doi:

DOI: 10.3724/SP.J.1245.2014.00245

Asian Herpetological Research 2014/5:4 PP.245-254

Can an Invasive Prey Species Induce Morphological and Behavioral Changes in an Endemic Predator?Evidence from a South Korean Snake(Oocatochus rufodorsatus)


Abstract:
Introduction of an invasive prey species into an ecosystem may affect an endemic predator's fitness by altering the prey-predator system. Successful adaptation may allow the endemic predator to eat and control the invasive species, while unsuccessful adaptation may result in extinction of the predator. We examine the possible effects of the invasive North American bullfrog(Rana [Lithobates] catesbeiana) on the endemic Red-backed rat snake(Oocatochus rufodorsatus) in South Korea. We do so by comparing the morphology and behavior of adult and hatchling snakes from bullfrog-exposed(Taean) and bullfrog-unexposed(Hongcheon) populations. Among the seven morphological characteristics investigated, relative tail length(tail length/snout-vent length) of both adults and hatchlings from Taean was significantly greater than that of adults and hatchlings from Hongcheon. Also, adult snakes from Taean had a significantly shorter latency of first tongue flick in response to prey compared to adults from Hongcheon. This difference was not observed in hatchlings. In other snake species, a longer relative tail length and shorter latency of first tongue flick are known to improve foraging efficiency, and these characters may be adaptations of O. rufodorsatus to prey on bullfrogs. This study provides preliminary evidence that the presence of an invasive prey species may cause morphological and behavioral changes in an endemic predator.

Key words:invasive prey,bullfrog,Rana catesbeiana,Oocatochus rufodorsatus,predator response

ReleaseDate:2015-03-27 09:32:50



Anson J. R., Dickman C. R., Boonstra R., Jessop T. S. 2013. Stress triangle: Do introduced predators exert indirect costs on native predators and prey? PLoS ONE, 8: e60916.doi:10.1371/journal.pone.0060916

Aubret F., Bonnet X., Maumelat S. 2005. Tail loss, body condition and swimming performances in Tiger snakes, Notechis ater occidentalis. J Exp Zool, 303A: 894-903

Aubret F., Shine R., Bonnet X. 2004. Evolutionary biology: adaptive developmental plasticity in snakes. Nature, 431: 261-262

4Strayer D. L. 2012. Eight questions about invasions and ecosystem functioning. Ecol Lett, 15: 1199-1210

Brodie III E. D., Brodie Jr E. D. 1999. Costs of exploiting poisonous prey: Evolutionary trade-offs in a predator-prey arms race. Evolution, 53: 626-31

Burghardt G. M., Abeshaheen J. P. 1971. Response to chemical stimuli of prey in newly hatched snakes of the genus Elaphe. Anim Behav, 19:486-489

Carlsson N. O., Sarnelle O., Strayer D. L. 2009. Native predators and exotic prey-an acquired taste? Front Ecol Environ, 7: 525-532

Case T. J., Bolger D. T. 1991. The role of introduced species in shaping the distribution and abundance of island reptiles. Evol Ecol, 5: 272-290

Choi D. S., Ko S. K., Chung H. H. 1998. Report on the use of and on the ecological characteristics and capture of American Bullfrogs. Gwacheon, South Korea: Ministry of Environment of Korea (In Korean)

Chung M. H. 2005. Factors involved in the decline of the Bullfrogs, Rana catesbeiana. Gwacheon, South Korea: Ministry of Environment of Korea (In Korean)

Clark Jr D. R. 1966. Notes on sexual dimorphism in tail-length in American snakes. Trans Kans Acad Sci, 69: 226-232

Cooper Jr W. E., Burghardt G. M. 1990. A comparative analysis of scoring methods for chemical discrimination of prey by squamate reptiles. J Chem Ecol, 16: 45-65

Cooper Jr W. E. 1994. Chemical discrimination by tongue-flicking in lizards: a review with hypothesis on its origin and its ecological and phylogenetic relationships. J Chem Ecol, 20:439-487

Cowles R. B., Phelan R. L. 1958. Olfaction in rattlesnakes. Copeia, 1958: 77-83

Da Silva E. T., Filho O. P. R. 2009. Predation on juveniles of the invasive American Bullfrog Lithobates catesbeianus (Anura, Ranidae) by native frog and snake species in South-eastern Brazil. Herpetol Notes, 2: 215-218

Da Silva E. T, Filho O. P. R., Feio R. N. 2011. Predation of native anurans by invasive Bullfrogs in Southeastern Brazil: spatial variation and effect of microhabitat use by prey. S Amer J Herpetol, 6: 1-10

De Rivera C. E., Ruiz G. M., Hines A. H., Jivoff P. 2005. Biotic resistance to invasion: native predator limits abundance and distribution of an introduced crab. Ecology, 86: 3364-3376

Gurevitch J., Padilla D. K. 2004. Are invasive species a major cause of extinctions? Trends Ecol Evol, 19: 470-474

Halpern M. 1992. Nasal chemical senses in reptiles: structure and function. Pp. 423-523 In Gans C., Crews D. (Eds.),Biology of the Reptilia, Vol. 18, Physiology E: Hormones, Brain, and Behavior. Chicago: University of Chicago Press, 423-523

Harley C. D. G., Anderson K. M., Lebreton C. A. M., MacKay A., Ayala-Díz M., Chong S. L., Pond L. M., Amerongen Maddison J. H., Hung B. H. C., Iverson S. L., Wong D. C. M. 2013. The introduction of Littorina littorea to British Columbia, Canada: potential impacts and the importance of biotic resistance by native predators. Mar Biol, 160: 1529-1541

Heinonen K. B., Auster P. J. 2012. Prey selection in crustacean-eating fishes following the invasion of crab Hemigrapsus sanguineus in a marine temperate community. J Exp Mar Biol Ecol, 413: 177-183

Hirai T. 2004. Diet composition of introduced bullfrog Rana catesbeiana the Mizorogaike pond of Kyoto, Japan. Ecol Res, 19: 375-380

Hongcheon. 2012. Hongcheon statistical yearbook. Hongcheon County, Kangwon Province, South Korea; Hongcheon County (In Korean)

Jancowski K., Orchard S. A. 2013. Stomach contents from invasive American Bullfrogs Rana catesbeianus (Lithobates catesbeianus) on southern Vancouver island, British Columbia, Canada. Neo Biota, 16: 17-37

Jang H. J., Suh J. H. 2010. Distribution of amphibian species in South Korea. Korean J Herpetol, 2: 45-51(In Korean)

Jang M. H., Koo K. S., Song J. Y. 2011. The list of amphibian species in 66 islands in Korea. Korean J Herpetol, 3: 19-24 (In Korean)

Ji X., Xie Y. Y., Sun P. Y., Zheng X. Z. 1997.Sexual dimorphism and female reproduction in a viviparous snake, Elaphe rufodorsata. J Herpetol, 31: 420-422

Johnson M. T. J., Agrawal A. A. 2003.The ecological play of predator-prey dynamics in an evolutionary theatre. Trends Ecol Evol, 18: 549-591

Kang Y. S., Yoon I. B. 1975. Illustrated encyclopedia of fauna and flora of Korea, Vol.17, Amphibia-Reptilia. Seoul, South Korea: Samhwa Publisher (In Korean)

Kang E. J., Youn C. H. 1994.The settlement and distribution of the introduced Bullfrog, Rana catesbeianus, in Korea. Korean Assoc Conserv Nat, 13: 231-250 (In Korean)

Kiesecker J. M., Blaustein A. R., Miller C. L. 2001. Potential mechanisms underlying the displacement of native Red-legged frogs by introduced Bullfrogs. Ecology, 82: 1964-1970

Kim H. K. 1972. Biology of the Bullfrog (Rana catesbeiana).J Korean Res Ins Better Living (Ewha Womans University), 8: 67-92 (In Korean)

Kim H. S., Ko S. K. 1998. Distribution, food habit and seasonal cycles of germ cell activity in the introduced Bullfrog, Rana catesbeianus in Korea. FRI J Forest Sci, 57: 165-177 (In Korean)

King R. B. 1986. Population ecology of the Lake Erie water snakes, Nerodia sipedon insularum. Copeia, 1986: 757-772

King R. B. 2002. Predicted and observed maximum prey size-snake size allometry. Funct Ecol, 16: 766-772

King R. B., Ray J. M., Stanford K. M. 2006. Gorging on gobies: beneficial effects of alien prey on a threatened vertebrate. Can J Zool, 84: 108-15

Kishida O., Mizuta Y., Nishimura K. 2006. Reciprocal phenotypic plasticity in a predator-prey interaction between larval amphibians. Ecology, 87: 1599-1604

Labra A., Beltrán S., Niemeyer H. M. 2001.Chemical exploratory behavior in the lizard Liolaemus bellii. J Herpetol, 35: 51-55

Langkilde T. 2009. Invasive fire ants alter behavior and morphology of native lizards. Ecology, 90: 208-217

Lee H.J., Lee J.H., Park D. 2011. Habitat use and movement patterns of the viviparous aquatic snake, Oocatochus rufodorsatus, from Northeast Asia. Zool Sci, 28: 593-599

Li Y., Ke Z., Wang S., Smith G. R., Liu X. 2011a. An exotic species is the favorite prey of a native enemy. PLoS ONE, 6(9): e24299. doi:10.1371/ journal.pone.0024299

Li Y., Zhunwei K. E., Wang Y., Blaackburn T. M. 2011b. Frog community responses to recent American Bullfrog invasions. Curr Zool, 57: 83-92

Lima S. L. 2002. Putting predators back into behavioral predator-prey interactions. Trends Ecol Evol, 17: 70-75

Llewelyn J., Schwarzkopf L., Phillips B. L., Shine R. 2013. After the crash: how do predators adjust following invasion of a novel toxic prey type? Austral Ecol, doi:10.1111/aec.12058

Lowe S., Browne M., Boudjelas S., De Poorter M. 2000.100 of the world's worst invasive alien species a selection from the global invasive species database. The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN).

Mittelbach G. G., Osenberg C. W., Wainwright P. C. 1999. Variation in feeding morphology between pumpkinseed populations: phenotypic plasticity or evolution? Evol Ecol Res, 1: 111-128

Mushinsky H. R., Lotz K. H. 1980. Chemoreceptive responses of two sympatric water snakes to extracts of commonly ingested prey species. J Chem Ecol, 6: 523-535

Nuismer S. L., Thompson J. N. 2006.Coevolutionary alternation in antagonistic interactions. Evolution, 60: 2207-2217

Oh H. S., Hong C. 2007. Current conditions of habitat for Rana catesbeianus and Trachemys scripta elegans imported to Jeju-do, including proposed management plans. Korean J Env Eco, 21: 311-317 (In Korean)

Phillips B. L., Shine R. 2004. Adapting to an invasive species: toxic cane toads induce morphological change in Australian snakes. Proc Natl Acad Sci USA, 101: 17150-17155

Phillips B. L., Shine R. 2006. An invasive species induces rapid adaptive change in a native predator: Cane toads and Black snakes in Australia. P R Soc B, 273: 1545-1550

Pothoven S. A., Madenjian C. P. 2008. Changes in consumption by alewives and lake Whitefish after Dreissenid mussel invasion in lakes Michigan and Huron. N Am J Fish Manag, 28: 308-320

Preacher K. J. 2001. Calculation for the chi-square test: an interactive calculation tool for chi-square tests of goodness of fit and independence . Available from http://quantpsy.org.

Preacher K. J., Briggs N. E. 2001. Calculation for Fisher's exact test: an interactive calculation tool for Fisher's exact probability test for 2 x 2 tables . Available from http://quantpsy.org

Ra N. Y., Park D., Cheong S., Kim N. S., Sung H. C. 2010. Habitat associations of the endangered Gold-spotted pond frog (Rana chosenica). Zool Sci, 27: 396-401

Saviola A. J., Lamoreaux W. E., Opferman R., Chiszar D. 2011. Chemosensory response of the threatened Eastern indigo snake (Drymarchon couperi) to chemical and visual stimuli of Mus musculus. Herpetol Conserv Biol, 6: 449-454

Strauss S. Y., Lau J. A., Carroll S. P. 2006. Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol Lett, 9: 357-374

Suarez A. V., Case T. J. 2002. Bottom-up effects on persistence of a specialist predator: ant invasions and Horned lizards. Ecol Appl, 12: 291-298

Suh J. H. 2005. Natural resource survey in Taean coastal national park: Herpetofauna. Seoul: Korea National Park Research Institute (In Korean)

Sung H. C., Kim S. K., Cheong S. W., Park S. R., Roh D. C., Baek K. W., LeeJ. H., Park D. 2006.Estimating detection probabilities and site occupancy rates of three anuran species using call surveys in Haenam Gun. Korean J Ecol Field Biol, 29: 331-335

Taean. 2013. Taean statistical yearbook. Taean County, Chungnam Province, South Korea; Taean County (In Korean)

Vellend M., Harmon L. J., Lockwood J. L., Mayfield M. M., Hughes A. R., Wares J. P., Sax D. F. 2007. Effects of exotic species on evolutionary diversification. Trends Ecol Evol, 22: 481-488

Wang Y. P., Guo Z. W., Pearl C. A., Li Y. M. 2007. Body size affects the predatory interactions between introduced American Bullfrogs Rana catesbeianus and native anurans in China: An experimental study. J Herpetol, 41: 514-520

Wanger T. C., Wielgoss A. C., Motzke I., Clough Y., Brook B. W., Sodhi N. S., Tschamtke T. 2011. Endemic predators, invasive prey and native diversity. P R Soc B, 278: doi: 10.1098/rspb.2010.1512

Wu Z., Li Y., Wang Y., Adams M. J. 2005. Diet of introduced Bullfrogs Rana catesbeianus: predation on and diet overlap with native frogs on Daishan island, China. J Herpetol, 39: 668-674

Zar J. H. 1999. Biostatistical analysis. Upper Saddle River, NJ, USA: Prentice Hall