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The Diet of the Eastern Musk Turtle (Sternotherus Odoratus) As It Pertains to Invasive Snail Consumption in a Freshwater Spring Habitat in Texas

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The Diet of the Eastern Musk Turtle (Sternotherus Odoratus) As It Pertains to Invasive Snail Consumption in a Freshwater Spring Habitat in Texas Herpetology Notes, volume 12: 1133-1139 (2019) (published online on 04 November 2019) The diet of the Eastern Musk Turtle (Sternotherus odoratus) as it pertains to invasive snail consumption in a freshwater spring habitat in Texas Madeleine Morrison1,2,*, Brian P. Butterfield3, Stephen G. Ross4, Chris Collins5, Andrew Walde1, Jordan Gray1, J. Brian Hauge6, and Eric C. Munscher1,7 Abstract. In this study we investigated the diet of the Eastern Musk Turtle (Sternotherus odoratus) in Comal Springs, a spring-fed lake system located in the Texas Hill Country. Due to high numbers of invasive snails in this system, we focused on consumption of invasive snails. The most abundant taxa present in the faecal samples were gastropods. In particular, three species of invasive snails, the Red-rimmed Melania (Melanoides tuberculata), the Quilted Melania (Tarebia granifera), and the Giant Ramshorn Snail (Marisa cornuarietis) were the most abundant items identified. We found fragments of M. tuberculata shells in the majority of the samples (77% male samples; 80% female samples; 78% total), opercula from M. cornuarietis in a smaller number of samples (20% male samples; 10% female samples; 16% total samples), and fragments of T. granifera shells in half of the faecal samples (50% male samples; 50% female samples; 50% total). No sexual difference in diet was apparent. Total consumption of molluscs was high relative to most other reports of S. odoratus diet. Our results suggest that the diet of S. odoratus in Comal Springs may have shifted towards focusing on the invasive snails as the result of a probable three-decade presence of these invasive species. Keywords. Sternotherus odoratus, Melanoides tuberculata, Marisa cornuarietis, Tarebia granifera, predation, invasive molluscs, Texas, Comal Springs, diet Introduction required to search for the prey item. Thus, a predator can maximise benefit relative to cost to increase its Foraging behaviours, including choice of diet, are fitness, which would be favoured by natural selection affected by a number of ecological factors. Some (Wermer and Hall, 1974). Therefore, we would expect predators consume prey items based on where they hunt in the ecosystem and thus are spatially constrained (Murdoch et al., 1974). Other predators choose from the available prey based on when they hunt and thus are temporally constrained (Elliot, 2004). However, in many cases predators eat whatever prey may be most 1 Turtle Survival Alliance, 1030 Jenkins Road, Suite D, common where and when they hunt. This results in Charleston, South Carolina 29407, USA. 2 prey switching, also known as frequency-dependent University of New England, 11 Hills Beach Road, Biddeford, Maine 04005, USA. predation, as abundance of prey changes over time 3 Freed-Hardeman University, 158 East Main Street, Henderson, (Allen, 1988). This strategy can become enhanced when Tennessee 38340, USA. the predator becomes better at utilising prey species over 4 Delta Land Services, 6750 West Loop South Suite 780, time (Berbelson, 1985). Factors other than frequency Bellaire, Texas 77401. can also influence whether a predator chooses one prey 5 SWCA Environmental Consultants, 4407 Monterey Oaks item over another, and these are the basis for optimal Blvd, Building 1, Suite 110, Austin, Texas 78749, USA. 6 foraging theory. Relevant factors include the amount of Department of Biology, Peninsula College, 1502 East Lauridsen Boulevard, Port Angeles, Washington 98362, energy gained from consuming a particular prey item USA. relative to the energy expended doing so, such as the: 7 SWCA Environmental Consultants, 10245 West Little York (1) cost of handling an item with a hard shell; (2) cost of Road, Suite 600, Houston, Texas 77040, USA. handling prey that is potentially dangerous; or (3) time * Corresponding author. E-mail: [email protected] 1134 Madeleine Morrison et al. a predator to maximise foraging benefits by switching a study in Oklahoma found snail remnants in 96% of S. to novel prey, such as invasive species, when these prey odoratus stomachs (Mahmoud, 1969). A similar study in items become abundant and provide large amounts a lake system in central Florida found that snails made of energy relative to cost. Over time, such a predator up 94% of the annual diet biomass for a population of S. may become more efficient at using the novel prey by odoratus (Bancroft et al., 1983). Lagler (1943) reported its individual phenotypic plasticity or the influence of snails and clams were the second most common food natural selection over generation time. Examples of this category and made up approximately 27% of their diet have been observed in multiple reptile species including by frequency of occurrence. In addition, Corbicula sp. the Red-Banded Snake (Dinodon rufozonatum), the were a substantial part of S. odortatus diet in Arkansas American bullfrog (Lithobates catesbeianus), and (Wilhelm and Plummer, 2012). numerous species of turtles (Li et al., 2011; King et al., Despite documentation of S. odoratus consuming 2006). invasive molluscs, there are limited accounts of this Accounts of native turtle species preying on exotic species consuming invasive gastropods (Morrison, species have been published previously. The Northern 2017). Our objective with this study is to describe the Map Turtle (Graptemys geographica) has incorporated diet of S. odoratus within a highly-altered freshwater Zebra Mussels (Dreissena polymorpha) into its diet spring environment where several invasive species, (e.g., Serrouya et al., 1996; Lindeman, 2006; Bulté and such as Red-rimmed Melania (Melanoides tuberculata), Blouin-Demers, 2008). Stable isotope analysis revealed Quilted Melania (Tarebia granifera), and Giant that this invasive prey constituted between 0% and Ramshorn Snail (Marisa cornuarietis) have established 14% of the diet in male G. geographica and between populations (Johnson et al., 2012; SWCA, 2018). 4% and 36% of the diet in females, creating estimates that this turtle population consumes approximately Material and Methods 3200 kg of D. polymorpha annually (Bulét and Blouin- Field Site.—Within the Comal Springs aquatic system, Demers, 2008). Other accounts of turtles preying upon our study site combines the 8.4-ha aquatic boundary of invasive species include the consumption of the Apple Landa Lake and a 1.77-km-long segment of the Comal Snail (Pomacea canaliculata) by four different species River, which feeds into it (Fig. 1). Thirteen boils that are of turtles, including the Red-Eared Slider (Trachemys linked to the Edwards Aquifer are scattered throughout scripta elegans), Chinese Softshell (Pelodiscus the lake providing an average supply of 726,799,000 l of sinensis), Chinese Pond Turtle (Mauremys reevesii), clear freshwater daily (Brune, 1981). Year-round water and the native Japanese Pond Turtle (M. japonica) in temperatures in the system range from approximately southern Japan (Yusa et al., 2006). Additionally, there 23.1–23.9°C, creating a consistent thermal boundary are numerous reports of invasive mollusc consumption (Brune, 1981). Despite these characteristics, some by Sternotherus sp. (Ford and Moll, 2004; Patterson anthropogenic changes arguably make the environment and Lindeman, 2009; Wilhelm and Plummer, 2012; less suitable for wildlife. The Comal River (Landa Atkinson, 2013). Lake) ecosystem is surrounded by residential housing, a The Eastern Musk Turtle (Sternotherus odoratus) has city golf course, a highly visited city park, and a heavily one of the largest geographic ranges of freshwater turtle used water park averaging close to one million visitors species in North America. The species occurs in a variety per year (Wade Tomlinson, City of New Braunfels, pers. of habitats such as swamps, streams, ponds, lakes, and comm.). Because of this urbanisation, the water’s edge freshwater spring systems (Newell, 2004; Ernst and is almost entirely bordered by concrete bulkheads and Lovich, 2009; Wilhelm and Plummer, 2012). Within reinforcements. these habitats, S. odoratus has a broad diet that includes arthropods, molluscs, fish, algae, seeds and other plant Data Collection.—Fifty adult S. odoratus were materials, and carrion (Mahmoud, 1968; Ford and Moll, randomly selected from among 189 individuals captured 2004; Wilhelm and Plummer, 2012; Munscher, 2016). as part of a mark-recapture study. These specimens were Several studies have shown that the diet of this captured during May 2017 by hand or with traps baited bottom-feeding omnivore typically includes high with buffalo fried chicken (Munscher et al., 2017). Of concentrations of gastropods and molluscs (Lagler, these individuals, 30 were males and 20 females. After 1943; Mahmoud, 1968; Mahmoud, 1969; Bancroft et morphometric measurements were obtained, each al., 1983; Wilhelm and Plummer, 2012). For example, turtle was placed into an individual plastic container The diet of the Eastern Musk Turtle as it pertains to invasive snail consumption 1135 Figure 1. Map of the Landa Lake study site. The figure depicts three representations of the study site, as well as an outline of the specific area sampled. Note the presence of residential homes to the north and east (the top right portion of the site), a golf course (along the southern edge of the site), and a highly used water park (to the southeast of the study site). containing 2.54 cm of tap water (Fig. 2). Containers using a Vertias M124A analytical balance (Hogentogler, were labelled with the individual specimen’s hard-mark Columbia, Maryland, USA), analysed
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