasing C:N values. In contrast to 13C, ammocoete 15N values were weakly related to the total length (LT)inL. aepyptera, but positively correlated to both LT and C:N ratios in L. appendix.InL. appendix, C:N also correlated positively with LT, and presumably age. A Bayesian mixing model using 13Cand15N was used to estimate nutritional subsidies of different potential food resources to ammocoetes at each site. The models suggested that although nutritional subsidies to ammocoetes varied as a function of site, ammocoetes were generally reliant on large contributions (42–62% at three sites) from aquatic plants. Contributions from aquatic sediment organic matter were also important at all sites (32–63%) for ammocoetes, with terrestrially derived plant materials contributing smaller amounts (4-33%). These findings provide important insights into the feeding ecology and nutrition of two species of lampreys. They also suggest that similar and other quantitative approaches are required to (1) fully understand how the observed stable-isotopes ratios are established in ammocoetes and (2) better assess ammocoete nutritional subsidies in different natal streams. © 2015 The Fisheries Society of the British Isles Key words: ammocoetes; Lampetra aepyptera; Lethenteron appendix;MixSIR. INTRODUCTION Lampreys (Order: Petromyzontiformes) are an ancient group of jawless fishes with a complex life history. As a result, many populations of lampreys are currently threatened by anthropogenic activities that have degraded habitat for all life stages and impeded the migration of juveniles and adults (Renaud, 1997; Close et al., 2002; Mesa & Copeland, 2009). Larval lampreys (i.e. ammocoetes) may be particularly vulnerable to human activities, in part because of their extended residence time filter feeding in low-flow sandy or silty sections of the stream bed (Potter, 1980; Potter et al., 1986; Mundahl *Author to whom correspondence should be addressed at present address: State University of New York, Col- lege of Environmental Science and Forestry, 144 Illick Hall, 1 Forestry Drive, Syracuse, NY 13210, U.S.A. Tel.: +1 215 692 2027; email: [email protected] 638 © 2015 The Fisheries Society of the British Isles STABLE-ISOTOPE ANALYSIS OF AMMOCOETES 639 et al., 2005). Although considerable interest has developed in lamprey conservation (Renaud, 1997; Close et al., 2002), numerous questions about ammocoete biology and ecology remain, including the nutritional sources that support ammocoetes as they develop. The importance of the ammocoete stage to lamprey life cycles and the abil- ity of humans to influence lamprey populations are high during the larval stage. A more quantitative understanding of the food sources supporting ammocoete growth and recruitment is still needed. Prior dietary studies of ammocoetes have focused on gut-content analysis and have concluded that algae are important for nutrition (Sutton & Bowen, 1994; Yap & Bowen, 2003; Mundahl et al., 2005). Ammocoete gut content is primarily composed of amor- phous detritus (Sutton & Bowen, 1994); however, this is difficult to categorize as to its ultimate sources, and as such the original starting material contributing to ammocoete growth remains debatable. Natural abundance isotopes represent a potential approach for assessing the types of organic matter (OM) supporting ammocoete somatic growth and energetic maintenance. Naturally occurring isotopes of C and N in organic materi- als may be used to trace these elements from their potential food sources to organisms, food webs and even ecosystems, provided the relative abundance of each isotope can be measured in both the relevant potential food sources and the target organisms (Peterson & Fry, 1987; Post, 2002; Cole et al., 2011). In biological systems, the lighter isotope of an element is processed at the enzymatic level to a slightly greater extent than the heav- ier isotope due to mass-dependent effects, resulting in isotopic fractionation (Hoefs, 2004). Therefore, fractionation results in more of the lighter isotope of a given element being lost (i.e. depleted) during respiration, and a greater relative retention (i.e. enrich- ment) of the heavier isotope within biomass. For example, 15N fractionates at c. 3‰ for each trophic level whereas 13C fractionates c. 1‰ per trophic level, although there is variation around these means (Peterson & Fry, 1987). Natural abundance stable iso- topes may therefore provide insight to both the trophic level and the food sources of an organism or population. Because biological systems cause fractionation during the use of various elements, the stable-isotope ratios in organisms can be different and tracked through consumers that depend on these organisms. For instance, stable-isotope ratios of terrestrial plants 13 usually have a Cofc. −28‰ in C3 plants and c. −13‰ in C4 plants (Peterson & Fry, 1987). In contrast, the 15N values are more variable, but are usually c. 0‰ in both groups of plants (Peterson & Fry, 1987). Although a consumer’s dependence on C3 or 15 C4 plants could not be distinguished with N, because both sources are identical, the use of 13C could distinguish the percentage contribution from each food source to the animal. Prior work on lampreys with stable isotopes has provided important insights into their feeding ecology, but has primarily targeted parasitic juveniles and adults (Adams et al., 2008; Harvey et al., 2008; Inger et al., 2010). For example, work in the Laurentian Great Lakes suggested that juvenile sea lamprey Petromyzon marinus L. 1758 feeding was more locally influenced because dispersal was more limited than initially thought (Harvey et al., 2008). Work on anadromous populations of P. marinus has shown that the biomass of spent adults provides marine-derived carbon (C) and nutrients to local streams after spawning (Weaver et al., 2015). Inger et al. (2010) also used stable iso- topes to determine whether non-native fish species were supporting native lamprey populations, and if lamprey populations were migratory. These authors found that a freshwater parasitic population fed primarily on brown trout Salmo trutta L. 1758 and © 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, 88, 638–654 640 T. M. EVANS AND J. E. BAUER common bream Abramis brama (L. 1758) within the local water body instead of migrat- ing to the ocean. Isotopes have also suggested that differences in the size of adult lam- prey are probably because of differences in feeding strategies and growth of juveniles (Adams et al., 2008). It is similarly predicted that the time to maturation in ammocoetes of different species and populations of lampreys is also controlled by differences in larval food resources, but ammocoete diets have not been the target of stable-isotope studies, although this life stage is critical for recruitment and maintenance of lamprey populations. Stable-isotope analysis simultaneously provides estimates of the C:N ratio of the sample. The C:N ratios of aquatic animals (including many fish species) have been used as a proxy for estimating lipid content in a broad range of consumer organisms (Post et al., 2007). Lipid content is important in controlling ammocoete metamorphosis (Moore & Potter, 1976; O’Boyle & Beamish, 1977), although not the only factor (e.g. temperature and photoperiod) (Manzon et al., 2015). Lampreys use one of two strate- gies to accumulate lipids to complete metamorphosis (Hardisty, 2011). In one strategy, lipid levels are maintained at low levels until an ammocoete approaches its maximum size, at which point it ceases significant growth in length and rapidly accumulates lipids. If the animal fails to reach a lipid threshold before the end of the growing season, it maintains its lipid levels and will attempt to increase them the following year (O’Boyle & Beamish, 1977) (the all-or-none strategy). The other documented strategy has ani- mals accumulating lipids annually without depleting them to initial levels. As a result, the following year’s initial lipid level is always higher than the previous year. Lipid accumulation continues until lipid levels reach levels high enough for metamorphosis to occur (Moore & Potter, 1976) (the rising-tide strategy; Hardisty, 2011). Whether these strategies are specific to a given species is currently unclear, and more work is required to determine how variable these life histories are in lamprey populations. In this study, ammocoete tissues and their potential nutritional sources were exam- ined using natural
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