Abstract
The red-eared slider (Trachemys scripta elegans) is currently introduced in many Mediterranean countries, where it behaves as an invasive species that competes and displaces native populations of the endangered Spanish terrapin (Mauremys leprosa). However, the nature of competitive interactions is relatively unknown. During basking activity, factors like greater body size or pre-existing behavioral adaptations to an original habitat with higher levels of interspecific competition might confer competitive advantages to introduced T. scripta with respect to native terrapins. We hypothesized that competition for basking places with the introduced T. scripta might negatively affect the efficiency of basking and thermoregulation of the native Spanish terrapin. We experimentally analyzed the basking activity of T. scripta and M. leprosa under occasional and long-term situations of intra- and inter-specific competition. Native M. leprosa subjected to interspecific competition reduced their basking activity, basked for shorter periods than T. scripta, and avoided basking stacked with the exotic turtles. These results suggested the displacement from the basking sites of the native terrapin by the introduced T. scripta. The decreased basking activity of native M. leprosa when competing directly for basking places with introduced sliders may lead native terrapins to a loss in the efficiency of physiological functions related to ineffective thermoregulation, such as digestion or locomotor performance, thus favoring the expansion of the invasive species.
Similar content being viewed by others
References
Arvy C, Servan J (1998) Imminent competition between Trachemys scripta and Emys orbicularis in France. Mertensiella 10:33–40
Auth DL (1975) Behavioral ecology of basking in the yellow-bellied turtle, Chrysemys scripta scripta (Schoepff). Bull Florida State Mus Biol Sci 20:1–45
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
Ben-Ezra E, Bulté G, Blouin-Demes G (2008) Are locomotor performances coadapted to preferred basking temperature in the Northern Map Turtle (Graptemys geographica)? J Herpetol 42:322–331
Boyer DR (1965) Ecology of the basking habit in turtles. Ecology 46:99–118
Bury RB, Wolfheim JH (1973) Aggression in free-living pond turtles (Clemmys marmorata). Bioscience 23:659–662
Bury RB, Wolfheim JH, Luckenbach RA (1979) Agonistic behavior in free-living painted turtles (Chrysemys picta bellii). Biol Behav 4:227–239
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
Cadi A, Joly P (2004) Impact of the introduction of the red-eared slider (Trachemys scripta elegans) on survival rates of the European pond turtle (Emys orbicularis). Biodivers Conserv 13:2511–2518
Cagle FR (1950) The life history of the slider turtle, Pseudemys scripta troostii (Hoolbrook). Ecol Monogr 20:31–54
Carrière MA, Rollinson N, Suley AN, Brooks RJ (2008) Thermoregulation when the growing season is short: sex-biased basking patterns in a northern population of painted turtles (Chrysemys picta). J Herpetol 42:206–209
Crawford KM, Spotila JR, Standora EA (1983) Operative environmental temperatures and basking behavior of the turtle Pseudemys scripta. Ecology 64:989–999
Crucitti P, Campeser A, Malora M (1990) Populazioni sintopiche di Emys orbicularis e Mauremys caspica nella Tracia, Grecia orientale (Reptilia, Testudines: Emydidae). Bull Mus Sci Nat Torino 8:187–196
Da Silva E (2002) Mauremys leprosa. In: Pleguezuelos JM, Márquez R, Lizana M (eds) Atlas y Libro Rojo de los Anfibios y Reptiles de España. AHE-MMA, Madrid, pp 143–146
Da Silva E, Blasco M (1995) Trachemys scripta elegans in Southwestern Spain. Herpetol Rev 26:133–134
Dawson WR (1975) On the physiological significance of the preferred body temperatures of reptiles. In: Gates PM, Scherl RB (eds) Perspectives of biophysical ecology, vol 12. Springer, New York, pp 443–473
De-Rosa CT, Taylor DH (1980) Homeward orientation mechanism in three species of turtles (Trionyx spinifer, Chysemys picta, and Terrapene carolina). Behav Ecol Sociobiol 7:15–23
Díaz-Paniagua C, Marco A, Andreu AC, Sánchez C, Peña L, Acosta M, Molina I (2002) Trachemys scripta en Doñana. Unpublished Report, AHE
Dubois Y, Blouin-Demers G, Thomas D (2008) Temperature selection in wood turtles (Glyptemys insculpta) and its implications for energetics. Ecoscience 15:398–406
Edwards AL, Blouin-Demers G (2007) Thermoregulation as a function of thermal quality in a northern population of painted turtles, Chrysemys picta. Can J Zool 85:526–535
Ganzhorn D, Licht P (1983) Regulation of seasonal gonadal cycles by temperature in the Painted Turtle, Chrysemys picta. Copeia 1983:347–358
Gianopulos KD, Rowe JW (1999) Effects of short-term water temperature variation on food consumption in painted turtles (Chrysemys picta marginata). Chel Cons Biol 3:504–507
Hammond KA, Spotila JR, Standora EA (1988) Basking behavior of the turtle Pseudemys scripta: effects of digestive state, acclimation, temperature, sex and season. Physiol Zool 61:69–77
Huey RB (1982) Temperature, physiology and the ecology of reptiles. In: Gans C, Pough FH (eds) Biology of the reptilia, vol 12. Academic Press, New York, pp 25–91
Hutchison VH, Maness JD (1979) The role of behavior in temperature acclimation and tolerance in ectotherms. Am Zool 19:367–384
Jackson DC (1971) The effect of temperature on ventilation in the turtle, Pseudemys scripta elegans. Respir Physiol 12:131–140
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, pp 57–88
Kepenis V, McManus JJ (1974) Bioenergetics of young painted turtles Chrysemys picta. Comp Biochem Physiol A 48:309–317
Krawchuk MA, Brooks RJ (1998) Basking behavior as a measure of reproductive cost and energy allocation in the Painted Turtle, Chrysemys picta. Herpetologica 54:112–121
Lefevre K, Brooks RJ (1995) Effects of sex and body size on basking behavior in a northern population of the painted turtle, Chrysemys picta. Herpetologica 51:217–224
Lindeman PV (1999) Aggressive interactions during basking among four species of emydid turtles. J Herpetol 33:214–219
López P, Marcos I, Martín J (2005) Effects of habitat-related visibility on escape decisions of the Spanish Terrapin Mauremys leprosa. Amphib-Reptil 26:557–561
Lovich J (1988) Aggressive basking behavior in eastern painted turtles (Chrysemys picta picta). Herpetologica 44:197–202
Meek R (1983) Body temperatures of a desert population of the stripe-necked terrapin, Mauremys caspica. Br J Herpetol 6:335–337
Meek R, Avery RA (1988) Thermoregulation in chelonians. Herpetol J 1:253–259
Mendonca MT (1987) Photothermal effects on the ovarian cycle of the musk turtle, Sternotherus odoratus. Herpetologica 43:82–90
Moll EO, Legler JM (1971) The life history of a neotropical slider turtle, Pseudemys scripta (Schoepff) in Panama. Sci Bull Nat Hist Mus Los Angeles Co 11:1–102
Neill WT, Allen ER (1954) Algae on turtles: some additional considerations. Ecology 35:581–584
Parmenter RR (1981) Digestive turnover rates in freshwater turtles: the influence of temperature and body size. Comp Biochem Physiol A 70:235–238
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, pp 501–532
Pluto TG, Bellis ED (1986) Habitat utilization by the turtle, Graptemys geographica, along a river. J Herpetol 20:22–31
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
Polo-Cavia N, López P, Martín J (2009a) Interspecific differences in chemosensory responses of freshwater turtles: consequences for competition between native and invasive species. Biol Invasions 11:431–440
Polo-Cavia N, López P, Martín J (2009b) Interspecific differences in heat exchange rates may affect competition between introduced and native freshwater turtles. Biol Invas 11:1755–1765
Pritchard PCH, Greenhood WF (1968) The sun and the turtle. Int Turt Tortoise Soc J 2:20–25
Rollinson N, Brooks RJ (2007) Proximate constraints on reproductive output in a northern population of painted turtles (Chrysemys picta): an empirical test of the bet-hedging paradigm. Can J Zool 85:177–184
Sarkar SN, Sarkar K, Das P, Maiti BR (1996) Photothermal effects on ovarian growth and function in the soft-shelled turtle Lissemys punctata punctata. J Exp Zool 274:41–55
Scharzkoplf L, Brooks RJ (1985) Application of operative environmental temperatures to analysis of basking behavior in Chrysemys picta. Herpetologica 41:206–212
Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W. H. Freeman, New York
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
Vogt RC (1979) Cleaning/feeding symbiosis between grackles (Quiscalus: Icteridae) and map turtles (Graptemys: Emydidae). Auk 96:608–609
Zimmerman LC, Tracy CR (1989) Interactions between the environment and ectothermy and herbivory in reptiles. Physiol Zool 62:374–409
Acknowledgments
We thank two anonymous reviewers for helpful comments, the “Grupo de Rehabilitación de la Fauna Autóctona y su Hábitat” (GREFA) for providing sliders, and “El Ventorrillo” MNCN Field Station for use of their facilities. Financial support was provided by the MEC project CGL2005-00391/BOS and the MCI project MCI-CGL2008-02119/BOS, and by an “El Ventorrillo” CSIC grant and a MEC-FPU grant to N. P.-C.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Polo-Cavia, N., López, P. & Martín, J. Competitive interactions during basking between native and invasive freshwater turtle species. Biol Invasions 12, 2141–2152 (2010). https://doi.org/10.1007/s10530-009-9615-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-009-9615-0