Abstract
Invasive species are a regional and global threat to biological diversity. In order to evaluate an invasive predator species’ potential to harm populations of native prey species, it is critical to evaluate the behavioral responses of all life stages of the native prey species to the novel predator. The invasion of the African clawed frog (Xenopus laevis) into southern California provides an opportunity to evaluate the predation risk and behavioral responses of native amphibians. We performed predation trials and explored prey behavioral responses to determine how this invasive predator may impact native amphibian populations using Pacific chorus frogs (Pseudacris regilla) as a representative native California prey species. We found that X. laevis will readily prey upon larval and adult life stages of P. regilla. Behavior trials indicated that both larval and adult P. regilla exhibit prey response behaviors and will spatially avoid the novel invasive predator. The results suggest that native anurans may have a redundant predator response in both the larval and adult life stages, which could reduce the predatory impact of X. laevis but also drive emigration of native amphibians from invaded habitat.
Similar content being viewed by others
References
Adams MJ, Pearl CA (2007) Problems and opportunities managing invasive bullfrogs. Is there any hope? In: Gherardi F (ed) Biological invaders in inland waters—profiles, distribution and threats. Springer, Dordrecht, pp 679–693
Amaral P, Rebelo R (2012) Diet of invasive clawed frog Xenopus laevis at Lage stream (Oeiras, W Portugal). Herpetol J 22:187–190
Bellard C, Cassey P, Blackburn TM (2016) Alien species as a driver of recent extinctions. Biol Lett 12:20150623
Bucciarelli GM, Blaustein AR, Garcia TS, Kats LB (2014) Invasion complexities: the diverse impacts of nonnative species on amphibians. Copeia 4:611–632
Crayon JJ (2005) Species account: Xenopus laevis. In: Lannoo MJ (ed) Amphibian declines: the conservation status of United States species, 1st edn. California, Berkeley, pp 522–525
Doak D, Kareiva P, Klepetka B (1994) Modeling population viability for the desert tortoise in the Western Mojave Desert. Ecol Appl 4:446–460
Faraone FP, Lillo F, Giacalone G, Valvo ML (2008) The large invasive population of Xenopus laevis in Sicily, Italy. Amphibia-Reptilia 29:405–412
Ferrari MCO, Wisenden BD, Chivers DP (2010) Chemical ecology of predator–prey interactions in aquatic ecosystems: a review and prospectus. Can J Zool 88:698–724
Fritts TH, Rodda GH (1998) The role of introduced species in the degradation of island ecosystems: a case history of Gaum. Ann Rev Ecol Syst 29:113–140
Gall BG, Mathis A (2010) Innate predator recognition and the problem of introduced trout. Ethology 116:47–58
Goldson SL, Bourdôt GW, Brockerhoff EG, Byrom AE, Clout MN, McGlone MS, Nelson WA, Popay AJ, Suckling DM, Templeton MD (2015) New Zealand pest management: current and future challenges. J R Soc N Z 45:31–58
Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190
Hammond JI, Luttbeg B, Sih A (2007) Predator and prey space use: dragonflies and tadpoles in an interactive game. Ecology 88:1525–1535
Hayes MP, Tennant MR (1985) Diet and feeding behavior of the California red-legged frog, Rana aurora draytonii (Ranidae). Southwest Nat 30:601
Herreid CF II, Kinney S (1966) Survival of Alaskan woodfrog (Rana sylvatica) larvae. Ecology 47:1039–1041
Hettyey A, Rölli F, Thürlimann N, Zuercher A, Van Buskirk J (2012) Visual cues contribute to predator detection in anuran larvae. Biol J Linn Soc 106:820–827
Hossie TJ, Ferland-Raymond B, Burness G, Murray DL (2010) Morphological and behavioral responses of frog tadpoles to perceived predation risk: a possible role for corticosterone mediation? Ecoscience 17:100–108
Innes J, Kelly D, Overton JC, Gillies C (2010) Predation and other factors currently limiting New Zealand forest birds. N Z J Ecol 34:86–114
Kats LB, Ferrer RP (2003) Alien predators and amphibian declines: review of two decades of science and the transition to conservation. Divers Distrib 9:99–110
Knapp RA, Matthews KR (2000) Non-native fish introductions and the decline of the mountain yellow-legged frog from within protected areas. Conserv Biol 14:428–438
Lillo F, Faraone FP, Valvo Lo M (2011) Can the introduction of Xenopus laevis affect native amphibian populations? Reduction of reproductive occurrence in presence of the invasive species. Biol Invasions 13:1533–1541
Lobos G, Jaksic FM (2005) The ongoing invasion of African clawed frogs (Xenopus laevis) in Chile: causes of concern. Biodivers Conserv 14:429–439
Lobos G, Measey GJ (2002) Invasive populations of Xenopus laevis (Daudin) in Chile. Herpetol J 12:163–168
Mack RN, Simberloff D, Lonsdale MW, Evans H, Clout M (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710
Mahrdt C, Knefler FT (1972) Pet or pest? The African clawed frog. Environ Southwest 446:2–5
Mandrillon A-L, Saglio P (2005) Prior exposure to conspecific chemical cues affects predator recognition in larval common toad (Bufo bufo). Arch Hydrobiol 164:1–12
Marquis O, Saglio P, Neveu A (2004) Effects of predators and conspecific chemical cues on the swimming activity of Rana temporaria and Bufo bufo tadpoles. Arch Hydrobiol 160:153–170
McCoid MJ, Fritts TH (1980) Notes on the diet of a feral population of Xenopus laevis (Pipidae) in California. Southwest Nat 25:272–275
Measey GJ (1998) Diet of feral Xenopus laevis (Daudin) in South Wales, UK. J Zool Lond 246:287–298
Measey GJ, Tinsley RC (1998) Feral Xenopus in South Wales. Herpetol J 8:23–27
Nunes AL, Richter-Boix A, Laurila A, Rebelo R (2012) Do anuran larvae respond behaviourally to chemical cues from an invasive crayfish predator? A community-wide study. Oecologia 171:115–127
Pearl CA, Adams MJ, Schuytema GS, Nebeker AV (2003) Behavioral responses of anuran larvae to chemical cues of native and introduced predators in the Pacific Northwestern United States. J Herpetol 37:572–576
Pease KM, Wayne RK (2013) Divergent responses of exposed and naive Pacific tree frog tadpoles to invasive predatory crayfish. Oecologia 174:241–252
Pope KL, Matthews KR (2002) Influence of anuran prey on the condition and distribution of Rana muscosa in the Sierra Nevada. Herpetologica 58:354–363
Rebelo R, Amaral P, Bernardes M, Oliveira J, Pinheiro P, Leitão D (2010) Xenopus laevis (Daudin, 1802), a new exotic amphibian in Portugal. Biol Invasions 12:3383–3387
Relyea RA (2001) Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82:523–540
Rieger JF, Binckley CA, Resetarits WJ (2004) Larval performance and oviposition site preference along a predation gradient. Ecology 85:2094–2099
Seale DB (1982) Obligate and facultative suspension feeding in anuran larvae: feeding regulation in Xenopus and Rana. Bio Bull 162:214–231
Sih A, Bolnick DI, Luttbeg B, Orrock JL, Peacor SD, Pintor LM, Preisser E, Rehage JS, Vonesh JR (2010) Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos 119:610–621
Skelly DK (1992) Field evidence for a cost of behavioral antipredator response in a larval amphibian. Ecology 73:704–708
Skelly DK, Werner EE (1990) Behavioral and life-historical responses of larval American toads to an odonate predator. Ecology 71:2313–2322
Tinsley RC, Kobel HR (1996) The biology of Xenopus. Oxford University Press, Oxford
Tinsley RC, McCoid MJ (1996) Feral Populations of Xenopus outside of Africa. In: Tinsley RC, Kobel HR (eds) The biology of Xenopus. Oxford University Press, Oxford, pp 81–93
Tinsley RC, Loumont C, Kobel HR (1996) Geographical distribution and ecology. In: Tinsley RC, Kobel HR (eds) The biology of Xenopus. Oxford University Press, Oxford, pp 35–56
Tinsley RC, Stott LC, Viney ME et al (2015) Extinction of an introduced warm-climate alien species, Xenopus laevis, by extreme weather events. Biol Invasions 17:3183–3195
Vonesh J, la Cruz De O (2002) Complex life cycles and density dependence: assessing the contribution of egg mortality to amphibian declines. Oecologia 133:325–333
Wiles GJ, Bart J, Beck RE, Aguon CF (2003) Impacts of the brown tree snake: patterns of decline and species persistence in Guam’s avifauna. Conserv Biol 17:1350–1360
Acknowledgements
This research benefitted from access by Sandy Hedrick and Friends of the Santa Clara River to Hedrick Ranch Nature Area where experiments were performed and African clawed frogs were collected. We also thank Mike Booth and Steve Howard of United Water Conservation District for providing access to collect African clawed frogs. Thank you to Scott Cooper and Steve Rothstein for their input and advice. Funding provided by the Coastal Fund, University of California, Santa Barbara (WIN13-13).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wilson, E.A., Dudley, T.L. & Briggs, C.J. Shared behavioral responses and predation risk of anuran larvae and adults exposed to a novel predator. Biol Invasions 20, 475–485 (2018). https://doi.org/10.1007/s10530-017-1550-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-017-1550-x