Skip to main content

Aggressive interactions during feeding between native and invasive freshwater turtles

Biological Invasions volume 13, pages 1387–1396 (2011)Cite this article

Abstract

The red-eared slider (Trachemys scripta elegans) is a worldwide highly invasive species, currently introduced in most freshwater habitats as a consequence of massive pet trade. In the Iberian Peninsula, this species is competing with and displacing the endangered native Spanish terrapin (Mauremys leprosa). Sliders are considered environmentally-aggressive turtles, capable of threatening or biting other individuals during competitive activities such as feeding. We hypothesized that agonistic behavior of introduced sliders against native terrapins might negatively affect the feeding efficiency of M. leprosa. We compared food ingestion of turtles and aggressive interactions during feeding, under situations of conspecific and heterospecific competition. The amount of food ingested by native and introduced turtles was similar under conspecific competition, but T. scripta ingested a greater percentage of food supplied under heterospecific competition. Also, introduced sliders initiated most of the aggressions observed during feeding activity, and aggression was more frequently directed to heterospecifics. Our results suggest a more aggressive and competitive behavior of introduced T. scripta in vying for food resources, which might contribute to explain the observed displacement of native populations of M. leprosa.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1

References

  • Abramsky Z, Rosenzweig ML, Pinshow B, Brown JS, Kotler BP, Mitchell WA (1990) Habitat selection: an experimental field test with two gerbil species. Ecology 71:2358–2369

    Article  Google Scholar 

  • Alatalo RV, Moreno J (1987) Body size, interspecific interactions, and use of foraging sites in tits (Paridae). Ecology 68:1773–1777

    Article  Google Scholar 

  • Alatalo RV, Gustafsson L, Lundberg A (1986) Interspecific competition and niche changes in tits (Parus spp.): evaluation of non experimental data. Am Nat 127:819–834

    Article  Google Scholar 

  • Arnold EN, Ovenden DW (2002) Guía de campo de los reptiles y anfibios de España y de Europa. Omega, Barcelona

    Google Scholar 

  • Arvy C, Servan J (1998) Imminent competition between Trachemys scripta and Emys orbicularis in France. Mertensiella 10:33–40

    Google Scholar 

  • Berry JF (1975) The population effects of ecological sympatry on musk turtles in northern Florida. Copeia 1975:692–701

    Article  Google Scholar 

  • Boice R (1970) Competitive feeding behaviors in captive Terrapene c. carolina. Anim Behav 18:703–710

    Article  Google Scholar 

  • Bury RB (1979) Population ecology of freshwater turtles. In: Harless M, Morlock H (eds) Turtles: perspectives and research. Wiley, New York, pp 571–602

    Google Scholar 

  • Butterfield BP, Meshaka WE Jr, Guyer C (1997) Non-indigenous amphibians and reptiles. In: Simberloff D, Schmitz DC, Brown TC (eds) Strangers in paradise: impact and management of non-indigenous species in Florida. Island Press, Washington, DC, pp 123–138

    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 

  • 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). Biodiv Conserv 13:2511–2518

    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 

  • Chen TH, Lue KY (1998) Ecological notes on feral populations of Trachemys scripta elegans in northern Taiwan. Chelon Conserv Biol 3:87–90

    CAS  Google Scholar 

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

    Google Scholar 

  • Díaz-Paniagua C, Marco A, Andreu AC, Sánchez C, Peña L, Acosta M, Molina I (2002) Trachemys scripta en Doñana. Asociación Herpetológica Española-Ministerio de Medio Ambiente, Sevilla (unpublished report)

  • Dodd CK, Seigel RA (1991) Relocation, repatriation, and translocation of amphibians and reptiles: are they effective conservation strategies that work? Herpetologica 47:336–350

    Google Scholar 

  • Fausch KD (1984) Profitable stream positions for salmonids: relating specific growth rate to net energy gain. Can J Zool 62:441–451

    Article  Google Scholar 

  • Fretwell SD, Lucas HL (1970) On territorial behavior and other factors influencing habitat distribution in birds. Acta Biotheor 19:16–36

    Article  Google Scholar 

  • Gause GF (1934) The struggle for existence. Williams and Wilkins, Baltimore

    Google Scholar 

  • Gaymer CF, Himmelman JH, Johnson LE (2001) Use of prey resources by the seastars Leptasterias polaris and Asterias vulgaris: a comparison between field observations and laboratory experiments. J Exp Mar Biol Ecol 262:13–30

    Article  Google Scholar 

  • Gaymer CF, Himmelman JH, Johnson LE (2002) Effect of intra- and interspecific interactions on the feeding behavior of two subtidal seastars. Mar Ecol Prog Ser 232:16–149

    Article  Google Scholar 

  • Gibbons WJ (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 

  • Gibbons WJ, Keaton GH, Schubauer JP, Greene JL, Bennett D, McAuliffe J, Sharitz RR (1979) Unusual population size structure in freshwater turtles on barrier islands. Ga J Sci 37:155–159

    Google Scholar 

  • Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19:470–474

    PubMed  Article  Google Scholar 

  • Hardin G (1960) The competitive exclusion principle. Science 131:1292–1297

    PubMed  Article  CAS  Google Scholar 

  • Hart DR (1983) Dietary and habitat shift with size of red-eared turtles (Pseudemys scripta) in a southern Louisiana population. Herpetologica 39:285–290

    Google Scholar 

  • Herbold B, Moyle PB (1986) Introduced species and vacant niches. Am Nat 128:751–760

    Article  Google Scholar 

  • Holmgren N (1995) The ideal free distribution of unequal competitors: predictions from a behaviour-based functional response. J Anim Ecol 64:197–212

    Article  Google Scholar 

  • Huntingford FA, García de Leániz C (1997) Social dominance, prior residence and the acquisition of profitable feeding sites in juvenile Atlantic salmon. J Fish Biol 51:1009–1014

    Article  Google Scholar 

  • Huntingford F, Turner A (1987) Animal conflict. Chapman and Hall, London

    Google Scholar 

  • Huntingford FA, Metcalfe NB, Thorpe JE (1993) Social status and feeding in Atlantic salmon Salmo salar parr: the effect of visual exposure to a dominant. Ethology 94:201–206

    Article  Google Scholar 

  • Jackson CG Jr, Davis JD (1972) A quantitative study of the courtship display of the red-eared turtle, Chrysemys scripta elegans (Wied). Herpetologica 28:58–64

    Google Scholar 

  • Kaufmann JH (1992) The social behavior of wood turtles, Clemmys insculpta, in central Pennsylvania. Herpetol Monogr 6:1–25

    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-Verlag, Wiesbaden, pp 57–88

    Google Scholar 

  • Kronfeld-Schor N, Dayan T (1999) The dietary basis for temporal partitioning: food habits of coexisting Acomys species. Oecologia 121:123–128

    Article  Google Scholar 

  • Kronfeld-Schor N, Dayan T (2003) Partitioning of time as an ecological resource. Ann Rev Ecol Evol Syst 34:153–181

    Article  Google Scholar 

  • Lindeman PV (1999) Aggressive interactions during basking among four species of emydid turtles. J Herpetol 33:214–219

    Article  Google Scholar 

  • Lockwood JL, Hoopes MF, Marchetti MP (2007) Invasion ecology. Blackwell Publishing, Oxford

    Google Scholar 

  • Lovich JE (1988) Aggressive basking behavior in eastern painted turtles (Chrysemys picta picta). Herpetologica 44:197–202

    Google Scholar 

  • Luiselli L, Capula M, Capizzi D, Filippi E, Trujillo JV, Anibaldi C (1997) Problems for conservation of pond turtles (Emys orbicularis) in central Italy: is the introduced redeared turtle (Trachemys scripta) a serious threat? Chelon Conserv Biol 2:417–419

    Google Scholar 

  • Manchester SJ, Bullock JM (2000) The impacts of non-native species on UK biodiversity and the effectiveness of control. J Appl Ecol 37:845–864

    Article  Google Scholar 

  • Martín J, Salvador A (1993) Tail loss reduces mating success in the Iberian rock-lizard, Lacerta monticola. Behav Ecol Sociobiol 32:185–189

    Article  Google Scholar 

  • Menge JL, Menge BA (1974) Role of resource allocation, aggression and spatial heterogeneity in coexistence of two competing intertidal starfish. Ecol Monogr 44:189–209

    Article  Google Scholar 

  • Moll DL (1976a) Food and feeding strategies of the Ouachita map turtle (Graptemys pseudogeographica ouachitensis). Amer Midl Natur 96:478–482

    Article  Google Scholar 

  • Moll DL (1976b) Environmental influence on growth rate in the Ouachita Map turtle, Graptemys pseudogeographica ouachitensis. Herpetologica 32:439–443

    Google Scholar 

  • Moody AL, Houston AI (1995) Interference and the ideal free distribution. Anim Behav 49:1065–1072

    Article  Google Scholar 

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

    Google Scholar 

  • Nakano S (1995) Competitive interactions for foraging microhabitats in a size-structured interspecific dominance hierarchy of two sympatric stream salmonids in a natural habitat. Can J Zool 73:1845–1854

    Article  Google Scholar 

  • Newbery R (1984) The American red-eared terrapin in South Africa. Afr Wildl 38:186–189

    Google Scholar 

  • Ovadia O, zu Dohna H (2003) The effect of intra and interspecific aggression on patch residence time in Negev Desert gerbils: a competing risk analysis. Behav Ecol 14:583–591

    Article  Google Scholar 

  • Parmenter RR (1980) Effects of food availability and water temperature on the feeding ecology of pond sliders (Chrysemys s. scripta). Copeia. pp 503–514

  • Parmenter RR, Avery HW (1990) The feeding ecology of the slider turtle. In: Gibbons WJ (ed) Life history and ecology of the slider turtle. Smithsonian Institution Press, Washington, DC, pp 257–266

    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. Asociación Herpetológica Española-Ministerio de Medio Ambiente, Madrid, pp 501–532

    Google Scholar 

  • Pleguezuelos JM, Márquez R, Lizana M (2002) Atlas y Libro Rojo de los Anfibios y Reptiles de España. Asociación Herpetológica Española-Ministerio de Medio Ambiente, 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

    Article  Google Scholar 

  • 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 Invas 11:431–440

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Polo-Cavia N, López P, Martín J (2010a) Competitive interactions during basking between native and invasive freshwater turtle species. Biol Invas 12:2141–2152

    Article  Google Scholar 

  • Polo-Cavia N, Gonzalo A, López P, Martín J (2010b) Predator-recognition of native but not invasive turtle predators by naïve anuran tadpoles. Anim Behav 80:461–466

    Article  Google Scholar 

  • Schlaepfer MA, Sherman PW, Blossey B, Runge MC (2005) Introduced species as evolutionary traps. Ecol Lett 8:241–246

    Article  Google Scholar 

  • Schoener TW (1983) Field experiments on interspecific competition. Am Nat 122:240–280

    Article  Google Scholar 

  • Shigesada N, Kawasaki K (1997) Biological invasions: theory and practice. Oxford University Press, Oxford

    Google Scholar 

  • Sloan NA (1984) Interference and aggregation: close encounters of the starfish kind. Ophelia 23:23–31

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. WH Freeman, New York

    Google Scholar 

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

    Google Scholar 

  • Spencer HG, Kennedy M, Gray RD (1995) Patch choice with competitive asymmetries and perceptual limits: the importance of history. Anim Behav 50:497–508

    Article  Google Scholar 

  • Vilà M, Valladares F, Traveset A, Santamaría L, Castro P (2008) Invasiones biológicas. Consejo Superior de Investigaciones Científicas, Madrid

    Google Scholar 

  • Vogt RC (1981) Food partitioning in three sympatric species of map turtle, genus Graptemys (Testudinata, Emydidae). Amer Midl Natur 105:102–111

    Article  Google Scholar 

  • Vogt RC, Guzman SG (1988) Food partitioning in a neotropical freshwater turtle community. Copeia 1988:37–47

    Article  Google Scholar 

  • Webb RG (1962) North American soft-shelled turtles (formerly Trionichidae). Univ Kans Publ Mus Nat Hist 13:429–611

    Google Scholar 

  • Weinstein M (2003) Spiny arthropods, spiny parasites and spiny mice—availability and ecology in En-Gedi. M.Sc. Dissertation, Tel-Aviv University

  • Wilcove DS, Rothstein D, Dubow D, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States. Bioscience 48:607–615

    Article  Google Scholar 

  • Williams TA, Christiansen JL (1981) The niches of two sympatric softshell turtles Trionyx muticus and Trionyx spiniferus in Iowa. Herpetologica 15:303–308

    Article  Google Scholar 

  • Williamson M (1996) Biological invasions. Chapman and Hall, London

    Google Scholar 

  • Ziv Y, Abramsky Z, Kotler BP, Subach A (1993) Interference competition and temporal and habitat partitioning in two gerbil species. Oikos 66:237–246

    Article  Google Scholar 

Download references

Acknowledgments

We thank an anonymous referee 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 CGL2008-02119/BOS, and by a MEC-FPU grant to N. P.-C. The experiments comply with all the present Spanish laws of the Environmental Organisms of the “Comunidad de Madrid” where they were performed.

Author information

Author notes

  1. Nuria Polo-Cavia

    Present address: Departamento de Biología, Universidad Autónoma de Madrid, Ciudad Universitaria de Cantoblanco, 28049, Madrid, Spain

Authors and Affiliations

  1. Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006, Madrid, Spain

    Nuria Polo-Cavia, Pilar López & José Martín

Authors
  1. Nuria Polo-Cavia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pilar López
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. José Martín
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nuria Polo-Cavia.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Polo-Cavia, N., López, P. & Martín, J. Aggressive interactions during feeding between native and invasive freshwater turtles. Biol Invasions 13, 1387–1396 (2011). https://doi.org/10.1007/s10530-010-9897-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-010-9897-2

Keywords

  • Aggressiveness
  • Feeding competition
  • Freshwater turtles
  • Invasive species
  • Mauremys leprosa
  • Trachemys scripta