The Journal of North American Herpetology
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ISSN 2333-0694 JNAHThe Journal of North American Herpetology Volume 2014(1): 81-86 2 July 2014 jnah.cnah.org DISTRIBUTION, DIET, AND PREVALENCE OF AMPHIBIAN CHYTRID FUNGUS IN NON-NATIVE AMERICAN BULLFROGS (LITHOBATES CATESBEIANUS) AT THE VALENTINE NATIONAL WILDLIFE REFUGE, NEBRASKA, USA ALYX R. LINGENFELTER1, KEITH GELUSO1,4, MELVIN P. NENNEMAN2, BRIAN C. PETERSON1 AND JACOB L. KERBY3 1Department of Biology, University of Nebraska at Kearney, Kearney, Nebraska 68849 2Valentine National Wildlife Refuge, 39679 Pony Lake Road, Valentine, Nebraska 69201 3Department of Biology, University of South Dakota, Vermillion, South Dakota 57069 4Corresponding author: [email protected] ABSTRACT: American Bullfrogs (Lithobates catesbeianus) have been widely introduced beyond their na- tive range in North America and can negatively affect organisms in wetland environments via a suite of mechanisms including interspecific interactions and disease transmission. Bullfrogs were introduced to the Valentine National Wildlife Refuge in the Sandhill Region of Nebraska, USA, yet little is known regarding their distribution, abundance, and potential effects on other vertebrates in the Refuge. Surveys in 1991-1992 documented bullfrogs in only one lake by the Refuge headquarters, and an- ecdotal historical observations indicated that bullfrogs were present primarily in lakes open to public fishing. In 2012, we determined the distribution of bullfrogs across the Refuge, examined their diets, and sampled them for the occurrence of the pathogenic fungus, Batrachochytrium dendrobatidis. We documented that bullfrogs were almost ubiquitous across the Refuge lakes and wetlands. From diet analyses, we observed that adult bullfrogs consumed several vertebrate species on the Refuge including: a Blanding’s Turtle (Emydoidea blandingii), small bullfrogs, an unidentifiable frog species, and numerous invertebrates, including crayfish. The amphibian chytrid fungus was prevalent on the refuge with 73.7% of bullfrogs testing positive for the fungus in early June and 6.3% in late June-Ju- ly. Preliminary data indicate that bullfrogs likely have already affected interspecific interactions with native amphibians via predation, competition, and/or disease transmission. Bullfrogs likely cannot be eradicated from the Refuge, but expanding the season of harvest of bullfrogs might reduce their abundance, which may benefit native amphibians and reptiles. INTRODUCTION bullfrog introductions include consumption of other ver- American Bullfrogs (Lithobates catesbeianus; hereafter, tebrate species (Bury and Whelan, 1984; Krupa, 2002), bullfrogs) originally were native to southern and east- interspecific competition (Kiesecker et al., 2001), and in- ern North America, but the species has been widely in- creased occurrence and transmission of the amphibian troduced throughout western and northern parts of the chytrid fungus (Batrachochytrium dendrobatidis; Lawl- United States (Bury and Whelan, 1984; Ficetola et al., er et al., 1999; Bai et al., 2010). For example, North- 2007). The exact western limits of its native distribution ern Leopard Frogs (Lithobates pipiens) appear to have are not well understood across the Great Plains. In Ne- been dramatically impacted by bullfrogs in western parts braska, for example, bullfrogs are suspected to be native of North America (Hammerson, 1982; Johnson et al., only to eastern parts of the state in river-bottoms and 2011). Furthermore, in Ontario, Canada, Hecnar and Mc- river oxbows (McAuliffe, 1978; Fogell, 2010). Purpose- Closkey (1997) demonstrated that when bullfrogs were ful and accidental releases beyond its native range in eradicated from an area, populations of other amphibi- North America have caused major changes to ecosys- ans increased, in part, due to predator release. Bullfrogs tems worldwide where they now occur (Moyle, 1973; have been included in the list of the 100 worst invasive Kats and Ferrer, 2003; see Kraus, 2009). Some effects of species worldwide (Lowe et al., 2000; Crayon, 2009). Journal of North American Herpetology 2014(1) 81 Understanding the potential role of non-native bullfrogs times each on the belly, thighs, and feet (Fisherfinest in the decline of native amphibians is important because Transport Swabs, Fisher Scientific Inc., Pittsburgh, PA, native amphibians are often vital components in both USA). Swabs were air dried and then stored on ice or in terrestrial and aquatic ecosystems (Whiles et al., 2006). freezers until placed on dry ice and sent to the laboratory In addition, many amphibian species are experiencing for testing. Contamination between frogs was limited by declines due to the emergence of the amphibian chy- wearing vinyl gloves and changing them for each indi- trid fungus Batrachochytrium dendrobatidis (Berger et vidual handled. We released most bullfrogs at sites of al., 1998; Daszak et al., 1999; Skerratt et al., 2007). capture. The amphibian chytrid fungus causes hyperkeratosis, a In the laboratory, we extracted DNA from the swab sam- skin infection that creates erosions and, sometimes, ul- ples using Qiagen DNEasy spin columns and then ran a cerations on the epidermis (Berger et al., 1998; Bosch et Taqman based fast qPCR (Quantitative Polymerase Chain al., 2001). Death may ensue due to osmotic imbalance Reaction) assay to determine the presence or absence which leads to heart dysfunction (Voyles et al., 2009). Al- of the chytrid fungus (Kerby et al., 2013). Samples were though many amphibians appear susceptible to the dis- run in triplicate with both negative and positive controls ease, bullfrogs normally do not show symptoms (Daszak per plate. Samples were designated as positive for the et al., 2004) and are considered carriers, likely having a amphibian chytrid fungus if a minimum of 2/3 samples in role in sustaining the fungus at sites and in transmission each triplicate were positive. Samples with only a single of the fungus to other species (Hanselmann et al., 2004; positive result were rerun and determined to be positive Garner et al., 2006). However, Gervasi et al. (2013) re- if at least one of the subsequent triplicate was positive. cently suggested that bullfrogs also can succumb to ch- After swabbing bullfrogs in late July, 15 bullfrogs were ytridiomycosis depending on the strain of the amphibian collected for dietary analyses from Pelican and Dewey chytrid fungus that they are exposed to and the number lakes. Larger bullfrogs (≥ 100 mm snout-vent length) of zoospores that are present at this exposure. were chosen to facilitate the potential for finding recently To date, little is known about the distribution or eco- metamorphosed frogs in their stomach. Bullfrogs were logical effects of bullfrogs at the Valentine National Wild- placed in a container filled with a low dose (approxi- life Refuge, Nebraska, USA (Corn et al., 1995; hereafter, mately 1%) Tricaine-S (Western Chemical Inc., Ferndale, the Refuge). In a herpetofaunal survey at the Refuge WA, USA) in water for anesthetization, then, they were in 1991-1992, Corn et al. (1995) documented bullfrogs euthanized by exposing them to a lethal concentration only at Hackberry Lake. In a comprehensive resurvey of of Tricaine-S. Twelve additional stomach samples were the Refuge in 2012, we provide an update on the dis- obtained from frogs captured by fisherman on Dewey tribution of bullfrogs, in addition to investigating their Lake at the Refuge in August 2012. Frogs were placed diet and prevalence of the amphibian chytrid fungus in in individually labeled water-proof bags and frozen for the species. Because bullfrogs are known to consume stomach analyses in the laboratory. We identified prey to numerous prey species, including other species of frogs lowest identifiable taxonomic determination and reported (Bury and Whelan, 1984), we were interested in exam- number of prey items in stomachs, number of frogs that ining whether bullfrogs directly affect native amphibians consumed prey items, and percentage of frog stomachs via predation at the Refuge, specifically the Northern with specific prey items. Leopard Frog. Moreover, the amphibian chytrid fungus has recently been documented along the Platte River in RESULTS south-central Nebraska, but no documentation exists in Bullfrogs were observed in 33 of the 35 major lakes north-central parts of the state (Harner et al., 2011; Har- and marsh complexes throughout the refuge (Appendix ner et al., 2013). Because the Refuge is located in the 1), including all nine public fishing lakes. We did not ob- Sandhill Region of Nebraska, a rather pristine area of the serve bullfrogs inhabiting the two lakes farthest east on state with little urban or suburban land use, we predicted the Refuge (i.e., East Long and Crooked lakes) where that the fungus would be absent or have low prevalence human access is limited, although suitable frog habitat in amphibian populations (Johnson et al., 2011). was available. Lakes with bullfrogs, and the two without bullfrogs, had emergent vegetation around their edges MATERIALS AND METHODS including bulrushes (Scirpus spp.), cattails (Typha spp.), We surveyed for bullfrogs in June and July 2012 and common reed (Phragmites spp.). We also docu- throughout the Valentine National Wildlife Refuge, Cher- mented bullfrogs in stock tanks with vegetation. At most ry County, in north-central Nebraska, USA, to deter- lakes with bullfrogs, we failed to detect Northern Leopard mine their distribution. Survey sites included all major Frogs during our brief surveys, but we observed