Skip to main content
Log in

Turtles Are Not Just Walking Stones: Conspicuous Coloration and Sexual Selection in Freshwater Turtles

  • Original Paper
  • Published:
Biosemiotics Aims and scope Submit manuscript

Abstract

Turtles are among the most intriguing amniotes but their communication and signaling have rarely been studied. Traditionally, they have been seen as basically just silent armored ‘walking stones’ with complex physiology but no altruism, maternal care, or aesthetic perception. Recently, however, we have witnessed a radical change in the perception of turtle behavioral and cognitive skills. In our study, we start by reviewing some recent findings pertaining to various highly developed behavioral and cognitive patterns with special emphasis on turtles. Then we focus on freshwater turtles and use data about their sexual behavior and size sexual dimorphism (SSD) to test whether conspicuous coloration of the head is in these animals related to sexual processes. We found that absence of aggressive mating behavior is statistically associated with the presence of conspicuous coloration on turtles’ heads. It also seems that while species with female-biased SSD are characterised by conspicuously colored head ornaments, in species with male-biased SSD conspicuous coloration is absent. Unlike large females, males thus seem to be under pressure to develop conspicuous coloration and engage in non-aggressive behavior using signaling to succeed in courtship. And finally, we discuss possible roles of head color patterns in turtle communication during mating.

This is a preview of subscription content, log in via an institution to check access.

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Agha, M., Lovich, J. E., Ennen, J. R., & Wilcox, E. (2013). Nest-guarding by female Agassiz’s desert tortoise (Gopherus agassizii) at a wind-energy facility near Palm Springs, California. The Southwestern Naturalist, 58, 254–257.

    Article  Google Scholar 

  • Alberts, A. C., Rostal, D. C., & Lance, V. A. (1994). Studies on the chemistry and social significance of chin gland secretions in the desert tortoise, Gopherus agassizii. Herpetological Monographs, 8, 116–124.

    Article  Google Scholar 

  • Anders, B. (2012). Callin’ all rednecks! Turtle Survival, 57–58.

  • Auffenberg, W. (1966). On the courtship of Gopherus Polyphemus. Herpetologica, 22, 113–117.

    Google Scholar 

  • Auffenberg, W. (1977). Display behavior in tortoises. American Zoologist, 17, 241–250.

    Article  Google Scholar 

  • Bartholomew, G. A. (1970). A model for the evolution of pinniped polygyny. Evolution, 24, 546–559.

    Article  Google Scholar 

  • Berry, J. F., & Shine, R. (1980). Sexual size dimorphism and sexual selection in turtles (order Testudines). Oecologia, 44, 185–191.

    Article  Google Scholar 

  • Blackenhorn, W. U. (2005). Behavioral causes and consequences of sexual size dimorphism. Ethology, 111, 977–1016.

    Article  Google Scholar 

  • Brattstorm, B. H. (1974). The evolution of reptilian social behavior. American Zoologist, 14, 35–49.

    Article  Google Scholar 

  • Brykczynska, U., Tzika, A. C., Rodriguez, I., & Milinkovitch, M. C. (2013). Contrasted evolution of the vomeronasal receptor repertoires in mammals and squamate reptiles. Genome Biology and Evolution, 5, 389–401.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Burghardt, G. M. (1977). Of iguanas and dinosaurs: social behavior and communication in neonate reptiles. American Zoologist, 17, 177–190.

    Article  Google Scholar 

  • Burghardt, G. M. (1991). Cognitive ethology and critical anthropomorphism: A snake with two heads and hognose snake that play dead. In C. A. Ristau (Ed.), Cognitive ethology: The minds of other animals: Essays in honor of Donald R. Griffin (pp. 53–90). Hillsdale: Laurence Erlbaum Associates, Inc.

    Google Scholar 

  • Burghardt, G. M. (2005). The genesis of animal play: Testing the limits. Cambridge: Massachusetts Institute of Technology Press.

    Google Scholar 

  • Burghardt, G. M. (2013). Environmental enrichment and cognitive complexity in reptiles and amphibians: concepts, review, and implications for captive populations. Applied Animal Behaviour Science, 147, 286–298.

    Article  Google Scholar 

  • Burghardt, G. M., Greene, H. W., & Rand, A. S. (1977). Social behaviour in hatchling green iguanas: life as a reptile rookery. Science, 195, 689–691.

    Article  CAS  PubMed  Google Scholar 

  • Cailliez, F. (1983). The analytical solution of the additive constant problem. Psychometrika, 48, 305–308.

    Article  Google Scholar 

  • Carr, A., & Hirth, H. (1960). Social facilitation in Green turtle siblings. Animal Behaviour, 9, 68–70.

    Article  Google Scholar 

  • Ceballos, C. P., Adams, D. C., Iverson, J. B., & Valenzuela, N. (2013). Phylogenetic patterns of sexual size dimorphism in turtles and their implications for Rench’s rule. Journal of Evolutionary Biology, 40, 194–208.

    Article  Google Scholar 

  • Chittka, L., & Brockmann, A. (2005). Perception space – the final frontier. PLoS Biology, 3, e137.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cox, R. M., Butler, M. A., & John-Alder, H. B. (2007). The evolution of sexual size dimorphism in reptiles. In D. J. Fairbairn, W. U. Blanckenhorn, & T. Székely (Eds.), Sex, size and gender roles: Evolutionary studies of sexual size dimorphism (pp. 38–49). Oxford: Oxford University Press.

    Chapter  Google Scholar 

  • Crawford, N. G., Parham, J. F., Sellas, A. B., Faircloth, B. C., Glenn, T. C., Papenfuss, T. J., Henderson, J. B., Hansen, M. H., & Simison, W. B. (2014). A phylogenomic analysis of turtles. Molecular Phylogenomics and Evolution. doi:10.1016/j.ympev.2014.10.021.

    Google Scholar 

  • Davis, K. M., & Burghardt, G. M. (2007). Training and long-term memory of novel food acquisition task in a turtle (Pseudemys nelsoni). Behavioural Processes, 75, 225–230.

    Article  PubMed  Google Scholar 

  • Davis, K. M., & Burghardt, G. M. (2011). Turtles (Pseudemys nelsoni) learn about visual cues indicating food from experienced turtles. Journal of Comparative Psychology, 125, 404–410.

    Article  PubMed  Google Scholar 

  • Davis, K. M., & Burghardt, G. M. (2012). Long-term retention of visual tasks by two species of emydid turtles, Pseudemys nelsoni and Trachemys scripta. Journal of Comparative Psychology, 126, 213–223.

    Article  PubMed  Google Scholar 

  • Dinets, V., Brueggen, J. C., & Brueggen, J. D. (2013). Crocodilians use tools for hunting. Ethology Ecology & Evolution. doi:10.1080/03949370.2013.858276.

    Google Scholar 

  • Doody, J. S., Stewart, B., Camacho, B., & Christian, K. (2012). Good vibrations? Sibling embryos expedite hatching in a turtle. Animal Behaviour, 83, 645–651.

    Article  Google Scholar 

  • Eisner, T., Conner, W. E., Hicks, K., Dodge, K. R., Rosenberg, H. I., Jones, T. H., Cohen, M., & Meinwald, J. (1977). Stink of Stinkpot turtle identified: ω- Phenylalkanoic acids. Science, 196, 1347–1349.

    Article  CAS  PubMed  Google Scholar 

  • Escalona, T., Valenzuela, N., & Adams, D. C. (2009). Nesting ecology in the freshwater turtle Podocnemis unifilis: spatiotemporal patterns and inferred explanations. Functional Ecology, 23, 826–835.

    Article  Google Scholar 

  • Fairbairn, D. J. (2007). Introduction: The enigma of sexual size dimorphism. In D. J. Fairbairn, W. U. Blanckenhorn, & T. Székely (Eds.), Sex, size and gender roles: Evolutionary studies of sexual size dimorphism (pp. 1–10). Oxford: Oxford University Press.

    Chapter  Google Scholar 

  • Faivre, B., Grégoire, A., Préault, M., Cézilly, F., & Sorci, G. (2003). Immune activation rapidly mirrored in a secondary sexual trait. Science, 300, 103.

    Article  CAS  PubMed  Google Scholar 

  • Ferrara, C. R., Schneider, L., Vogt, R. C., & Burger, J. (2009). The role of receptivity in the courtship behavior of Podocnemis erythrocephala in captivity. Acta Ethologica, 12, 121–125.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ferrara, C. R., Vogt, R. C., & Sous-Lima, R. S. (2012). Turtle vocalizations as the first evidence of posthatching parental care in chelonians. Journal of Comparative Psychology, 127, 24–32.

    Article  PubMed  Google Scholar 

  • Ferrara, C. R., Vogt, R. C., Giles, J. C., & Kuchling, G. (2014). Chelonian vocal communication. In G. Witzany (Ed.), Biocommunication of animals (pp. 261–274). Dordrecht: Springer Science & Business Media.

    Chapter  Google Scholar 

  • Foth, C., Tischlinger, H., & Rauhut, O. W. M. (2014). New specimen of Archaeopteryx provides insights into the evolution of pennaceous feathers. Nature, 511, 79–81.

    Article  CAS  PubMed  Google Scholar 

  • Frankenberg, E. (1982). Vocal behavior of the Mediterranean house gecko Hemidactylus turcicus. Copeia, 4, 770–775.

    Article  Google Scholar 

  • Frazier, J., & Peters, G. (1981). The call of the Aldabra tortoise (Geochelone gigantea) (Reptilia, Testudinidae). Amphibia-Reptilia, 2, 165–179.

    Article  Google Scholar 

  • Gans, C., & Maderson, P. F. A. (1973). Sound producing mechanisms in recent reptiles: review and comment. American Zoologist, 13, 1195–1203.

    Article  Google Scholar 

  • Gardner, M. G., Bull, C. M., Cooper, J. B., & Duffield, G. A. (2001). Genetic evidence for a family structure in stable social aggregations of the Australian lizard Egernia stokesii. Molecular Ecology, 10, 175–183.

    Article  CAS  PubMed  Google Scholar 

  • Garrick, L. D., & Lang, J. W. (1977). Social signals and behaviors of adult alligators and crocodiles. American Zoologist, 17, 225–239.

    Article  Google Scholar 

  • Gibbons, J. W., & Lovich, J. E. (1990). Sexual dimorphism in turtles with emphasis on the slider turtle (Trachemys scripta). Herpetological Monographs, 4, 1–29.

    Article  Google Scholar 

  • Giles, J. C., Davis, J. A., McCauley, R. D., & Kuchling, G. (2009). Voice of the turtle: the underwater acoustic repertoire of the long-necked freshwater turtle, Chelodina oblonga. The Journal of the Acoustical Society of America, 126, 434–443.

    Article  PubMed  Google Scholar 

  • Halpern, M., & Martínez-Marcos, A. (2003). Structure and function of the vomeronasal system: an update. Progress in Neurobiology, 70, 245–318.

    Article  CAS  PubMed  Google Scholar 

  • Hamilton, A. M., Freedman, A. H., & Franz, R. (2002). Effects of deer feeders, habitat and sensory cues on predation rates on artificial turtle nests. American Midland Naturalist, 147, 123–134.

    Article  Google Scholar 

  • Head, M. L., Keogh, J. S., & Doughty, P. (2005). Male southern water skinks (Eulamprus heatwolei) use both visual and chemical cues to detect female sexual receptivity. Acta Ethologica, 8, 79–85.

    Article  Google Scholar 

  • Hoffmeyer, J. (2007). Semiotic scaffolding of living systems. In M. Barbieri (Ed.), Introduction to biosemiotics. The new biological synthesis (pp. 149–166). Dordrecht: Springer.

    Chapter  Google Scholar 

  • Hoffmeyer, J. (2008). The semiotic body. Biosemiotics, 2, 169–190.

    Article  Google Scholar 

  • Hoffmeyer, J. (2014a). The semiome: from genetic to semiotic scaffolding. Semiotica, 198, 11–31.

    Google Scholar 

  • Hoffmeyer, J. (2014b). Semiotic scaffolding: A biosemiotic link between sema and soma. In K. R. Cabell & J. Valsiner (Eds.), The catalyzing mind: Beyond models of causality (pp. 95–110). Dordrecht: Springer.

    Chapter  Google Scholar 

  • Houck, L. D. (2009). Pheromone communication in amphibians and reptiles. Annual Review of Physiology, 71, 161–176.

    Article  CAS  PubMed  Google Scholar 

  • Ibáñez, A., Polo-Cavia, N., López, P., & Martín, J. (2014). Honest sexual signaling in turtles: experimental evidence of a trade-off between immune response and coloration in red-eared sliders Trachemys scripta elegans. Natturwissenschaften, 101, 803–811.

    Article  CAS  Google Scholar 

  • Inouye, C. Y., Hill, G. E., Stradi, R. D., & Montgomerie, R. (2001). Carotenoid pigments in male House finch plumage in relation to age, subspecies, and ornamental coloration. The Auk, 118, 900–915.

    Article  Google Scholar 

  • Jenssen, T. A., Garrett, S., & Sydor, W. J. (2012). Complex signal usage by advertising male Green anoles (Anolis carolinensis): a test of assumptions. Herpetologica, 68, 345–357.

    Article  Google Scholar 

  • Kleisner, K. (2008a). Homosemiosis, mimicry and superficial similarity: notes on the conceptualization of independent emergence of similarity in biology. Theory in Biosciences, 127, 15–21.

    Article  PubMed  Google Scholar 

  • Kleisner, K. (2008b). The semantic morphology of Adolf Portmann: a starting point for the biosemiotics of organic form? Biosemiotics, 1, 207–219.

    Article  Google Scholar 

  • Kleisner, K. (2011). Perceive, co-opt, modify, and live! Organism as a centre of experience. Biosemiotics, 4, 223–241.

    Article  Google Scholar 

  • Kleisner, K. (2015). Semantic organs: the concept and its theoretical ramifications. Biosemiotics. doi:10.1007/s12304-015-9246-z.

    Google Scholar 

  • Kleisner, K., & Maran, T. (2014). Visual communication in animals: Applying Portmannian and Uexküllian biosemiotic approach. In D. Machin (Ed.), Visual communication (pp. 659–676). Berlin: De Gruyter.

    Google Scholar 

  • Komárek, S. (2003). Mimicry, aposematism and related phenomena: Mimetism in nature and the history of its study. München: LIMCOM.

    Google Scholar 

  • Kull, K. (2010). Ecosystems are made of semiosic bonds: consortia, umwelten, biophony and ecological codes. Biosemiotics, 3, 347–357.

    Article  Google Scholar 

  • Lazell, J. D., & Spitzer, N. C. (1977). Apparent play behaviour in an American alligator. Copeia, 1, 188.

    Article  Google Scholar 

  • Leal, M., & Powell, B. J. (2011). Behavioural flexibility and problem-solving in tropical lizard. Biology Letters. doi:10.1098/rsbl.2011.0480.

    PubMed  Google Scholar 

  • Legler, J. M. (1990). The genus Pseudemys in Mesoamerica: Taxonomy, distribution, and origins. In J. W. Gibbons (Ed.), Life history and ecology of the slider turtle (pp. 82–105). Washington, D.C.: Smithsonian Institution Press.

    Google Scholar 

  • Lestel, D. (2011). What capabilities for the animal? Biosemiotics, 4, 83–102.

    Article  Google Scholar 

  • Lindeman, P. V. (2008). Evolution of body size in the map turtles and sawbacks (Emydidae: Deirochelyinae: Graptemys). Herpetologica, 64, 32–46.

    Article  Google Scholar 

  • Liu, Y., Wang, J., Shi, H., Murphy, R. W., Hong, M., He, B., Fong, J. J., Wang, J., & Fu, L. (2009). Ethogram of Sacalia quadriocellata (Reptilia: Testudines: Geoemydidae) in captivity. Journal of Herpetology, 43, 318–325.

    Article  Google Scholar 

  • Liu, Y., Davy, C. M., Shi, H., & Murphy, R. W. (2013). Six in the half-shell: a review of the functions and evolution of courtship behavior in freshwater turtles. Chelonian Conservation and Biology, 12, 84–100.

    Article  Google Scholar 

  • Loew, E. R., & Govardovskii, V. I. (2001). Photoreceptors and visual pigments in the red-eared turtle, Trachemys scripta elegans. Visual Neuroscience, 18, 753–757.

    Article  CAS  PubMed  Google Scholar 

  • Lovich, J. E., Garstka, W. R., & Cooper, W. E., Jr. (1990a). Female participation in courtship behavior of the turtle Trachemys s. scripta. Journal of Herpetology, 24, 422–424.

    Article  Google Scholar 

  • Lovich, J. E., McCoy, C. J., & Garstka, W. R. (1990b). The development and significance of melanism in the slider turtle. In J. W. Gibbons (Ed.), Life history and ecology of the slider turtle (pp. 233–254). Washington, D.C.: Smithsonian Institution Press.

    Google Scholar 

  • Mafli, A., Wakamatsu, K., & Roulin, A. (2011). Melanin-based coloration predicts aggressiveness and boldness in captive eastern Hermann’s tortoises. Animal Behaviour, 81, 859–863.

    Article  Google Scholar 

  • Maran, T. (2011). Becoming a sign: the mimic’s activity in biological mimicry. Biosemiotics, 4, 243–257.

    Article  Google Scholar 

  • Maran, T. (2015). Scaffolding and mimicry: a semiotic view of the evolutionary dynamics of mimicry systems. Biosemiotics. doi:10.1007/s12304-014-9223-y.

    Google Scholar 

  • Maran, T., & Kleisner, K. (2010). Towards an evolutionary biosemiotics: semiotic selection and semiotic co-option. Biosemiotics, 3, 189–200.

    Article  Google Scholar 

  • Marcellini, D. (1977). Acoustic and visual display behaviour of gekkonid lizards. American Zoologist, 17, 251–260.

  • Martínez, A., & Barbosa, A. (2010). Are pterins able to modulate oxidative stress? Theoretical Chemistry Accounts, 127, 485–492.

    Article  CAS  Google Scholar 

  • Martínez, M., & Esposito, M. (2014). Multilevel causation and the extended synthesis. Biological Theory, 9, 209–220.

    Article  Google Scholar 

  • Martins, E. P. (1994). Structural complexity in a lizard communication system: the Scleroporus graciosus “push-up” display. Copeia, 4, 944–955.

    Article  Google Scholar 

  • Mason, R. T., & Parker, M. R. (2010). Social behavior and pheromonal communication in reptiles. Journal of Comparative Physiology A, 196, 729–749.

    Article  CAS  Google Scholar 

  • McGraw, K. J. (2005). The antioxidant function of many animal pigments: are there consistent health benefits of sexually selected colourants? Animal Behaviour, 69, 757–764.

    Article  Google Scholar 

  • Moll, E. O., Matson, K. E., & Krehbiel, E. B. (1981). Sexual and seasonal dichromatism in the Asian river turtle Callagur borneoensis. Herpetologica, 37, 181–194.

    Google Scholar 

  • Mueller-Paul, J., Wilkinson, A., Steuer, M., Hall, G., & Huber, L. (2014). Touchscreen performance and knowledge transfer in the red-footed tortoise (Chelonoidis carbonaria). Behavioural Processes, 106, 187–192.

    Article  PubMed  Google Scholar 

  • Muñoz, A. (2004). Chemo-orientation using conspecific chemical cues in the stripe-necked terrapin. Journal of Chemical Ecology, 30, 519–530.

    Article  PubMed  Google Scholar 

  • Noble, D. W. A., Byrne, R. W., & Whiting, M. J. (2014). Age-dependent social learning in a lizard. Animal Behaviour. doi:10.1098/rsbl.2014.0430.

    Google Scholar 

  • Owens, D. W., Grassman, M. A., & Hendrickson, J. R. (1982). The imprinting hypotheses and sea turtle reproduction. Herpetologica, 38, 124–135.

    Google Scholar 

  • Paradis, E., Claude, J., & Strimmer, K. (2004). APE: analyses of phylogenetics and evolution in R language. Bioinformatics. doi:10.1093/bioinformatics/btg412.

    PubMed  Google Scholar 

  • Patterson, R. (1971). Aggregation and dispersal behavior in captive Gopherus agassizi. Journal of Herpetology, 5, 214–216.

    Article  Google Scholar 

  • Patterson, R. (1976). Vocalization in the Desert tortoise. In N. J. Engberg, S. Allan, & R. L. Young (Eds.), Desert Tortoise Council proceedings of 1976 symposium (pp. 77–80). Las Vegas: Desert Tortoise Council.

    Google Scholar 

  • Polo-Cavia, N., López, P., & Martín, J. (2009). Interspecific differences in chemosensory responses of freshwater turtles: consequences for competition between native and invasive species. Biological Invasions, 11, 431–440.

    Article  Google Scholar 

  • Polo-Cavia, N., López, P., & Martín, J. (2013). Head coloration reflects health state in the red-eared slider Trachemys scripta elegans. Behavioral Ecology and Sociobiology, 67, 153–162.

    Article  Google Scholar 

  • Portmann, A. (1960). Die Tiergestalt. Studien über die Bedeutung der tierischen Ercheinung. Basel: Friedrich Reinhardt.

    Google Scholar 

  • Price, A. H. (1988). Observations on maternal behaviour and neonate aggregation in the Western diamondback rattlesnake, Crotalus atrox (Crotalidae). The Southwestern Naturalist, 33, 370–373.

    Article  Google Scholar 

  • Prum, R. O. (2012). Aesthetic evolution by mate choice: Darwin’s really dangerous idea. Philosophical Transactions of the Royal Society, B: Biological Sciences, 367, 2253–2265.

    Article  PubMed Central  Google Scholar 

  • Puts, D. A. (2010). Beauty and the beast: mechanisms of sexual selection in humans. Evolution and Human Behavior, 31, 157–175.

    Article  Google Scholar 

  • R Development Core Team. (2013). R: A language and environment for statistical computing. Vienna: R foundation for Statistical Computing.

    Google Scholar 

  • Regnier, F. E. (1971). Semiochemicals - structure and function. Biology of Reproduction, 4, 309–326.

    CAS  PubMed  Google Scholar 

  • Revell, L. J. (2012). phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217–223.

    Article  Google Scholar 

  • Robinson, C. D. (2014). Convergence in communication behavior and brain morphology in lizards: An evolutionary approach. Trinity University: Biology Honors Theses, Department of Biology.

  • Rosenblatt, J. S. (2003). Outline of the evolution of behavioral and nonbehavioral patterns of parental care among the vertebrates: critical characteristics of mammalian and avian parental behavior. Scandinavian Journal of Psychology, 44, 265–271.

    Article  PubMed  Google Scholar 

  • Rowe, C. (1999). Receiver psychology and the evolution of multicomponent signals. Animal Behavior, 58, 921–931.

    Article  Google Scholar 

  • Rowe, J. W., Clark, D. L., Price, M., & Tucker, J. K. (2009). Reversible melanization following substrate color reversal in Midland painted turtles (Chrysemys picta marginata) and Red-eared sliders (Trachemys scripta elegans). Journal of Herpetology, 43, 402–408.

    Article  Google Scholar 

  • Ryan, M. J. (1998). Sexual selection, receiver biases, and the evolution of the sex differences. Science, 281, 1999–2003.

    Article  CAS  PubMed  Google Scholar 

  • Ryan, M. J. (2011). The brain as a source of selection on the social niche: examples from thy psychophysics of mate choice in tungara frogs. Integrative and Comparative Biology, 51, 756–770.

    Article  PubMed  Google Scholar 

  • Ryan, M. J., & Cummings, M. E. (2013). Perceptual biases and mate choice. Annual Review of Ecology, Evolution, and Systematics, 44, 437–459.

    Article  Google Scholar 

  • Sacchi, R., Galeotti, P., Fasola, M., & Ballasina, D. (2003). Vocalizations and courtship intensity with mounting success in marginated tortoises Testudo marginata. Behavioral Ecology and Sociobiology, 55, 95–102.

    Article  Google Scholar 

  • Sachsse, W. (1969). Über Bewegungsweisen, Beuteerwerb und Lautäusserung bei der Grosskopfschildkröte (Platysternon megacephalum). Salamandra, 5, 150–152.

    Google Scholar 

  • Saks, L., McGraw, K., & Hõrak, P. (2003). How feather color reflects its carotenoid content. Functional Ecology, 17, 555–561.

    Article  Google Scholar 

  • Sereno, P. C. (1991). Basal archosaurs: phylogenetic relationships and functional implications. Memoir (Society of Vertebrate Paleontology), 2, 1–53.

    Article  Google Scholar 

  • Shaffer, H. B., Minx, P., Warren, D. E., Sheldock, A. M., Thomson, R. C., Valenzuela, N., Abramyan, J., Amemiya, C. T., Badenhorst, D., Biggar, K. K., Borchert, G. M., Botka, C. W., Bowden, R. M., Braun, E. L., Bronikowski, A. M., Bruneau, B. G., Buck, L. T., Capel, B., Castoe, T. A., Czerwinski, M., Delehaunty, K. D., Edwards, S. V., Fronick, C. C., Fujita, M. K., Fulton, L., Graves, T. A., Green, R. E., Haerty, W., Hariharan, R., Hernandez, O., Hillier, L. W., Holloway, A. K., Janes, D., Janzen, F. J., Kandoth, C., Kong, L., Koning, A. P. J., Li, Y., Literman, R., McGaugh, S. E., Mork, L., O’Laughlin, M., Paitz, R. T., Pollock, D. D., Ponting, C. P., Radhakrishnan, S., Raney, B. J., Richman, J. M., St. John, J., Schwarz, T., Sethuraman, A., Spinks, P. Q., Storey, K. B., Thane, N., Vinar, T., Zimmerman, L. M., Warren, W. C., Mardis, E. R., & Wilson, R. K. (2013). The western painted turtle genome, a model for the evolution of extreme physiological adaptations in slowly evolving lineage. Genome Biology. doi:10.1186/gb-2013-14-3-r28. http://genomebiology.com/2013/14/3/R28.

    PubMed  Google Scholar 

  • Steffen, J. E., & McGraw, K. J. (2007). Contributions of pterin and carotenoid pigments to dewlap coloration in two anole species. Comparative Biochemistry and Physiology, Part B, 146, 42–46.

    Article  CAS  Google Scholar 

  • Stella, M., & Kleisner, K. (2010). Uexküllian umwelt as science and as ideology: the light and the dark side of a concept. Theory in Biosciences, 129, 39–51.

    Article  CAS  PubMed  Google Scholar 

  • Stirling, I. (1975). Factors affecting the evolution of social behavior in pinnipedia. Rapports et procès-verbaux des reunions/ Conseil permanent international pour l’exploration de la mer, 169, 205–212.

    Google Scholar 

  • Strauss, B. (2002). Social facilitation in motor tasks: a review of research and theory. Psychology of Sport and Exercise, 3, 237–256.

    Article  Google Scholar 

  • Stuart-Fox, D., & Moussalli, A. (2008). Selection for social signaling drives the evolution of chameleon color change. PLoS Biology. doi:10.1371/journal.pbio.0060025.

    PubMed  PubMed Central  Google Scholar 

  • Thayer, A. H. (1896). The law which underlies protective coloration. The Auk, 13, 124–129.

    Article  Google Scholar 

  • Thomas, R. B. (2002). Conditional mating strategy in long-lived vertebrate: Ontogenic shifts in the mating tactics of male slider turtles (Trachemys scripta). Copeia, 2, 456–461.

    Article  Google Scholar 

  • Tønnessen, M. (2010). Wolf land. Biosemiotics, 3, 289–297.

    Article  Google Scholar 

  • Veselovský, Z. (2005). Etologie: Biologie chování zvířat. Praha: Academia.

    Google Scholar 

  • Vetter, H. (2004). TERRALOG: Turtles of the World Vol. 2 North America – Schildkröten der Welt Band 2 Nordamerika. Frankfurt am Main/Rodgau: Edition Chimaira/Verlag ACS Gmbh (AQUALOG).

  • Vetter, H. (2005). TERRALOG: Turtles of the World Vol. 3 Central and South America - Schildkröten der Welt Band 3 Mittel- und Südamerika. Frankfurt am Main/Rodgau: Edition Chimaira/Verlag ACS Gmbh (AQUALOG).

  • Vetter, H. (2011). TERRALOG: Turtles of the World Vol. 1 Africa, Europe and Western Asia - Schildkröten der Welt Band 1 Africa, Europa und Westasien. Frankfurt am Main/Rodgau: Edition Chimaira/Verlag ACS Gmbh (AQUALOG).

  • Vetter, H.& van Dijk, P. P. (2006). TERRALOG: Turtles of the World Vol. 4 East and South Asia - Schildkröten der Welt Band 4 Ost- und Südasien. Frankfurt am Main/Rodgau: Edition Chimaira/Verlag ACS Gmbh (AQUALOG).

  • Vitousek, M. N., Adelman, J. S., Gregory, N. C., & St Clair, J. J. H. (2007). Heterospecific alarm call recognition in a non-vocal reptile. Biology Letters, 3, 632–634.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vogt, R. C. (1993). Systematics of the false map turtles (Graptemys pseudogeographica complex: Reptilia, Testudines, Emydidae). Annals of Carnegie Museum, 62, 1–46.

    Google Scholar 

  • Vogt, R. C., & Bull, J. J. (1982). Temperature controlled sex-determination in turtles: ecological and behavioral aspects. Herpetologica, 38, 156–164.

    Google Scholar 

  • von Uexküll, J. (1921). Umwelt und Innenwelt der Tiere. Berlin: Springer.

    Book  Google Scholar 

  • Wang, X., Wang, D., Zhang, S., Wang, C., Wang, R., & Wu, X. (2009). Why do Chinese alligators (Alligator sinensis) form bellowing choruses: a playback approach. The Journal of Acoustical Society of America, 126, 2082–2087.

    Article  Google Scholar 

  • Wang, J.-C., Yang, C.-C., Liang, W., & Shi, H.-T. (2013a). Spectra analysis reveals the sexual dichromatism of red-eared slider turtle. (Trachemys scripta). Zoological research, 34, 475–478.

    CAS  PubMed  Google Scholar 

  • Wang, Z., Pascual-Anaya, J., Zadissa, A., Li, W., Niimura, Y., Huang, Z., Li, C., White, S., Xiong, Z., Fang, D., Wang, B., Ming, Y., Chen, Y., Zheng, Y., Kuraku, S., Pignatelli, M., Herrero, J., Beal, K., Masafumi, N., Li, Q., Wang, J., Zhang, H., Yu, L., Shigenobu, S., Wang, J., Liu, J., Flicek, P., Searle, S., Wang, J., Kuratani, S., Yin, Y., Aken, B., Zhang, G., & Irie, N. (2013b). The draft genomes of soft-shell turtle and green sea turtle yield insights into the development and evolution of the turtle-specific body plan. Nature Genetics. doi:10.1038/ng.2615.

    Google Scholar 

  • Weber, E., & Werner, Y. L. (1977). Vocalizations of two snake-lizards (Reptilia: Sauria: Pygopodidae). Herpetologica, 33, 353–363.

    Google Scholar 

  • Weiss, S. L., Kennedy, E. A., Safran, R. J., & McGraw, K. J. (2011). Pterin-based ornamental coloration predicts yolk antioxidant levels in female striped plateau lizards (Scleroporus virgatus). Journal of Animal Ecology, 80, 519–527.

    Article  PubMed  Google Scholar 

  • Wilkinson, A., Chan, H. M., & Hall, G. (2007). Spatial learning and memory in the tortoise (Geochelone carbonaria). Journal of Comparative Psychology, 121, 412–418.

    Article  PubMed  Google Scholar 

  • Wilkinson, A., Mandl, I., & Bugnyar, T. (2010). Gaze following in the red-footed tortoise (Geochelone carbonaria). Animal Cognition, 13, 765–769.

    Article  PubMed  Google Scholar 

  • Wilkinson, A., Mueller-Paul, J., & Huber, L. (2013). Picture-object recognition in the tortoise (Chelonoidis carbonaria). Animal Cognition, 16, 99–107.

    Article  PubMed  Google Scholar 

  • Young, B. A. (2003). Snake bioacoustics: toward a richer understanding of the behavioral ecology of snakes. The Quarterly Review of Biology, 78, 303–325.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Servicio de Vida Silvestre, D.G. Medi Natural de la Generalitat Valenciana and their project ‘Strategy and proven techniques for the eradication of freshwater invaders’, project ‘LIFE-Trachemys’ (LIFE09 NAT/ES000529), for their kind collaboration and for providing us with space for thinking. Further, we owe our thanks to Lucie Čermáková for drawing the illustrations of turtles’ heads. Our research was supported by the Czech Grant Agency project GACR P505/11/1459. We dedicate this publication in memoriam to Prof. Vojtěch Jarošík.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jindřich Brejcha.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brejcha, J., Kleisner, K. Turtles Are Not Just Walking Stones: Conspicuous Coloration and Sexual Selection in Freshwater Turtles. Biosemiotics 9, 247–266 (2016). https://doi.org/10.1007/s12304-015-9249-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12304-015-9249-9

Keywords

Navigation