Chelonian Vocal Communication

  • Camila R. Ferrara
  • Richard C. Vogt
  • Jacqueline C. Giles
  • Gerald Kuchling

Abstract

Recently it was discovered that freshwater turtles communicate underwater by sound. The vocal repertoire of the Western Australian longneck turtle Chelodina colliei includes complex and percussive calls which are harmonically structured and frequency modulated, with dominant frequencies below 1 kHz and a range from around 100 to 3.5 kHz. Sounds with similar characteristics are used by the females of the South American river turtle Podocnemis expansa when migrating to nesting beaches and during communal nesting. Near term embryos inside eggs vocalize, and hatchlings emerging from nests and scampering across the beach and into the river continue to vocalize. In the water the adult females respond and the hatchlings then migrate with the females down the river, presumably to the flooded forests where they feed. Many unexplained aspects of aquatic turtles social behavior may eventually be explained when their vocalizations have been studied.

Keywords

Sound Absorption Acoustic Communication Freshwater Turtle Nest Beach Vocal Repertoire 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Alho CJR, Pádua FM (1982) Reproductive parameters and nesting behavior of the Amazon turtle Podocnemis expansa (Testudinata: Pelomedusidae) in Brazil. Can J Zool 60:97–103CrossRefGoogle Scholar
  2. Auffenberg W (1964) Notes on the courtship of the land tortoise Geochelone travancorica (Boulenger). J Bombay Nat Hist Soc 61:247–253Google Scholar
  3. Auffenberg W (1965) Sex and species discrimination in two sympatric South American tortoises. Copeia 1965:335–342CrossRefGoogle Scholar
  4. Auffenberg W (1977) Display behavior in tortoises. Am Zool 17:241–250Google Scholar
  5. Auffenberg W (1978) Courtship and breeding behaviour in Geochelone radiata (testudines: Testudinidae). Herpetologica 34:277–287Google Scholar
  6. Berry JF, Shine R (1980) Sexual size dimorphism and sexual selection in turtles (order Testudines). Oecologia 44:185–191CrossRefGoogle Scholar
  7. Bradbury JW, Vehrencamp S (1998) Principles of animal communication. Sinauer Associates, SunderlandGoogle Scholar
  8. Brito E, Strussmann C, Baicere-Silva CM (2009) Courtship behavior of Mesoclemmys vanderhaegei (Bour, 1973) (Testudines: Chelidae) under natural conditions in the Brazilian Cerrado. Herpetol Notes 2:67–72Google Scholar
  9. Britton ARC (2001) Review and classification of call types of juvenile crocodilians and factors affecting distress calls. In: Grigg GC, Seebacher F, Franklin CE (eds) Crocodilian biology and evolution. Surrey Beatty & Sons, Chipping Norton, pp 364–377Google Scholar
  10. Campbell HW (1967) Stop, look, and listen. Acoustic behaviour of turtles. J Int Turt Tortoise Soc 1:13–44Google Scholar
  11. Campbell HW (1972) Observations on the vocal behavior of Chelonians. Herpetologica 28:277–280Google Scholar
  12. Campbell HW, Evans WE (1967) Sound production in two species of tortoises. Herpetologica 23:204–209Google Scholar
  13. Carpenter CC (1980) An ethological approach to reproductive success in reptiles. In: Murphy JB, Collins JT (eds) Reproductive biology and diseases of captive reptiles, Contributions to herpetology no. 1. Society for the Study Amphibians Reptiles, Oxford, pp 33–48Google Scholar
  14. Carr AFJ (1952) Handbook of turtles. Comstock, IthacaGoogle Scholar
  15. Cohen MA (1994) Russian tortoise, Testudo horsfieldii. Tortuga Gaz 30:4Google Scholar
  16. Connor MJ, Wheeler V (1998) The Chinese box turtle, Cistoclemmys flavomarginata Gray 1863. Tortuga Gaz 34:1–7Google Scholar
  17. Cook SL, Forrest TG (2005) Sounds produced by nesting Leatherback sea turtles (Dermochelys coriacea). Herpetol Rev 36:387–390Google Scholar
  18. Cope ED (1865) Third contribution to the herpetology of tropical America. Proc Natl Acad Sci U S A 173:185–196Google Scholar
  19. Ernst CH, Barbour RW (1989) Turtles of the world. Smithsonian Institution Press, Washington, DCGoogle Scholar
  20. Evans WE (1949) The reproductive behaviour of the giant tortoises T. vicinia and T. vandenberghii. Anat Rec 105:579Google Scholar
  21. Ferrara CR (2012) Comunicação acústica em tartaruga-da-amazônia (Podocnemis expansa (Schweigger, 1812) Testudines: Podocnemididae) na Reserva Biológica do rio Trombetas, Pará, Brasil. PhD thesis, Instituto Nacional de Pesquisas da Amazônia, Amazon, Brazil, 111 ppGoogle Scholar
  22. Ferrara CR, Schneider L, Burger J, Vogt RC (2009) The role of receptivity in the courtship behavior of Podocnemis erythrocephala in captivity. Acta Ethol 12:121–125PubMedCrossRefGoogle Scholar
  23. Ferrara CR, Vogt RC, Sousa-Lima RS (2012) Turtle vocalizations as the first evidence of post-hatching parental care in chelonians. Q J Exp Psychol B Comp Physiol Psychol 2012:1–9Google Scholar
  24. Ferrara CR, Vogt RC, Harfush MR, Sousa-Lima, RS, Albavera E, Tavera A (in press) First evidence of Dermochelys coriacea emitting sound from unpipped eggs. Chelonian Conserv BiolGoogle Scholar
  25. Flower SS (1899) Notes on a second collection of reptiles made in the Malay Peninsula and Siam, from November 1896 to September 1898, with a list of species recorded from those countries. Proc Zool Soc (Lond) 1899:600–696Google Scholar
  26. Forrest TG (1994) From sender to receiver: propagation and environmental effects on acoustic signals. Am Zool 34:644–654Google Scholar
  27. Forrest TG, Miller GL, Zagar JR (1993) Sound propagation in shallow water: implications for acoustic communication by aquatic animals. Bioacoust Int J Anim Sound Rec 4:259–270Google Scholar
  28. Frazier J, Peters G (1982) The call of the Aldabra tortoise (Geochelone gigantea) (Reptilia, Testudinidae). Amphib-Reptil 2:165–179CrossRefGoogle Scholar
  29. Galeotti P, Sacchi R, Fasola M, Peellitteri Rosa D, Fasola M (2004) Female preference for fast-rate, high-pitched calls in Hermann’s tortoises Testudo hermanni. Behav Ecol 16:301–308CrossRefGoogle Scholar
  30. Galeotti P, Sacchi R, Fasola M, Ballasina D (2005a) Do mounting in tortoises have a communication function? A comparative analysis. Herpetol J 15:61–71Google Scholar
  31. Galeotti P, Sacchi R, Fasola M, Pellitteri D, Rosa DP, Marchesi M, Ballasina D (2005b) Courtship displays and mounting calls are honest condition-dependent signals that influence mounting success in Hermann’s tortoises. Can J Zool 83:1306–1313CrossRefGoogle Scholar
  32. Gelfand DL, McCracken GF (1986) Individual variation in the isolation calls of Mexican free-tailed bat pups (Tadarida brasiliensis mexicana). Anim Behav 34:1078–1086CrossRefGoogle Scholar
  33. Giles J (2006) The underwater acoustic repertorie of the long-necked, freshwater turtle Chelodina oblonga. PhD thesis, School of Environmental Science, Murdoch University, Perth, Australia, 224 ppGoogle Scholar
  34. Giles JC, Davis JA, McCauley RD, Kuchling G (2009) Voice of the turtle: the underwater acoustic repertoire of the long-necked freshwater turtle, Chelodina oblonga. J Acoust Soc Am 126:434–443PubMedCrossRefGoogle Scholar
  35. Goode J (1967) Freshwater tortoises of Australia and New Guinea (in the family Chelidae). Lansdowne Press, MelbourneGoogle Scholar
  36. Grubb P (1971) Comparative notes on the behaviour of Geochelone sulcata. Herpetologica 27:328–332Google Scholar
  37. Gunther A (1864) Reptiles of British India. Robert Hardwicks, LondonGoogle Scholar
  38. Halliday TR, Slater PJB (1983) Animal behavior, vol 2, Communication. Blackwell Scientific Publications, OxfordGoogle Scholar
  39. Harless M (1979) Social behavior. In: Harless M, Morlock H (eds) Turtles perspectives and research. Wiley, New York/Chichester/Brisbane/Toronto, pp 475–492Google Scholar
  40. Herzog HA, Burghardt GM (1977) Vocalization in juvenile crocodilians. Z Tierpsychol 44:294–304PubMedGoogle Scholar
  41. Hine M (1982) Notes on the marginated tortoise (Testudo marginata) in Greece and captivity. Bull Br Herpetol Soc 5:35–38Google Scholar
  42. Hoofien JH (1971) The voices of snake and tortoises. Israel J Zool 20:148Google Scholar
  43. Ibáñez A, Pilar L, Martín J (2012) Discrimination of conspecifics’ chemicals may allow Spanish terrapins to find better partners and avoid competitors. Anim Behav 83:1107–1113CrossRefGoogle Scholar
  44. Jackson CG, Awbrey FT (1972) Mating bellows of the Galapagos Tortoise, Geochelone elephantopus. Herpetologica 34:134–136Google Scholar
  45. Jackson CG, Davis JD (1972) A quantitative study of the courtship display of the red-eared turtle, Chrysemys scripta elegans. Herpetologica 28:58–64Google Scholar
  46. Kaufmann JH (1992) The social behaviour of Wood Turtles, Clemmys insculpta, in Central Pennsylvania. Herpetol Monogr 6:1–25CrossRefGoogle Scholar
  47. Kiester AR (1977) Communication in amphibians and reptiles. In: Sebeok TA (ed) How animals communicate? Indiana University Press, Bloomington, pp 519–544Google Scholar
  48. Kirkpatrick DT (1998) African hingeback tortoises of the genus Kinixys. Reptile Amphib Mag 54:32–37Google Scholar
  49. Krebs JR, Davis NB (1993) An introduction to behavioral ecology. Blackwell Science Press, CambridgeGoogle Scholar
  50. Kuchling G (1999) The reproductive biology of the chelonia, Zoophysiol 38. Springer, Berlin/Heidelberg/New YorkCrossRefGoogle Scholar
  51. Kumpf HE (1964) Use of underwater television in bioacoustic research. In: Marine bio-acoustic. Pergamon Press, New York, pp 45–57Google Scholar
  52. Mahmoud IY (1967) Courtship behavior and sexual maturity in four species of Kinosternid turtles. Copeia 1967:314–319CrossRefGoogle Scholar
  53. Marler PR (1977) The structure of animal communication sounds. In: Bullock TH (ed) Recognition of complex acoustic signals. Verlagsgellschaft Konferenzen, Berlin, pp 17–36Google Scholar
  54. Marler P, Slabbkoorn H (2004) Nature’s music: the science of birdsong. Elsevier Academic Press, AmsterdamGoogle Scholar
  55. Marten K, Marler P (1977) Sound transmission and its significance for animal vocalisation. I. Temperate habitats. Behav Ecol Sociobiol 2:271–290CrossRefGoogle Scholar
  56. McCormick B (1992) The elongated tortoise, Indotestudo elongata. Tortuga Gaz 28:1–3Google Scholar
  57. McKeown S, Meier DE, Juvik JO (1990) The management and breeding of the Asian Forest Tortoise (Manouria emys) in captivity. In: Beaman KR, Caporaso F, McKeown S, Graff MD (eds) Proceedings of the first international symposium on turtles and tortoises: conservation and captive husbandry. California Turtle & Tortoise Club, Van Nuys, Los Angeles, CA, pp 138–159Google Scholar
  58. Morris L (1974) Western hinge-back tortoise, Kinixys belliana nogueyi. Tortuga Gaz 30:1–3Google Scholar
  59. Morton ES (1977) On the occurrence and significance of motivation-structural rules in some birds and mammal sounds. Am Nat 111:855–869CrossRefGoogle Scholar
  60. Mrosovsky N (1972) Spectrographs of the sounds of Leatherback Turtles. Herpetologica 28:256–258Google Scholar
  61. Neil WT (1950) Sound produced by the Suwanee terrapin. Copeia 1950:52CrossRefGoogle Scholar
  62. Nummela S, Thewissen JGM (2008) The physics of sound in air and water. In: Thewissen JGM, Nummela S (eds) Sensory evolution on the threshold: adaptations in secondarily aquatic vertebrates. University of California Press, Berkeley, pp 175–181Google Scholar
  63. Olsson M, Madsen T (1998) Sexual selection and sperm competition in reptiles. In: Birkhaed TR, Moller AP (eds) Sperm competition and sexual selection. Morgan Kaufmann, Stockholm, pp 503–564CrossRefGoogle Scholar
  64. Palmer M (1994) The speckled tortoise, Homopus signatus, in captivity. Tortuga Gaz 30:1–5Google Scholar
  65. Pellitteri-Rosa D, Sacchi R, Galeotti P, Marchesi M, Fasola M (2011) Courtship displays are condition-dependent signals that reliably reflect male quality in Greek tortoises, Testudo graeca. Chelonian Conserv Biol 10:10–17CrossRefGoogle Scholar
  66. Pope CH (1939) Turtles of the United States & Canada. AA Knopf, New YorkGoogle Scholar
  67. Pope CH (1955) The reptile world. AA Knopf, New YorkGoogle Scholar
  68. Rogers PH, Cox M (1988) Underwater sound as a biological stimulus. In: Atema J, Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, New York, pp 131–140CrossRefGoogle Scholar
  69. Sacchi R (2004) Riproduzione nei Cheloni: aspetti morfologici, ematologici e comportamentali legati alle vocalizzazioni. PhD dissertation, University of Pavia, Pavia, ItalyGoogle Scholar
  70. Sacchi R, Galeotti P, Fasola M, Ballasina D (2003) Vocalizations and courtship intensity correlate with mounting success in marginated tortoises Testudo marginata. Behav Ecol Sociobiol 55:95–102CrossRefGoogle Scholar
  71. Seidel ME, Fritz U (1997) Courtship behavior provides additional evidence for a monophyletic Pseudemys, and comments on mesoamerican Trachemys (Testudines: Emydidae). Herpetol Rev 28:70–72Google Scholar
  72. Stacey NE, Kyle AL, Liley NR (1986) Fish reproductive pheromones. In: Chemical signals in vertebrates. Plenum, New York, pp 117–134Google Scholar
  73. Tyack PL (2001) Bioacoustics. In: Encyclopaedia of ocean sciences. Woods Hole Oceanographic Institution, Woods Hole, pp 295–302CrossRefGoogle Scholar
  74. Urick RJ (1983) Principles of underwater sound, 3rd edn. McGraw Hill Book Company, New YorkGoogle Scholar
  75. Vince MA (1968) Retardation as a factor in the synchronization of hatching. Anim Behav 16:332–335PubMedCrossRefGoogle Scholar
  76. Vogt RC (1993) Systematics of the false map turtles (Graptemys pseudogeographica complex: Reptilia, Testudines, Emydidae). Ann Carnegie Mus 62:1–46Google Scholar
  77. Vogt RC (2008) Amazon turtles. Bíblios, LimaGoogle Scholar
  78. Wever WG Jr (1970) Courtship and combat behaviour in Gopherus berlandieri. Bull Fla State Mus 15:1–43Google Scholar
  79. Wever EG (1978) Order testudines: the turtles. In: Wever EG (ed) The reptile ear: its structure and function. Princeton University Press, Princeton, pp 833–922Google Scholar
  80. Wiley RH, Richards DG (1978) Physical constraints on acoustic communication in the atmosphere: implications for the evolution of animal vocalisations. Behav Ecol Sociobiol 3:69–94CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Camila R. Ferrara
    • 1
  • Richard C. Vogt
    • 2
  • Jacqueline C. Giles
    • 3
  • Gerald Kuchling
    • 4
  1. 1.Aquatic BiologyWildlife Conservation Society - WCS BrazilRio de JaneiroBrazil
  2. 2.Curator of Reptiles and Amphibians, Department of BiodiversityInstituto Nacional de Pesquisas da Amazônia - INPAPetrópolis, ManausBrazil
  3. 3.PerthAustralia
  4. 4.School of Animal BiologyThe University of Western AustraliaPerthAustralia

Personalised recommendations