Diets of Freshwater Turtles Often Reflect the Availability of Food Resources in the Environment

Herpetological Conservation and Biology 8(3):561−570. HerpetologicalSubmitted: 26 March Conservation 2013; Accepted: and Biology 21 October 2013; Published: 31 December 2013. RazoR-Backed Musk TuRTle (SternotheruS carinatuS) dieT acRoss a GRadienT of invasion carla l. atkinSon1,2, 3 1Oklahoma Biological Survey, 111 E. Chesapeake St., Norman, OK 73019 2Department of Biology and Ecology and Evolutionary Biology Graduate Program, University of Oklahoma, Norman, Ok 73019 3Present Address: Dept. of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca, NY 14853 e-mail: [email protected] abstract.—diets of freshwater turtles often reflect the availability of food resources in the environment. accordingly, bottom- feeding turtles’ diets are typically composed of benthic macroinvertebrate fauna (e.g., insects and mollusks). However, the composition of benthic systems has changed because many freshwater ecosystems have been invaded by non-native species, including bivalve species such as the asian clam, corbicula fluminea. i studied the diet of Sternotherus carinatus, the Razor- backed Musk Turtle, in southeastern oklahoma across three zones of corbicula abundances: no corbicula, moderate corbicula densities, and high corbicula densities. i hypothesized that the composition of corbicula in the diet would increase with increased abundance of corbicula in the riverine environment. Turtles were caught by snorkel surveys in the little and Mountain fork rivers and kept overnight for the collection of fecal samples. The diet was similar to that found in previous studies on S. carinatus except that corbicula is a new component of the diet and composed the majority of the diet in high-density corbicula areas. an index of Relative importance (iRi) showed that corbicula was the most important prey item in the areas with high corbicula density, was equally as important as gastropods in the areas with moderate corbicula density, and was absent from the diet in areas without corbicula. as indicated by a non-metric dimensional scaling ordination, the diet of turtles in the areas without corbicula was more diverse, containing insects, crayfish, gastropods, unionids, and seeds in high proportions. My data suggest that the diet of S. carinatus has become more molluscivorous and diet diversity has been reduced as the result of the presence of corbicula. Key Words.—Corbicula fluminea; invasive species; geographical informational systems (GIS); diet analysis; diet diversity; non- metric multidimensional scaling (NMDS); Oklahoma inTRoducTion large component of the biomass in many freshwater systems (McMahon 1982; Karatayev Diets of freshwater turtles often reflect the et al. 2005), but seem restricted to larger, more- availability of food resources in the environment. permanent bodies of water (Morgan et al. 2003; The diet of bottom-feeding turtles is typically Karatayev et al. 2005; Sousa et al. 2008). composed of the benthic macroinvertebrate Corbicula have been shown to influence nutrient fauna, which is often composed of both insects cycling (Atkinson et al. 2010), alter energy flows and mollusks (Ernst and Lovich 2009). (Hakenkamp et al. 2001; Sousa et al. 2008; However, many turtles exhibit some sort of Atkinson et al. 2011), change community selectivity, by often selecting for particular composition (Werner and Rothhaupt 2008), and resources (Mahmoud 1968; Ernst and Lovich potentially compete with or negatively impact 2009). The availability of certain food resources native unionid mussel assemblages (Leff et al. can also be highly influenced by aquatic invasive 1990; Cherry et al. 2005; Vaughn and Spooner species and can even lead to shifts in diet 2006). While the success of Corbicula is evident (Preston et al. 2012; Rush et al. 2012). For from their increasing abundance and expanding example, female map turtles (Graptemys spp.) distributions, their impact on food webs is poorly have been found to shift their diets to invasive understood (Vaughn and Spooner 2006). bivalves (Dreissena, Corbicula), thereby Additionally, previous research has shown that reducing dietary diversity (Lindeman 2006a, b; the invasion of Corbicula has likely Bulté and Blouin-Demers 2008). The full differentially influenced the feeding of benthic ecosystem repercussions of invasive bivalves to freshwater turtles (Lindeman 2006a; Wilhelm diet diversity and populations of higher trophic and Plummer 2012), thus it is important to study levels are not fully understood. various turtle species. The Asian Clam (Corbicula fluminea) invaded The Razor-backed Musk Turtle (Sternotherus many water bodies in the southeastern and carinatus) occurs in the deep waters of rivers, midwestern United States beginning in the 1950s streams, oxbow lakes, and swamps, but is a (McMahon 1982). Corbicula have become a relatively understudied turtle species (Ernst and Copyright © 2013. Carla Atkinson. All Rights Reserved. 561 Atkinson.—Sternotherus carinatus diets across an invasion gradient. Lovich 2009). The distribution of the S. richness and densities of native unionid mussels carinatus is restricted to the Gulf Coastal Plain (although distributions are patchy; Matthews et and the Ouachita Mountains in Alabama, al. 2005). During the study, all sites I snorkeled Arkansas, Louisiana, Mississippi, Oklahoma, for turtles were sampled qualitatively (visual and Texas (Ernst and Lovich 2009). snorkel searches) and several sites along a Sternotherus carinatus is considered a benthic- gradient were quantitatively sampled for feeding omnivore and has been reported to feed Corbicula presence in 0.25 m2 quadrats (Fig. 1). on insects, seeds, mollusks, crayfish, carrion, It is not clear when Corbicula invaded the aquatic vegetation, and amphibians (Tinkle system, but the first report in the Little River is 1958; Mahmoud 1968), but has been reported to from 1981 (USGS 2012). Turtles were collected favor mollusks (Mahmoud 1968). Additionally, primarily in a 68 km reach of the upper Little previous work has shown that body size can River, within which Corbicula was not recorded influence feeding preference in that mollusks in the uppermost 37 km, but became more oftentimes make up a small proportion or mass prevalent downstream (Fig. 1; mean 30 of younger turtles’ diets while adults feed more Corbicula m-2, range 6.4–63.4 m-2). heavily on mollusks as they get larger Additionally, turtles were collected in an 18 km (Lindeman 2006a; Ernst and Lovich 2009; reach of the Mountain Fork River in which Wilhelm and Plummer 2012). It is unclear Corbicula occurs at very high densities (Fig. 1; whether S. carinatus has shifted its diet in mean 130 Corbicula m-2, range 35.2–348 m-2). response to the introduction of Corbicula to river This allowed me to study the diet of S. carinatus systems, but a preference for Corbicula has been in areas with no Corbicula (upstream portion of reported in a closely related species, the Little River), areas with moderate densities Sternotherus odoratus (Wilhelm and Plummer of Corbicula (downstream portions of the Little 2012). There have been no diet studies to date River), and areas with high densities of on the species since the introduction of Corbicula (Mountain Fork River). Corbicula to the geographic range of S. Upon capture, I took standard morphometric carinatus. measurements and determined sex for all turtles. My objective was to describe the diet of S. For each capture location, I recorded the water carinatus in the streams of southeastern depth (nearest 0.1 m), substrate type (cobble, Oklahoma across a zone of Corbicula invasion gravel, boulder, etc.), and location (UTM and to determine if Corbicula has become a main coordinates). I kept turtles in tubs or buckets of component of the diet. Diet is often reflective of shallow water (~5 cm) overnight for fecal availability of a food resource (Krebs 1989), thus sample collection. I then filtered samples with a my study encompassed a range of sites that 250 µm sieve and stored in 95% ethanol included areas where Corbicula has not invaded (Demuth and Buhlmann 1997). I released and areas where Corbicula is present. Turtles sampled individuals at their sites of capture were captured in each of these habitats allowing within 48 h. I first sorted fecal samples into me to discern whether S. carinatus was feeding broad taxonomic categories and then identified on Corbicula and if S. carinatus has become items to the lowest classification (Lindeman more molluscivorous in the presence of 2007) possible under a Leica Wild M3Z Corbicula. In the spectrum of food web studies, dissecting microscope (Leica Microsystems, this study incorporates knowledge of an Buffalo Grove, Illinois, USA). I grouped items understudied species (Lindeman 2008) while into 8 categories: unionid mussels, Corbicula, incorporating concepts of invasive species gastropods, insects, crayfish, seeds, leaves, or ecology and ecosystem change. unidentifiable/other (primarily rocks, sand, and detrital material). Following separation of the MaTeRials and MeTHods groups, I dried each individual sample in a drying oven for 24 hours at 60° C and then I opportunistically collected turtles between determined the dry weight of each dietary item May 2011 and September 2012 during another to the nearest 0.0001 g. ongoing project in the Little and Mountain Fork rivers of southeastern Oklahoma, USA. The analyses.—To determine if there was a streams are located in the Ouachita Highland difference in the amount of Corbicula in the diets region and contain relatively

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