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Geographical variation in body size and sexual size dimorphism of introduced American bullfrogs in southwestern China

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An Erratum to this article was published on 29 October 2009

Abstract

Invasive species often exhibit geographical variations in life history traits that may allow them to successfully invade different environments. We investigated geographical variation in body size and sexual size dimorphism (SSD) of invasive bullfrogs in southwestern China, by sampling two breeding populations (descendants of a single source population) inhabiting sites at low (1,412 m, Shiping) and high (2,692 m, Luguhu) altitudes. Both populations exhibited significant SSD, with females larger than males. At high altitude, mean body size of both sexes and the degree of SSD were significantly reduced; the reduction in mean body size with increasing altitude was more pronounced in females, although not significantly so. Female bullfrogs also showed a significant decrease in average age at high altitude that may be a major factor related to this pattern; average age of male bullfrogs did not vary significantly with altitude. Growth rate of both sexes was also lower at high altitude. Our results provide the first evidence that introduced bullfrog’s exhibit geographical variation in morphology in invaded areas in response to different environments, likely due to changes in climate. Additional research is required to determine the mechanism of this variation (i.e., physiological or developmental plasticity, mortality rate, selective pressure) and most importantly, to evaluate the potential for variation in the impacts of introduced bullfrogs on native ecosystems in China.

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References

  • Adams MJ (1999) Correlated factors in amphibian decline: exotic species and habitat change in western Washington. J Wildl Manage 63:1162–1171

    Article  Google Scholar 

  • 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, The Netherlands, pp 679–693

    Chapter  Google Scholar 

  • Alcaraz C, Garcia-Berthou E (2007) Life history variation of invasive mosquitofish (Gambusia holbrooki) along a salinity gradient. Biol Conserv 139:83–92

    Article  Google Scholar 

  • Alexander JM, Edwards PJ, Poll M, Parks CG, Dietz H (2009) Establishment of parallel altitudinal clines in traits of native and introduced forbs. Ecol 90:612–622

    Article  Google Scholar 

  • Ashton KG (2002) Do amphibians follow Bergmann’s rule? Can J Zool 80:708–716

    Article  Google Scholar 

  • Ashton KG, Feldman CR (2003) Bergmann’s rule in nonavian reptiles: turtles follow it, lizards and snakes reverse it. Evolution 57:1151–1163

    PubMed  Google Scholar 

  • Becker T, Dietz H, Billeter R, Buschmann H, Edwards PJ (2005) Altitudinal distribution of alien plant species in the Swiss Alps. Perspect Plant Ecol 7:173–183

    Google Scholar 

  • Benejam L, Alcaraz C, Sasal P, Simon-Levert G (2008) Life history and parasites of the invasive mosquitofish (Gambusia holbrooki) along a latitudinal gradient. Biol Inv Online First. Available at: http://www.springerlink.com/content/a8927140mhrh7171/. Accessed 12 Aug 2009

  • Bergmann C (1847) Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Göttinger Studien 3:595–708

    Google Scholar 

  • Blackburn TM, Gaston KJ, Loder N (1999) Geographic gradients in body size: a clarification of Bergmann’s rule. Divers Distrib 5:165–174

    Article  Google Scholar 

  • Blanckenhorn WU, Demont M (2004) Bergmann and converse Bergmann latitudinal clines in arthropods: two ends of a continuum? Integr Comp Biol 44:413–424

    Article  Google Scholar 

  • Bohn T, Sandlund OT, Amundsen PA, Primicerio R (2004) Rapidly changing life history during invasion. Oikos 106:138–150

    Article  Google Scholar 

  • Boone MD, Semlitsch RD, Little EE, Doyle MC (2007) Multiple stressors in amphibian communities: effects of chemical contamination, bullfrogs, and fish. Ecol Appl 17:291–301

    Article  PubMed  Google Scholar 

  • Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789

    Article  Google Scholar 

  • Bruneau M, Magnin E (1980) Croissance, nutrition et reproduction des ouaouarons Rana catesbeiana Shaw (Amphibia Anura) des Laurentides au nord de Montreal. Can J Zool 58:175–183

    Article  Google Scholar 

  • Campbell T, Echternacht A (2003) Introduced species as moving targets: changes in body sizes of introduced lizards following experimental introductions and historical invasions. Biol Inv 5:193–212

    Article  Google Scholar 

  • Castanet J, Newman DG, Saintgirons H (1988) Skeletochronological data on the growth, age, and population-structure of the Tuatara, Sphenodon punctatus, on Stephens island and Lady-Alice island, New Zealand. Herpetologica 44:25–37

    Google Scholar 

  • Chen SZ (1993) Preliminary study on introduced frogs in China. Chin J zool 28(2):12–14

    Google Scholar 

  • Chen YH, Bi JF (2007) Biogeography and hotspots of amphibian species of China: implications to reserve selection and conservation. Curr Sci 92:480–489

    Google Scholar 

  • Daehler CC (2005) Upper-montane plant invasions in the Hawaiian islands: patterns and opportunities. Perspect Plant Ecol 7:203–216

    Article  Google Scholar 

  • Ficetola GF, Thuiller W, Miaud C (2007) Prediction and validation of the potential global distribution of a problematic alien invasive species––the American bullfrog. Divers Distrib 13:476–485

    Article  Google Scholar 

  • Gaston KJ, Blackburn TM (2000) Macroecology: pattern and process. Blackwell, Oxford

    Book  Google Scholar 

  • Gibbons MM, McCarthy TK (1983) Age determination of frogs and toads (Amphibia, Anura) from north-western Europe. Zool Scr 12:145–151

    Article  Google Scholar 

  • Govindarajulu P, Price WS, Anholt BR (2006) Introduced bullfrogs (Rana catesbeiana) in western Canada: has their ecology diverged? J Herpetol 40:249–260

    Article  Google Scholar 

  • Halliday TR, Verrell PA (1988) Body size and age in amphibians and reptiles. J Herpetol 22:253–265

    Article  Google Scholar 

  • Hänfling B, Kollmann J (2002) An evolutionary perspective of biological invasions. Trends Ecol Evol 17:545–546

    Article  Google Scholar 

  • Hemelaar A (1988) Age, growth and other population characteristics of Bufo bufo from different latitudes and altitudes. J Herpetol 22:369–388

    Article  Google Scholar 

  • Howard RD (1978a) Evolution of mating strategies in bullfrogs, Rana catesbeiana. Evolution 32:850–871

    Article  Google Scholar 

  • Howard RD (1978b) Influence of male-defended oviposition sites on early embryo mortality in bullfrogs. Ecology 59:789–798

    Article  Google Scholar 

  • Howard RD (1981) Sexual dimorphism in bullfrogs. Ecology 62:303–310

    Article  Google Scholar 

  • Institute of Special Aquaculture Species of Hanshou County Hunan Province, Departmant of Biology, Hunan Normal University (1986) Breeding and farming technology of bullfrogs (Rudin). China Fish 11:21

    Google Scholar 

  • Jiang GZ (2008) On the development of Chinese freshwater fish culture technology in the 20th century. Dissertation, Nanjing Agricultural University

  • 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

    Article  Google Scholar 

  • Kiesecker JM, Blaustein AR, Miller CL (2001) Potential mechanisms underlying the displacement of native red-legged frogs by introduced bullfrogs. Ecology 82:1964–1970

    Article  Google Scholar 

  • Kollmann J, Banuelos MJ (2004) Latitudinal trends in growth and phenology of the invasive alien plant Impatiens glandulifera (Balsaminaceae). Divers Distrib 10:377–385

    Article  Google Scholar 

  • Kupferberg SJ (1997) Bullfrog (Rana catesbeiana) invasion of a California river: the role of larval competition. Ecology 78:1736–1751

    Google Scholar 

  • Lai YC, Lee TH, Kam YC (2005) A skeletochronological study on a subtropical, riparian ranid (Rana swinhoana) from different elevations in Taiwan. Zool Sci 22:653–658

    Article  PubMed  Google Scholar 

  • Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391

    Article  Google Scholar 

  • Li C, Xie F (2004) Invasion of bullfrog (Rana catesbeiana) in China and its management strategies. Chinese J Appl Environ Biol 10:95–99

    Article  CAS  Google Scholar 

  • Li YM, Wu ZJ, Duncan RP (2006) Why islands are easier to invade: human influences on bullfrog invasion in the Zhoushan archipelago and neighboring mainland China. Oecologia 148:129–136

    Article  Google Scholar 

  • Liu X, Li YM (2009) Aquaculture enclosures relate to the establishment of feral populations of introduced species. PLoS ONE 4(7): e6199. doi:10.1371/journal.pone.0006199. Accessed 12 Aug 2009

  • Lockwood JL (1999) Using taxonomy to predict success among introduced avifauna: relative importance of transport and establishment. Conserv Biol 13:560–567

    Article  Google Scholar 

  • Lodge DM (2004) Alien species and evolution: the evolutionary ecology of exotic plants, animals, microbes, and interacting native species. Nature 432:276–277

    Article  CAS  Google Scholar 

  • Lovich JE, Gibbons JW (1992) A review of techniques quantifying sexual size dimorphism. Growth Dev Aging 56:269–281

    Google Scholar 

  • 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. Published by The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN)

  • Ma X, Tong L, Lu X (2009) Variation of body size, age structure and growth of a temperate frog, Rana chensinensis, over an elevational gradient in northern China. Amphib-reptil 30:111–117

    Article  Google Scholar 

  • McGarrity M, Johnson S (2009) Geographic trend in sexual size dimorphism and body size of Osteopilus septentrionalis (Cuban treefrog): implications for invasion of the southeastern United States. Biol Inv 11:1411–1420

    Article  Google Scholar 

  • Miaud C, Guyetant R, Elmberg J (1999) Variations in life-history traits in the common frog Rana temporaria (Amphibia : Anura): a literature review and new data from the French Alps. J Zool 249:61–73

    Article  Google Scholar 

  • Ministry of Agriculture of the P.R.C. (1996) Brief introduction of aquaculture species in China. J Beij Fish 3:3–11

    Google Scholar 

  • Monnet JM, Cherry MI (2002) Sexual size dimorphism in anurans. P Roy Soc Lond B Bio 269:2301–2307

    Article  Google Scholar 

  • Mooney H, Hobbs R (2000) Invasive species in a changing world. Island Press, Washington, DC

    Google Scholar 

  • Morrison C, Hero JM (2003) Geographic variation in life-history characteristics of amphibians: a review. J Anim Ecol 72:270–279

    Article  Google Scholar 

  • Morrison C, Hero JM, Browning J (2004) Altitudinal variation in the age at maturity, longevity, and reproductive lifespan of anurans in subtropical Queensland. Herpetologica 60:34–44

    Article  Google Scholar 

  • Pearson D, Shine R, Williams A (2002) Geographic variation in sexual size dimorphism within a single snake species (Morelia spilota, Pythonidae). Oecologia 131:418–426

    Article  Google Scholar 

  • Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288

    Article  Google Scholar 

  • Rosecchi E, Thomas F, Crivelli AJ (2001) Can life-history traits predict the fate of introduced species? A case study on two cyprinid fish in southern France. Freshw Biol 46:845–853

    Article  Google Scholar 

  • Rosso A, Castellano S, Giacoma C (2005) Ecogeographic analysis of morphological and life-history variation in the Italian treefrog. Evol Ecol 18:303–321

    Article  Google Scholar 

  • Ryser J (1996) Comparative life histories of a low-and a high-elevation population of the common frog Rana temporaria. Amphibia-Reptilia 17:183–195

    Article  Google Scholar 

  • Sagor ES, Ouellet M, Barten E, Green DM (1998) Skeletochronology and geographic variation in age structure in the wood frog, Rana sylvatica. J Herpetol 32:469–474

    Article  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Schauble CS (2004) Variation in body size and sexual dimorphism across geographical and environmental space in the frogs Limnodynastes tasmaniensis and L. peronii. Biol J Linn Soc 82:39–56

    Article  Google Scholar 

  • Schroeder EE, Baskett TS (1968) Age estimation, growth rates, and population structure in Missouri bullfrogs. Copeia 3:583–592

    Article  Google Scholar 

  • Shirose LJ, Brooks RJ, Barta JR, Desser SS (1993) Intersexual differences in growth, mortality, and size at maturity in bullfrogs in central Ontario. Can J Zool 71:2363–2369

    Article  Google Scholar 

  • Simberloff D, Parker IM, Windle PN (2005) Introduced species policy, management, and future research needs. Front Ecol Environ 3:12–20

    Article  Google Scholar 

  • Smirina E (1994) Age determination and longevity in amphibians. Gerontol 40:133–146

    Article  CAS  Google Scholar 

  • Smith RJ (1999) Statistics of sexual size dimorphism. J Hum Evol 36:423–458

    Article  CAS  PubMed  Google Scholar 

  • Spear P, Boily M, Giroux I, DeBlois C, Leclair M, Levasseur M, Leclair R (2009) Study design, water quality, morphometrics and age of the bullfrog, Rana catesbeiana, in sub-watersheds of the Yamaska river drainage basin, Québec, Canada. Aquat Toxicol 91:110–117

    Article  CAS  PubMed  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Stillwell RC, Morse GE, Fox CW (2007) Geographic variation in body size and sexual size dimorphism of a seed-feeding beetle. Am Nat 170:358–369

    Article  PubMed  Google Scholar 

  • Sun DJ (1990) The artificial breeding technology of bullfrogs. J Heilongjiang For 1:23–24

    Google Scholar 

  • Travis J (1994) Evaluating the adaptive role of morphological plasticity. In: Wainright PC, Reilly SM (eds) Ecological morphology: integrative organismal biology. University of Chicago Press, Chicago

    Google Scholar 

  • von Bertalanffy L (1957) Quantitative laws in metabolism and growth. Q Rev Biol 32:217–231

    Article  Google Scholar 

  • Wang YP, Guo ZW, Pearl CA, Li YM (2007) Body size affects the predatory interactions between introduced American bullfrogs (Rana catesbeiana) and native anurans in China: an experimental study. J Herpetol 41:514–520

    Article  CAS  Google Scholar 

  • Wilcove DS, Chen LY (1998) Management costs for endangered species. Conserv Biol 12:1405–1407

    Article  Google Scholar 

  • Wu ZJ, Wang YP, Li YM (2004) Natural populations of bullfrogs (Rana catesbeiana) and their potential threat in the east of Zhejiang province. Biodivers Sci 12:441–446

    Google Scholar 

  • Wu ZJ, Li YM, Wang YP, Adams MJ (2005) Diet of introduced Bullfrogs (Rana catesbeiana): predation on and diet overlap with native frogs on Daishan island, China. J Herpetol 39:668–674

    Article  Google Scholar 

  • Xu H, Qiang S, Han Z, Gu J, Huang Z, Sun H, He S, Ding H, Wu H, Wan F (2006) The status and causes of alien species invasion in China. Biodivers Conserv 15:2893–2904

    Article  Google Scholar 

  • Zeng XJ (1998) Prospect and strategy of bullfrog farming. Inland Fish 10:4–5

    Google Scholar 

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Acknowledgments

We thank Y. Luo for assistance with field work. We also thank D. Simberloff and two anonymous referees for their careful examination of an earlier draft and for their constructive comments and help in greatly improving the final manuscript. This study was supported by grants from the “973” program (code: 2007CB411600) and National Science Foundation (code: 30870312). This study was conducted under the approval of the Animal Care and Ethics Committee, Institute of Zoology, Chinese Academy of Sciences.

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Correspondence to Li Yiming.

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An erratum to this article can be found at http://dx.doi.org/10.1007/s10530-009-9621-2

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Xuan, L., Yiming, L. & McGarrity, M. Geographical variation in body size and sexual size dimorphism of introduced American bullfrogs in southwestern China. Biol Invasions 12, 2037–2047 (2010). https://doi.org/10.1007/s10530-009-9606-1

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