Size does matter: crocodile mothers react more to the voice of smaller offspring

T. Chabert; A. Colin; T. Aubin; V. Shacks; S. L. Bourquin; R. M. Elsey; J. G. Acosta; N. Mathevon

doi:10.1038/srep15547

journal article Open Access Oct 23, 2015

Size does matter: crocodile mothers react more to the voice of smaller offspring

T. Chabert A. Colin T. Aubin V. Shacks S. L. Bourquin R. M. Elsey J. G. Acosta N. Mathevon

Scientific Reports Vol. 5 No. 1 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/srep15547

Abstract

AbstractParental care is widespread in Archosaurs (birds, crocodilians, dinosaurs and pterosaurs) and this group provides a useful model for the evolution of parent-offspring interactions. While offspring signalling has been well-studied in birds, the modulation of parental care in crocodilians remains an open question. Here we show that acoustic communication has a key role in the dynamics of crocodilian’ mother-offspring relationships. We found embedded information about the emitter’s size in juvenile calls of several species and experimentally demonstrated that Nile crocodile mothers breeding in the wild are less receptive to the calls of larger juveniles. Using synthetized sounds, we further showed that female’ reaction depends on call pitch, an important cue bearing size information. Changes in acoustic interactions may thus go with the break of maternal care as well as dispersal of juvenile crocodilians. This process could have characterized other archosaurs displaying rapid early growth such as dinosaurs and pterosaurs.

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References

59

[1]

Janke, A. & Arnason, U. The complete mitochondrial genome of Alligator mississippiensis and the separation between recent archosauria (birds and crocodiles). Mol. Biol. Evol. 14, 1266–1272 (1997). 10.1093/oxfordjournals.molbev.a025736

[2]

Grigg, G. & Kirshner, D. Biology and Evolution of Crocodylians (Cornell University Press, 2015). 10.1071/9781486300679

[3]

Zhang, G., Jarvis, E. D. & Gilbert, M. T. P. A flock of genomes. Science 346, 1308–1309 (2014). 10.1126/science.346.6215.1308

[4]

Emery, N. J., Seed, A. M., von Bayern, A. M. & Clayton, N. S. Cognitive adaptations of social bonding in birds. Philos. Trans. R. Soc. B 362, 489–505 (2007). 10.1098/rstb.2006.1991

[5]

Dinets, V. Apparent coordination and collaboration in cooperatively hunting crocodilians. Ethol. Ecol. Evol. 2, 244–250 (2014).

[6]

Nowicki, S. & Searcy, W. A. The evolution of vocal learning. Curr. Opin. Neurobiol. 28, 48–53 (2014). 10.1016/j.conb.2014.06.007

[7]

Liu, W., Wada, K., Jarvis, E. D. & Nottebohm, F. Rudimentary substrates for vocal learning in a suboscine. Nat. Com. 4, 2082 (2013). 10.1038/ncomms3082

[8]

Brochu, C. A. Phylogenetic approaches toward crocodylian history. Annu. Rev. Earth Planet. Sci. 31, 357–397 (2003). 10.1146/annurev.earth.31.100901.141308

[9]

Larsson, H. C. E., Heppleston, A. C. & Elsey, R. M. Pentadactyl ground state of the manus of Alligator mississipiensis and insights into the evolution of digital reduction in Archosauria. J. Exp. Zool. (Mol. Dev. Evol.) 314B, 571–579 (2010). 10.1002/jez.b.21362

[10]

Meredith, R. W. et al. A phylogenetic hypothesis for Crocodylus (Crocodylia) based on mitochondrial DNA: Evidence for a trans-Atlantic voyage from Africa to the New World. Mol. Phyl. Evol. 60, 183–191 (2011). 10.1016/j.ympev.2011.03.026

[11]

Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs

Richard E. Green, Edward L. Braun, Joel Armstrong et al.

Science 2014 10.1126/science.1254449

[12]

Senter, P. Homology between and antiquity of stereotyped communicatory behaviors of crocodilians. J. Herpetol. 42, 354–360 (2008). 10.1670/07-150.1

[13]

Brazaitis, P. & Watanabe, M. E. Crocodilian behaviour: a window to dinosaur behaviour? Hist. Biol. 23, 73–90 (2011). 10.1080/08912963.2011.560723

[14]

Brochu, C. A. Progress and future directions in Archosaur phylogenetics. J. Paleont. 75, 1185–1201 (2001). 10.1017/s0022336000017236

[15]

Cockburn, A. Prevalence of different modes of parental care in birds. Proc. R. Soc. B 273, 1375–1383 (2006). 10.1098/rspb.2005.3458

[16]

Trutnau, L. & Sommerlad, R. Crocodilians: Their Natural History & Captive Husbandry (Chimaira, 2006).

[17]

Somaweera, R., Brien, M. & Shine, R. The role of predation in shaping crocodilian natural history. Herpetological Monographs 27, 23–51 (2013). 10.1655/herpmonographs-d-11-00001

[18]

Horner, J. R. & Makela, R. Nest of juveniles provides evidence of family structure among dinosaurs. Nature 282, 296–298 (1979). 10.1038/282296a0

[19]

Carpenter, K. Eggs, nests and baby dinosaurs: a look at dinosaur reproduction (Indiana University Press, 1999).

[20]

Horner, J. R. Dinosaur reproduction and parenting. Annu. Rev. Earth Planet. Sci. 28, 19–45 (2000). 10.1146/annurev.earth.28.1.19

[21]

Meng, Q. et al. Palaeontology: Parental care in an ornithischian dinosaur. Nature 431, 145–146 (2004). 10.1038/431145a

[22]

Lu, J. et al. An egg-adult association, gender and reproduction in pterosaurs. Science 331, 321–324 (2011). 10.1126/science.1197323

[23]

Campbell, H. W. Observation on the acoustic behavior of crocodilians. Zoologica 58, 1–12 (1973).

[24]

Burghardt, G. M. Of Iguanas and Dinosaurs: Social behavior and communication in neonate reptiles. Amer. Zool. 17, 177–190 (1977). 10.1093/icb/17.1.177

[25]

Staton, M. A. “Distress calls” of crocodilians - Whom do they benefit? Amer. Nat. 112, 327–332 (1978). 10.1086/283275

[26]

Young, B. A., Mathevon, N. & Tang, Y. in Insights from Comparative Hearing Research, Springer Handbook of Auditory Research Volume 49 (Springer, 2014).

[27]

Wright, J. & Leonard M. L. The evolution of begging (Kluwer Academic Publishers, 2002). 10.1007/0-306-47660-6

[28]

Vergne, A. L., Pritz, M. B., & Mathevon, N. Acoustic communication in crocodilians: from behaviour to brain. Biol. Rev. 84, 391–411 (2009). 10.1111/j.1469-185x.2009.00079.x

[29]

Crocodile egg sounds signal hatching time

Amélie L. Vergne, Nicolas Mathevon

Current Biology 2008 10.1016/j.cub.2008.04.011

[30]

Vergne, A. L., Aubin, T., Taylor, P. & Mathevon, N. Acoustic signals of baby black caimans. Zoology 114, 313–320 (2011). 10.1016/j.zool.2011.07.003

[31]

Hunt, R. H. & Watanabe, M. E. Observations on maternal behavior of the American alligator, Alligator mississippiensis. J. Herpetol. 3, 235–239 (1982). 10.2307/1563716

[32]

Brien, M. L. et al. The good, the bad and the ugly: Agonistic behaviour in juvenile crocodilians. PloS ONE 8, e80872 (2013a). 10.1371/journal.pone.0080872

[33]

Brien, M. L. et al. Born to be bad: agonistic behaviour in hatchling saltwater crocodiles (Crocodylus porosus). Behaviour 150, 737–762 (2013b). 10.1163/1568539x-00003078

[34]

Adkins-Regan, E. Hormones and animal social behavior (Princeton University Press, 2005).

[35]

Vergne, A. L., Avril, A., Martin, S., & Mathevon, N. Parent-offspring communication in the Nile crocodile Crocodylus niloticus: do newborns’ calls show an individual signature? Naturwissen. 94, 49–54 (2007). 10.1007/s00114-006-0156-4

[36]

Vergne, A. L., Aubin, T., Martin, S. & Mathevon, N. Acoustic communication in crocodilians: information encoding and species specificity of juvenile calls. Anim. Cogn. 15, 1095–1109 (2012). 10.1007/s10071-012-0533-7

[37]

Hauser, M. D. The evolution of communication (MIT press, 1997). 10.7551/mitpress/2867.001.0001

[38]

Taylor, A. M. & Reby, D. The contribution of source-filter theory to mammal vocal communication research: Advances in vocal communication research. J. Zool. 280, 221–236 (2010). 10.1111/j.1469-7998.2009.00661.x

[39]

Riede, T., Li, Z., Tokuda, I. T. & Farmer C. Functional morphology of the Alligator mississipiensis larynx with implications for vocal production. J. Exp. Biol. 218, 991–998 (2015). 10.1242/jeb.117101

[40]

Riede, T., Tokuda, I. T. & Farmer C. Subglottal pressure and fundamental frequency control in contact calls of juvenile Alligator mississipiensis. J. Exp. Biol. 214, 3082–3095 (2011). 10.1242/jeb.051110

[41]

Meredith, R. W., Hekkala, E. R., Amato, G. & Gatesy, J. A phylogenetic hypothesis for Crocodylus (Crocodylia) based on mitochondrial DNA: Evidence for a trans-Atlantic voyage from Africa to the New World. Mol. Phyl. Evol. 60, 183–191 (2011). 10.1016/j.ympev.2011.03.026

[42]

Modha, M. L. The ecology of the Nile crocodile (Crocodylus niloticus) on Central Island, Lake Rudolf. Afric. J. Ecol. 5, 74–95 (1967).

[43]

Pooley, A. C. Parental care in the Nile crocodile. Lammergeyer 21, 43–45 (1974).

[44]

Pooley, A. C. Nest opening response of the Nile crocodile Crocodylus niloticus. J. Zool. 182, 17–26 (1977). 10.1111/j.1469-7998.1977.tb04137.x

[45]

Hutton, J. Movements, home range, dispersal and the separation of size classes in Nile crocodiles. Integr. Comp. Biol. 29, 1033–1049 (1989).

[46]

Royle, N. J., Smiseth, P. T. & Kölliker, M. The Evolution of Parental Care (Oxford University Press, 2012). 10.1093/acprof:oso/9780199692576.003.0001

[47]

Bradbury, J. W. & Vehrencamp, S. L. Principles of Animal Communication (Sinauer Associates Inc., 2011).

[48]

Hardy, I. C. W. & Briffa, M. Animal Contests (Cambridge University Press, 2013). 10.1017/cbo9781139051248

[49]

Padian, K., De Ricqles, A. & Horner, J. R. Dinosaurian growth rates and bird origins. Nature 412, 405–408 (2001). 10.1038/35086500

[50]

Horner, J. R. & Padian, K. Age and growth dynamics of Tyrannosaurus rex. Proc. R. Soc. Lond. B. 271, 1875–1880 (2004). 10.1098/rspb.2004.2829

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Published: Oct 23, 2015
Vol/Issue: 5(1)
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Authors

NAM, Laboratoire des Mecanismes de la Communication, URA 1491 du CNRS, Universite Paris XI, 91400 Orsay, France

Cite This Article

T. Chabert, A. Colin, T. Aubin, et al. (2015). Size does matter: crocodile mothers react more to the voice of smaller offspring. Scientific Reports, 5(1). https://doi.org/10.1038/srep15547

Size does matter: crocodile mothers react more to the voice of smaller offspring

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