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Interspecific differences in heat exchange rates may affect competition between introduced and native freshwater turtles

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Abstract

In the Iberian Peninsula, the red-eared slider (Trachemys scripta elegans) is an introduced invasive species that is displacing the endangered native Spanish terrapin (Mauremys leprosa). However, the nature of competitive interactions is relatively unclear. In temperate zones, mechanisms for maximizing heat retention could be selectively advantageous for aquatic turtle species, since individuals usually lose the heat gained from basking very rapidly when entering the water. We hypothesized that interspecific differences in morphology, and thus, in heating and cooling rates, might confer competitive advantages to introduced T. scripta. We compared the surface-to-volume ratios of both, introduced and native turtles, basing on biometric measures, and their effects on thermal exchange rates. T. scripta showed a more rounded shape, a lower surface-to-volume ratio and a greater thermal inertia, what facilitates body heat retention and favors the performance of activities and physiological functions such as foraging or digestion, thus aggravating the competition process with native turtles in Mediterranean habitats.

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References

  • Aceituno J (2001) La población del galápago de Florida (Trachemys scripta elegans) en la desembocadura del Río Cofio-Embalse de San Juan (Madrid). AHE, Madrid (unpublished report)

  • Arnold EN, Burton JA (1982) Guía de campo de los reptiles y anfibios de España y de Europa. Omega, Barcelona

    Google Scholar 

  • Avery RA (1982) Field studies of body temperatures and thermoregulation. In: Gans C, Pough FH (eds) Biology of the Reptilia, vol 12. Academic Press, New York, pp 93–166

    Google Scholar 

  • Avery HW, Spotila JR, Congdon JD, Fischer RU Jr, Standora EA, Avery SB (1993) Roles of diet protein and temperature in the growth and nutritional energetics of juvenile Slider Turtles, Trachemys scripta. Physiol Zool 66:902–925

    Google Scholar 

  • Ayers DY, Shine R (1997) Thermal influences on foraging ability: body size, posture and cooling rate of an ambush predator, the python Morelia spilota. Funct Ecol 11:342–347

    Article  Google Scholar 

  • Bartholomew GA (1982) Physiological control of body temperature. In: Gans C, Pough FH (eds) Biology of the Reptilia, vol 12. Academic Press, New York, pp 167–212

    Google Scholar 

  • Bogert CM (1949) Thermoregulation in reptiles, a factor in evolution. Evolution 3:195–211

    Article  PubMed  CAS  Google Scholar 

  • Boyer DR (1965) Ecology of the basking habit in turtles. Ecology 46:99–118

    Article  Google Scholar 

  • Cadi A, Joly P (2003) Competition for basking places between the endangered European pond turtle (Emys orbicularis galloitalica) and the introduced red-eared slider (Trachemys scripta elegans). Can J Zool 81:1392–1398

    Article  Google Scholar 

  • Cagle FR (1950) The life history of the slider turtle, Pseudemys scripta troostii (Hobrook). Ecol Monogr 20:31–54

    Article  Google Scholar 

  • Cailleux A (1947) L’indice d’emousse: definition et premiere application. C R S Soc Geol Fr 13:250–252

    Google Scholar 

  • Claude J, Paradise E, Tong H, Auffray JC (2003) A geometric morphometric assessment of the effects of environment and cladogenesis on the evolution of the turtle shell. Biol J Linn Soc 79:485–501

    Article  Google Scholar 

  • Cloudsley-Thompson JL (1974) Physiological thermoregulation in the spurred tortoise (Testudo graeca L.). J Nat Hist 8:577–587

    Article  Google Scholar 

  • Congdon JD (1989) Proximate and evolutionary constraints on energy relations of reptiles. Physiol Zool 62:356–373

    Google Scholar 

  • Crawford KM, Spotila JR, Standora EA (1983) Operative environmental temperatures and basking behavior of the turtle Pseudernys scripta. Ecology 64:989–999

    Article  Google Scholar 

  • Crucitti P, Campeser A, Malori M (1990) Populazioni sintopiche di Emys orbicularis e Mauremys caspica nella Tracia, Grecia orientale (Reptilia, Testudines: Emydidae). Ball Mus Reg Sci Nat Torino 8:187–196

    Google Scholar 

  • Da Silva E, Blasco M (1995) Trachemys scripta elegans in Southwestern Spain. Herpetol Rev 26:133–134

    Google Scholar 

  • Do Amaral JPS, Marvin GA, Hutchison VH (2002) Thermoregulation in the box turtles Terrapene carolina and Terrapene ornata. Can J Zool 80:934–943

    Article  Google Scholar 

  • Dunham AE, Grant BW, Overall KL (1989) Interfaces between biophysical and physiological ecology and the population ecology of terrestrial vertebrate ecthoterms. Physiol Zool 62:335–355

    Google Scholar 

  • Ernst CH (1972) Temperature activity relationship in the painted turtle, Chrysemys picta. Copeia 1972:217–222

    Article  Google Scholar 

  • Ernst CH (1982) Environmental temperatures and activities in wild spotted turtles, Clemmys guttata. J Herpetol 16:112–120

    Article  Google Scholar 

  • Gianopulos KD, Rowe JW (1999) Effects of short-term water temperature variation on food consumption in Painted Turtles (Chrysemys picta marginata). Chelonian Conserv Biol 3:504–507

    Google Scholar 

  • Gibbons JW (1990) The slider turtle. In: Gibbons JW (ed) Life history and ecology of the slider turtle. Smithsonian Institution Press, Washington, DC, pp 3–18

    Google Scholar 

  • Gould SJ (1966) Allometry and size in ontogeny and phylogeny. Biol Rev 41:587–640

    Article  PubMed  CAS  Google Scholar 

  • Greene HW (1988) Antipredator mechanisms in reptiles. In: Gans C, Huey RB (eds) Biology of the Reptilia, vol 16. Academic Press, New York, pp 1–152

    Google Scholar 

  • Grigg GC, Drane CR, Courtice GP (1979) Time constants of heating and cooling in the eastern water dragon, Physignathus lesueurii and some generalizations about heating and cooling in reptiles. J Therm Biol 4:95–103

    Article  Google Scholar 

  • Gronke WK, Chipps SR, Bandas SJ, Higgins KF (2006) Reticulate melanism in western painted turtles (Chrysemys picta bellii): exploring linkages with habitat and heating rates. Am Midl Nat 156:289–298

    Article  Google Scholar 

  • Huey RB, Slatkin M (1976) Cost and benefit of lizard thermoregulation. Q Rev Biol 51:363–384

    Article  PubMed  CAS  Google Scholar 

  • Hutchison VH (1979) Thermoregulation. In: Harless M, Morlock H (eds) Turtles perspectives and research. Wiley, New York, pp 207–228

    Google Scholar 

  • Hutchison VH, Maness JD (1979) The role of behavior in temperature acclimation and tolerance in ectotherms. Am Zool 19:367–384

    Google Scholar 

  • Janzen FJ, Tucker JK, Paukstis GL (2000) Experimental analysis of an early life-history stage: avian predation selects for larger body size of hatchling turtles. J Evol Biol 13:947–954

    Article  Google Scholar 

  • Kaufman KW (1981) Fitting and using growth curves. Oecologia 49:293–299

    Article  Google Scholar 

  • Keller C, Busack SD (2001) Mauremys leprosa (Schweigger, 1812)—Maurische Bachschildkröte. In: Fritz U (ed) Handbuch der Reptilien und Amphibien Europas, vol 3/IIIA. Schildkröten (Testudines) I. Aula, Wiesbaden, Germany, pp 57–88

  • Klamkin MS (1971) Elementary approximations to the area of n-dimensional ellipsoids. Am Math Mon 78:280–283

    Article  Google Scholar 

  • Krumbein WC (1941) Measurement and geological significance of shape and roundness of sedimentary particles. J Sediment Petrol 11:64–72

    CAS  Google Scholar 

  • Legendre AM (1811) Exercices de calcul intégral, vol 1. Huzard-Courcier, Paris, pp 182–194

    Google Scholar 

  • Lysenko S, Gillis JE (1980) The effect of ingestive status on the thermoregulatory behavior of Thamnophis sirtalis sirtalis and Thamnophis sirtalis parietalis. J Herpetol 14:155–159

    Article  Google Scholar 

  • Manning B, Grigg GC (1997) Basking is not of thermoregulatory significance in the “basking” freshwater turtle Emydura signata. Copeia 1997:579–584

    Article  Google Scholar 

  • Martín J, López P, Carrascal LM, Salvador A (1995) Adjustments of basking postures in the high altitude Iberian rock lizard (Lacerta monticola ). Can J Zool 73:1065–1068

    Article  Google Scholar 

  • Meek R (1983) Body temperatures of a desert population of the stripe-necked terrapin, Mauremys caspica. Br J Herpetol 6:335–337

    Google Scholar 

  • Meek R, Avery RA (1988) Thermoregulation in chelonians. Herpetol J 1:253–259

    Google Scholar 

  • Moll EO, Legler JM (1971) The life history of a neotropical slider turtle, Pseudemys scripta (Schoepff) in Panama. Bull Los Angel Cty Mus Nat Hist Sci 11:1–102

    Google Scholar 

  • Morreale SJ, Gibbons JW (1986) Habitat suitability index models: Slider turtle. US Fish Wildl Serv Biol Rep: 82(10.125), 14 pp

  • Mrosovsky N (1980) Thermal biology of sea turtles. Am Zool 20:531–547

    Google Scholar 

  • Obbard ME, Brooks RJ (1979) Factors affecting basking in a northern population of the common snapping turtle, Chelydra serpentina. Can J Zool 57:435–440

    Article  Google Scholar 

  • Obbard ME, Brooks RJ (1981) A radio-telemetry and mark-recapture study of the activity in the common snapping turtle, Chelydra serpentina. Copeia 1981:630–637

    Article  Google Scholar 

  • Paladino FV, O’Connor MP, Spotila JR (1990) Metabolism of leatherback turtles, gigantothermy, and thermoregulation of dinosaurs. Nature 344:858–860

    Article  Google Scholar 

  • Parmenter RR (1981) Digestive turnover rates in freshwater turtles: the influence of temperature and body size. Comp Biochem Physiol A 70:235–238

    Article  Google Scholar 

  • Pearson D, Shine R, Williams A (2003) Thermal biology of large snakes in cool climates: a radio-telemetric study of carpet pythons (Morelia spilota imbricata) in south-western Australia. J Therm Biol 28:117–131

    Article  Google Scholar 

  • Pleguezuelos JM (2002) Las especies introducidas de Anfibios y Reptiles. In: Pleguezuelos JM, Márquez R, Lizana M (eds) Atlas y Libro Rojo de los Anfibios y Reptiles de España. AHE-MMA, Madrid, Spain, pp 501–532

    Google Scholar 

  • Pleguezuelos JM, Márquez R, Lizana M (2002) Atlas y Libro Rojo de los Anfibios y Reptiles de España. AHE-MMA, Madrid

    Google Scholar 

  • Polo-Cavia N, López P, Martín J (2008) Interspecific differences in responses to predation risk may confer competitive advantages to invasive freshwater turtle species. Ethology 114:115–123

    Google Scholar 

  • Pritchard PCH, Greenhood WF (1968) The sun and the turtle. Int Turtle Tortoise Soc J 2:20–25

    Google Scholar 

  • Rice AN, Roberts L, Dorcas ME (2006) Heating and cooling rates of eastern diamondback rattlesnakes, Crotalus adamanteus. J Therm Biol 31:501–505

    Article  Google Scholar 

  • Seebacher F, Grigg GC, Beard LA (1999) Crocodiles as dinosaurs: behavioural thermoregulation in very large ectotherms leads to high and stable body temperatures. J Exp Biol 202:77–86

    PubMed  Google Scholar 

  • Slip DJ, Shine R (1988) Reptilian endothermy: a field-study of thermoregulation by brooding diamond pythons. J Zool 216:367–378

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W. H Freeman, New York

    Google Scholar 

  • Spotila JR, Lommen PW, Bakken GS, Gates DM (1973) A mathematical model for body temperatures of large reptiles: implications for dinosaur ecology. Am Nat 107:391–404

    Article  Google Scholar 

  • Spotila JR, Foley RE, Schubauer JP, Semlitsch RD, Crawford KM, Standora EA, Gibbons JW (1984) Opportunistic behavioral thermoregulation of turtles, Pseudemys scripta, in response to micro-climatology of a nuclear reactor cooling reservoir. Herpetologica 40:299–308

    Google Scholar 

  • Spotila JR, O’Connor MP, Dodson P, Paladino FV (1991) Hot and cold running dinosaurs: body size, metabolism and migration. Mod Geol 16:203–227

    Google Scholar 

  • Spray DC, May ML (1972) Heating and cooling rates in four species of turtles. Comp Biochem Physiol A 41:507–522

    Article  PubMed  CAS  Google Scholar 

  • Standora EA (1982) A telemetric study of the thermoregulatory behavior and climate space of free-ranging yellow-bellied turtles, Pseudemys scripta. Dissertation, University of Georgia

  • Sturbaum BA (1982) Temperature regulation in turtles. Comp Biochem Physiol A 72:615–620

    Article  Google Scholar 

  • Turner JS (1982) The relationship between heat exchange and blood flow in reptiles. Dissertation, Colorado State University

  • Vogt RC (1979) Cleaning/feeding symbiosis between grackles (Quiscalus: Icteridae) and map turtles (Graptemys: Emydidae). Auk 96:608–609

    Google Scholar 

  • Von Bertalanffy L (1960) Principles and theory of growth. In: Nowinski WW (ed) Fundamental aspects of normal and malignant growth. Elsevier, Princeton, pp 137–259

    Google Scholar 

  • Wallace BP, Williams CL, Paladino FV, Morreale SJ, Lindstrom RT, Spotila JR (2005) Bioenergetics and diving activity of internesting leatherback turtles Dermochelys coriacea at Parque Nacional Marino las Baulas, Costa Rica. J Exp Biol 208:3873–3884

    Article  PubMed  Google Scholar 

  • Weathers WW (1970) Physiological thermoregulation in the lizard Dipsosaurus dorsalis. Copeia 1970:549–557

    Article  Google Scholar 

  • Weathers WW, White FN (1971) Physiological thermoregulation in turtles. Am J Physiol 221:704–710

    PubMed  CAS  Google Scholar 

  • Whittow GC, Balazs GH (1982) Basking behavior of the Hawaiian green turtle (Chelonia mydas). Pac Sci 36:129–140

    Google Scholar 

  • Wilson TP (1994) Ecology of the spotted turtles, Clemmys guttata, at the western range limit. Dissertation, Eastern Illionois University

  • Zimmerman LC, Tracy CR (1989) Interactions between the environment and ectothermy and herbivory in reptiles. Physiol Zool 62:374–409

    Google Scholar 

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Acknowledgments

We thank A. Marzal for allowing us to work in his dehesa state (“La Asesera”), the “Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat” (GREFA) for providing exotic turtles, and “El Ventorrillo” MNCN Field Station for use of their facilities. Helpful suggestions for the analytical model of thermal exchange rates were provided by V. Polo. Financial support was provided by MEC-FPU grant to N.P.-C. and by the MEC project CGL2005-00391/BOS. The experiments comply with the current laws of Spain and the Environmental Agencies of the “Junta de Extremadura” and “Comunidad de Madrid” where they were performed.

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Correspondence to Nuria Polo-Cavia.

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Polo-Cavia, N., López, P. & Martín, J. Interspecific differences in heat exchange rates may affect competition between introduced and native freshwater turtles. Biol Invasions 11, 1755–1765 (2009). https://doi.org/10.1007/s10530-008-9355-6

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