Abstract
A fundamental question in animal behaviour is the role of vocal communication in the regulation of social interactions in species that organise themselves into social groups. Context dependence and seasonality in vocalizations are present in the communication of many species, although very little research has addressed this dependence in marine mammals. The study presented here examined variations in the rate at which free-ranging dyads of bottlenose dolphins emit social-signals in an effort to better understand the relationship between vocal communication and social context. The results demonstrate that changes in the social-signal production in bottlenose dolphins are related to the sex of the partner, mating season and social affiliation between the components of the dyad. In a context of foraging behaviour on the same feeding ground, mixed (male–female) dyads were found to emit more pulsed burst sounds during the mating season. Another relevant aspect of the study seems to be the greater production of agonistic social-signals in the dyads formed by individuals with a lower degree of social affiliation. Overall, this study confirms a clear relationship between dyad composition and context-specific social-signals that could reflect the motivational state of individuals linked to seasonal changes in vocal behaviour.
Similar content being viewed by others
Data availability
All analyses were carried out, and can be reproduced, in the open-source programs SOCPROG 2.8 and in v. 1.8.1. of the statistics and graphics tool R. Most of the data generated during this study are included in this published article [and its supplementary information files]. Additional data and R scripts will be made available by the authors upon request.
References
Aelianus C (2019) La personalité des animaux, trans. A. Zucker. Les Belles Letres, Paris
Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 49:227–267
Aristotle (1910) Historia animalium trans. D’A. W. Thompson. Clarendon Press, Oxford
Berger J, Cunningham C (1991) Bellows, copulations, and sexual selection in bison (Bison bison). Behav Ecol 2(1):1–6
Biben M, Symmes D, Masataka N (1986) Temporal and structural analysis of affiliative vocal exchanges in squirrel monkeys (Saimiri sciureus). Behaviour 98:259–273
Blomquist C, Amundin M (2004) High-frequency burst-pulse sounds in agonistic/aggressive interactions in bottlenose dolphins, Tursiops truncatus. In: Thomas JA, Moss CF, Vater M (eds) Echolocation in bats and dolphins. University of Chicago Press, Chicago, pp 425–455
Boughman JW, Moss CF (2003) Social sounds: vocal learning and development of mammal and bird calls. In: Simmons AM, Fay RR, Popper AN (eds) Acoustic communication. Springer, New York, pp 138–224
Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer Associates, Sunderland
Caldwell MC, Caldwell DK, Tyack PL (1990) Review of the signature-whistle hypothesis for the Atlantic bottlenose dolphin. In: Leatherwood S, Reeves RR (eds) The bottlenose dolphin. Academic Press, San Diego, pp 199–234
Cheney DL, Seyfarth RM (2018) Flexible usage and social function in primate vocalizations. Proc Natl Acad Sci 115(9):1974–1979
Clay Z, Smith CL, Blumstein DT (2012) Food-associated vocalizations in mammals and birds: what do these calls really mean? Anim Behav 83(2):323–330
Connor RC, Smolker RA (1996) ‘Pop’ goes the dolphin: a vocalization male bottlenose dolphin produce during courtships. Behaviour 133:643–662
Connor RC, Wells RS, Mann J, Read AJ (2000) The bottlenose dolphin: social relationships in a fission-fusion society. In: Mann J, Connor R, Tyack PL, Whitehead H (eds) Cetacean societies: field studies of dolphins and whales. University of Chicago Press, Chicago, pp 91–126
Dahlin CR, Balda RP, Slobodchikoff C (2005) Food, audience and sex effects on pinyon jay (Gymnorhinus cyanocephalus) communication. Behav Proc 68(1):25–39
Dall SR, Giraldeau LA, Olsson O, McNamara JM, Stephens DW (2005) Information and its use by animals in evolutionary ecology. Trends Ecol Evol 20(4):187–193
Darwin C (1872) The expression of the emotions in man and animals. University of Chicago press, Chicago
Díaz López B (2006a) Bottlenose dolphin (Tursiops truncatus) predation on a marine fin fish farm: some underwater observations. Aquat Mamm 32(3):305–310
Díaz López B (2006b) Interactions between Mediterranean bottlenose dolphins (Tursiops truncatus) and gillnets off Sardinia, Italy. ICES J Mar Sci 63:946–951
Díaz López B (2009) The bottlenose dolphin Tursiops truncatus foraging around a fish farm: effects of prey abundance on dolphins’ behaviour. Curr Zool 55(4):243–248
Díaz López B (2011) Whistle characteristics in free-ranging bottlenose dolphins (Tursiops truncatus) in the Mediterranean Sea: influence of behaviour. Mamm Biol 76:180–189
Díaz López B (2012) Bottlenose dolphins and aquaculture: Interaction and site fidelity on the north-eastern coast of Sardinia (Italy). Mar Biol 159(10):2161–2172
Díaz López B (2019) ‘Hot deals at sea’: responses of a top predator (bottlenose dolphin, Tursiops truncatus) to human-induced changes in the coastal ecosystem. Behav Ecol 30(2):291–300
Díaz López B (2020) When personality matters: personality and social structure in wild bottlenose dolphins, Tursiops truncatus. Anim Behav 163:73–84
Díaz López B, Shirai JAB (2007) Bottlenose dolphin (Tursiops truncatus) presence and incidental capture in a marine fish farm on the north-eastern coast of Sardinia (Italy). J Mar Biol Assoc UK 87(1):113–117
Díaz López B, Shirai JAB (2008) Marine aquaculture and bottlenose dolphins’ (Tursiops truncatus) social structure. Behav Ecol Sociobiol 62:887–894
Díaz López B, Shirai JAB (2010) Mediterranean common bottlenose dolphin’s repertoire and communication use. In: Pearce AG, Correa LM (eds) Dolphins: anatomy, behaviour and threats. NOVA Science Publishers, New York, pp 129–147
dos Santos ME, Caporin G, Moreira HO, Ferreira AJ, Coelho JLB (1990) Acoustic behaviour in a local population of bottlenose dolphins. In: Thomas J, Kastelstein R (eds) Sensory abilities of cetaceans. Plenum Press, New York, pp 585–598
dos Santos ME, Ferreira AJ, Harzen S (1995) Rhythmic sound sequences emitted by aroused bottlenose dolphins in the Sado estuary, Portugal. In: Kastelein RA, Thomas JA, Nachtigall PE (eds) Sensory systems of aquatic mammals. De Spil Publishers, Woerden, pp 325–334
Evans CS, Marler P (1994) Food calling and audience effects in male chickens, Gallus gallus: their relationships to food availability, courtship and social facilitation. Anim Behav 47:1159–1170
Fedurek P, Machanda ZP, Schel AM, Slocombe KE (2013) Pant hoot chorusing and social bonds in male chimpanzees. Anim Behav 86:189–196
Fichtel C, Manser M (2010) Vocal communication in social groups. In: Kappeler P (ed) Animal behaviour: evolution and mechanisms. Springer, Berlin, pp 29–54
Fischer J, Price T (2017) Meaning, intention, and inference in primate vocal communication. Neurosci Biobehav Rev 82:22–31
Freeberg TM, Dunbar RIM, Ord TJ (2012) Social complexity as a proximate and ultimate factor in communicative complexity. Philos Trans R Soc B Biol Sci 367(1597):1785–1801
Fruchterman T, Reingold E (1991) Graph drawing by force directed placement. Softw Pract Exp 21(11):1129–1164
Geissmann T, Orgeldinger M (2000) The relationship between duet songs and pair bonds in siamangs, Hylobates syndactylus. Anim Behav 60:805–809
Gros-Louis J (2004) The function of food-associated calls in white-faced capuchin monkeys, Cebus capucinus, from the perspective of the signaller. Anim Behav 67(3):431–440
Harcourt AH, Stewart KJ (1996) Function and meaning of wild gorilla ‘close’ calls correlations with rank and relatedness. Behaviour 133:827–845
Herman LM (2006) Intelligence and rational behaviour in the bottlenosed dolphin. In: Hurley S, Nudds M (eds) Rational animals. Oxford University Press, Oxford, pp 439–467
Herzing DL (1996) Vocalizations and associated underwater behaviours of free-ranging Atlantic spotted dolphins, Stenella frontalis and bottlenose dolphins, Tursiops truncatus. Aquat Mamm 22:61–79
Herzing DL (2000) Acoustics and social behaviour of wild dolphins: implications for a sound society. In: Au WL, Fay RR, Popper AN (eds) Hearing by whales and dolphins. Springer, New York, pp 225–272
Janik VM (2000) Food-related bray calls in wild bottlenose dolphins (Tursiops truncatus). Proc R Soc B Biol Sci 267(1446):923–927
Janik VM (2009) Acoustic communication in delphinids. Adv Study Behav 40:123–157
Janik VM (2013) Cognitive skills in bottlenose dolphin communication. Trends Cogn Sci 17(4):157–159
Janik VM, Slater PJB (1998) Context-specific use suggests that bottlenose dolphin signature whistles are cohesion calls. Anim Behav 56:829–838
Jones GJ, Sayigh LS (2002) Geographic variation in rates of vocal production of free-ranging bottlenose dolphins. Mar Mamm Sci 18(2):374–393
Jones B, Zapetis M, Samuelson MM, Ridgway S (2020) Sounds produced by bottlenose dolphins (Tursiops): A review of the defining characteristics and acoustic criteria of the dolphin vocal repertoire. Bioacoustics 29(4):399–440
King SL, Janik VM (2015) Come dine with me: food-associated social signalling in wild bottlenose dolphins (Tursiops truncatus). Anim Cogn 18:969–974
King SL, Allen SJ, Krützen M, Connor RC (2019) Vocal behaviour of allied male dolphins during cooperative mate guarding. Anim Cogn 22(6):991–1000
Kishida T, Thewissen JGM, Hayakawa T, Imai H, Agata K (2015) Aquatic adaptation and the evolution of smell and taste in whales. Zoological Letters 1(1):1–10
Lammers MO, Au WW, Herzing DL (2003) The broadband social acoustic signaling behavior of spinner and spotted dolphins. J Acoust Soc Am 114(3):1629–1639
Lusseau D, Newman ME (2004) Identifying the role that animals play in their social networks. Proc R Soc B Biol Sci 271(6):S477–S481
Mann J, Richards AF, Smolker RA, Connor RC (1996) Patterns of female attractiveness in Indian Ocean bottlenose dolphins. Behaviour 133(1–2):37–69
Mann J, Stanton MA, Patterson EM, Bienenstock EJ, Singh LO (2012) Social networks reveal cultural behaviour in tool-using dolphins. Nat Commun 3:980
Manser MB (2010) The generation of functionally referential and motivational vocal signals in mammals. In: Brudzynsky SM (ed) Handbook of mammalian vocalization. Elsevier, New York, pp 479–488
Marler P, Dufty A, Pickert R (1986) Vocal communication in the domestic chicken: I. Does a sender communicate information about the quality of a food referent to a receiver? Anim Behav 34:188–193
McComb K, Semple S (2005) Coevolution of vocal communication and sociality in primates. Biol Lett 1(4):381–385
McGregor P (2005) Animal communication networks. Cambridge University Press, Cambridge
Methion S, Díaz López B (2020) Individual foraging variation drives social organization in bottlenose dolphins. Behav Ecol 31(1):97–106
Möller LM, Beheregaray LB, Allen SJ, Harcourt RG (2006) Association patterns and kinship in female Indo-Pacific bottlenose dolphins (Tursiops aduncus) of southeastern Australia. Behav Ecol Sociobiol 61(1):109–117
Oda R (1996) Effects of contextual and social variables on contact call production in free-ranging ringtailed lemurs (Lemur catta). Int J Primatol 17:191–205
Overstrom NA (1983) Association between burst-pulsed and aggressive behaviour in captive Atlantic bottlenosed dolphins (Tursiops truncatus). Zoo Biol 2:93–103
Pizzari T (2003) Food, vigilance, and sperm: the role of male direct benefits in the evolution of female preference in a polygamous bird. Behav Ecol 14:593–601
Reiss D, McCowan B, Marino L (1997) Communicative and other cognitive characteristics of bottlenose dolphins. Trends Cogn Sci 1(4):140–145
Rendall D (2003) Acoustic correlates of caller identity and affect intensity in the vowel-like grunt vocalizations of baboons. J Acoust Soc Am 113:3390–3402
Schehka S, Esser KH, Zimmermann E (2007) Acoustical expression of arousal in conflict situations in tree shrews (Tupaia belangeri). J Comp Physiol A 193:845–852
Schroeder JP, Keller KV (1989) Seasonality of serum testosterone levels and sperm density in Tursiops truncatus. J Exp Zool 249(3):316–321
Semple S, McComb K (2000) Perception of female reproductive state from vocal cues in a mammal species. Proc R Soc Lond Ser B Biol Sci 267(1444):707–712
Sewall KB (2015) Social complexity as a driver of communication and cognition. Integr Comp Biol 55(3):384–395
Seyfarth RM, Cheney DL (2010) Production, usage, and comprehension in animal vocalizations. Brain Lang 115(1):92–100
Sherman PW (1977) Nepotism and the evolution of alarm calls. Science 197(4310):1246–1253
Shimizu M (2001) Vocalizations of feral cats: sexual differences in the breeding season. Mammal Study 26(2):85–92
Smith JN, Goldizen AW, Dunlop RA, Noad MJ (2008) Songs of male humpback whales, Megaptera novaeangliae, are involved in intersexual interactions. Anim Behav 76(2):467–477
Vollmer NL, Hayek LC, Heithaus MR, Connor RC (2015) Further evidence of a context-specific agonistic signal in bottlenose dolphins: the influence of consortships and group size on the pop vocalization. Behaviour 152:1979–2000
Whitehead H (2009) SOCPROG programs: analysing animal social structures. Behav Ecol Sociobiol 63(5):765–778
Whitehead H, James R (2015) Generalized affiliation indices extract affiliations from social network data. Methods Ecol Evol 6(7):836–844
Witzany G (ed) (2014) Biocommunication of Animals. Springer, Dordrecht
Zuberbühler K (2008) Audience effects. Curr Biol 18:R189–R190
Acknowledgements
I thank the members of the Bottlenose Dolphin Research Institute (BDRI) team between 2004 and 2013 who generously gave their time to help with field, bioacoustics and photo-identification work. Many thanks are also extended to the BDRI students and volunteers who assisted with fieldwork. Thanks also to Séverine Methion, Ken Cheng and two anonymous reviewers for their insightful comments. Thanks to Olga Mosca for proofreading the English text. Last but not least, a very special thanks to Ariel for her constant support during the last 10 years, thank you very much for everything.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author of this study declares that he has no conflict of interest. This study was funded by the educational and volunteering programmes of the non-governmental organisation BDRI.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Díaz López, B. Context-dependent and seasonal fluctuation in bottlenose dolphin (Tursiops truncatus) vocalizations. Anim Cogn 25, 1381–1392 (2022). https://doi.org/10.1007/s10071-022-01620-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-022-01620-w