Abstract
Dolphins are known for their complex vocal communication, not least because of their capacity for acoustic plasticity. Paradoxically, we know little about their capacity for flexible vocal use. The difficulty in describing the behaviours performed underwater while vocalizing makes it difficult to analyse the contexts of emissions. Dolphins’ main vocal categories are typically considered to be used for scanning the environment (clicks), agonistic encounters (burst pulses) and socio-affiliative interactions (whistles). Dolphins can also combine these categories in mixed vocal emissions, whose use remains unclear. To better understand how vocalizations are used, we simultaneously recorded vocal production and the associated behaviours by conducting underwater observations (N = 479 events) on a group of 7 bottlenose dolphins under human care. Our results showed a non-random association between vocal categories and behavioural contexts. Precisely, clicks were preferentially emitted during affiliative interactions and not during other social/solitary contexts, supporting a possible complementary communicative function. Burst pulses were associated to high arousal contexts (agonistic and social play), pinpointing on their use as an “emotively charged” signal. Whistles were related to solitary swimming and not preferentially produced in any social context. This questions whistles’ functions and supports their potential role as a distant contact call. Finally, mixed vocalizations were especially found associated with sexual (bust pulse-whistle-click), solitary play (burst pulse-whistle) and affiliative (click-whistle) behaviours. Depending on the case, their emission seems to confirm, modify or refine the functions of their simple counterparts. These results open up new avenues of research into the contextual use of dolphin acoustic signals.
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Data availability
Raw data supporting the conclusion of this study will be made available by the authors without undue reservation.
References
Acevedo-Gutiérrez A, Stienessen SC (2004) Bottlenose dolphins (Tursiops truncatus) increase number of whistles when feeding. Aquat Mamm 30:357–362. https://doi.org/10.1578/AM.30.3.2004.357
Adret-Hausberger M (1982) Social influences on the whistled songs of starlings. Behav Ecol Sociobiol 11:241–246. https://doi.org/10.1007/BF00299300
Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 40:227–266
Arlet M, Jubin R, Masataka N, Lemasson A (2015) Grooming-at-a-distance by exchanging calls in nonhuman primates. Bioly Lett 11:2015071120150711. https://doi.org/10.1098/rsbl.2015.0711
Au W (2004) The sonar of dolphins. Acoust Aust 32:61–63. https://doi.org/10.1121/1.408312
Balsby T, Thorsten JS, Bradbury JW (2009) Vocal matching by orange-fronted conures (Aratinga canicularis). Behav Process 82:133–139. https://doi.org/10.1016/j.beproc.2009.05.005
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed effects models using LME4. J Stat Softw 67:1–48. https://doi.org/10.48550/arXiv.1406.5823
Blomqvist C, Amundin M (2004) An acoustic tag for recording directional pulsed ultrasounds aimed at free-swimming bottlenose dolphins (Tursiops truncatus) by conspecifics. Aquat Mamm 30:345–356. https://doi.org/10.1578/AM.30.3.2004.345
Blomqvist C, Mello I, Amundin M (2005) An acoustic play-fight signal in bottlenose dolphins (Tursiops truncatus) in human care. Aquat Mamm 31:187–194. https://doi.org/10.1578/AM.31.2.2005.187
Bohn KM, Wilkinson GS, Moss CF (2007) Discrimination of infant isolation calls by female greater spear-nosed bats, Phyllostomus hastatus. Anim behav 73:423–432. https://doi.org/10.1016/j.anbehav.2006.09.003
Boisseau O (2005) Quantifying the acoustic repertoire of a population: the vocalizations of free-ranging bottlenose dolphins in Fiordland, New Zealand. J Acous Soc Am 117:2318–2329. https://doi.org/10.1121/1.1861692
Briseño-Jaramillo M, Biquand V, Estrada A, Lemasson A (2017) Vocal repertoire of free-ranging black howler monkeys (Alouatta pigra): call types, contexts, and sex-related contributions. Am J Primatol 79:e22630. https://doi.org/10.1002/ajp.22630
Brudzynski SM (2014) Social origin of vocal communication in rodents. In: Witzany G (ed) Biocommun Anim. Springer, Dordrecht, pp 63–79. https://doi.org/10.1007/978-94-007-7414-8_5
Burghardt GM (2005) The genesis of animal play: testing the limits. MIT press
Caldwell MC, Caldwell DK (1965) Individualized whistle contours in bottlenosed dolphins (Tursiops truncatus). Nature 207:434–435. https://doi.org/10.1038/207434a0
Caldwell MC, Caldwell DK (1967) Intraspecific transfer of information via the pulsed sound in captive odontocete cetaceans. In: Busnel (ed) Animal Sonar Systems. Laborative de Physiologie Acoustique, Jouy-en-Josas, pp 879–936. https://doi.org/10.1007/978-1-4612-1150-1_5
Candiotti A, Zuberbühler K, Lemasson A (2012) Context-related call combinations in female Diana monkeys. Anim Cogn 15:327–339. https://doi.org/10.1007/s10071-011-0456-8
Cheney DL, Seyfarth RM, Palombit R (1996) The function and mechanisms underlying baboon ‘contact’ barks. Anim Behav 52:507–518. https://doi.org/10.1006/anbe.1996.0193
Chereskin E, Connor RC, Friedman WR, Jensen FH, Allen SJ, Sørensen PM, Krützen M, King SL (2022) Allied male dolphins use vocal exchanges to “bond at a distance”. Curr Biol 32:1657–1663.e4. https://doi.org/10.1016/j.cub.2022.02.019
Clausen KT, Wahlberg M, Beedholm K, De Ruiter S (2011) Click communication in harbour porpoises Phocoena phocoena. Bioacoustic 20:1–28. https://doi.org/10.1080/09524622.2011.9753630
Clegg ILK, Rödel HG, Cellier M, Vink D, Michaud I, Mercera B, Boye M, Hausberger M, Lemasson A, Delfour F (2017) Schedule of human-controlled periods structures bottlenose dolphin (Tursiops truncatus) behaviour in their free-time. J Comp Psychol 131:214. https://doi.org/10.1037/com0000059
Connor RC, Smolker RA (1996) “Pop” goes the dolphin: a vocalization male bottlenose dolphins produce during consortships. Behaviour 133:643–662
Connor RC, Vollmer N (2009) Sexual coercion in dolphin consortships: a comparison with chimpanzees. In: Muller MN, Wrangham RW (eds) Sexual coercion in primates: An evolutionary perspective on male aggression against females. Harvard University Press, Cambridge, pp 218–243. https://doi.org/10.4159/9780674054349-009
Connor RC, Wells RS, Mann J, Read AJ (2000) The bottlenose dolphin. In: Mann J, Connor CC, Tyack PL, Whitehead H (eds) Cetacean societies: field studies of dolphins and whales. The University of Chicago Press, Chicago, pp 91–125
Cook MLH, Sayigh LS, Blum JE, Wells R (2004) Signature–whistle production in undisturbed free–ranging bottlenose dolphins (Tursiops truncatus). Proc Royal Soc B 271:1043–1049. https://doi.org/10.1098/rspb.2003.2610
Cortopassi KA, Bradbury JW (2006) Contact call diversity in wild orange-fronted parakeet pairs, Aratinga canicularis. Anim Behav 71:1141–1154. https://doi.org/10.1016/j.anbehav.2005.09.011
Coye C, Townsend S, Lemasson A (2017) From animal communication to linguistics and back: insight from compositional abilities in monkeys and birds. In: Boë LJ, Fagot J, Perrier P, Schwartz JL (eds) Origins of human language: continuities and discontinuities with nonhuman primates. Peter Lang Publisher, Berlin, pp 187–232
Cranford TW, Amundin M, Norris KS (1996) Functional morphology and homology in the odontocete nasal complex: implications for sound generation. J Morphol 228:223–285. https://doi.org/10.1002/(SICI)1097-4687(199606)228:3%3c223::AID-JMOR1%3e3.0.CO;2-3
Dawson SM (1991) Clicks and communication: the behavioural and social contexts of Hector’s dolphin vocalizations. Ethology 88:265–276. https://doi.org/10.1111/j.1439-0310.1991.tb00281.x
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. https://doi.org/10.1016/j.mambio.2010.06.006
Díaz López B, Shirai JAB (2009) 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 129–148
Digweed SM, Fedigan LM, Rendall D (2007) Who cares who calls? Selective responses to the lost calls of socially dominant group members in the white-faced capuchin (Cebus Capucinus). Am J Prim 69:829–835. https://doi.org/10.1002/ajp.20398
Dormer KJ (1979) Mechanism of sound production and air recycling in delphinids: Cineradiographic evidence. J Acoust Soc Am 65:229–239. https://doi.org/10.1121/1.382240
dos Santos MF, 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
dos Santos ME, Louro S, Couchinho M, Brito C (2005) Whistles of bottlenose dolphins (Tursiops truncatus) in the Sado Estuary, Portugal: characteristics, production rates and long-term contour stability. Aquat Mamm 31:453–462. https://doi.org/10.1578/AM.31.4.2005.453
Dubrovsky NA (2004) Echolocation system of the bottlenose dolphin. Biol Acoust 50:369–383. https://doi.org/10.1134/1.1739499
Dudzinski KA, Clark CW, Würsig B (1995) A mobile video/acoustic system for simultaneous underwater recording of dolphin interactions. Aquat Mamm 21:187–194
Dudzinski KM (1996) Communication and behaviour in the Atlantic spotted dolphins (Stenella frontalis): Relationships between vocal and behavioural activities. Texas A&M University
Dunbar RIM (1996) Grooming, gossip, and the evolution of language. Harvard University Press, Cambridge
Esch HC, Sayigh LS, Wells RS (2009) Quantifying parameters of bottlenose dolphin signature whistles. Mar Mamm Sci 4:976–986. https://doi.org/10.1111/j.1748-7692.2009.00289.x
Eskelinen HC, Winship KA, Jones BL, Ames AEMM, Kuczaj SA II (2016) Acoustic behaviour associated with cooperative task success in bottlenose dolphins (Tursiops truncatus). Anim Cogn 19:789–797. https://doi.org/10.1007/s10071-016-0978-1
Evans-Wilent J, Dudzinski KM (2013) Vocalizations associated with pectoral fin contact in bottlenose dolphins (Tursiops truncatus). Behav Process 100:74–81. https://doi.org/10.1016/j.beproc.2013.07.025
Faragó T, Pongrácz P, Range F, Virányi Z, Miklósi Á (2010) ‘The bone is mine’: affective and referential aspects of dog growls. Anim Behav 79:917–925. https://doi.org/10.1016/j.anbehav.2010.01.005
Gallo A, Thieffry A, Boye M, Monmasson K, Hausberger M, Lemasson A (2022) Identification of individual bottlenose dolphins (Tursiops truncatus) emitters using a cheap wearable acoustic tag. Front Mar Sci 9:915168. https://doi.org/10.3389/fmars.2022.915168
Gouzoules H, Gouzoules S, Ashley J (1995) Representational signaling in non-human primate vocal communication. In: Zimmermann E, Newman JD, Jürgens U (eds) Current topics in primate vocal communication. Plenum Press, New York, pp 235–252. https://doi.org/10.1007/978-1-4757-9930-9_13
Greene WE, Melillo-Sweeting K, Dudzinski KM (2011) Comparing object play in captive and wild dolphins. I J Comp Psycholol 24:292–306. https://doi.org/10.46867/ijcp.2011.24.03.01
Gregg JD, Dudzinski KM, Smith HV (2007) Do dolphins eavesdrop on the echolocation signals of conspecifics? Int J Comp Psychol 20:65–88. https://doi.org/10.46867/ijcp.2007.20.01.01
Gridley T, Nastasi A, Kriesell HJ, Elwen SH (2015) The acoustic repertoire of wild common bottlenose dolphins (Tursiops truncatus) in Walvis Bay, Namibia. Bioacoustics 24:153–174. https://doi.org/10.1080/09524622.2015.1014851
Gustison ML, Bergman TJ (2016) Vocal complexity influences female responses to gelada male calls. Sci Rep 6:1–9. https://doi.org/10.1038/srep19680
Harley HE (2008) Whistle discrimination and categorization by the Atlantic bottlenose dolphin (Tursiops truncatus): a review of the signature whistle framework and a perceptual test. Behav Process 77:243–268. https://doi.org/10.1016/j.beproc.2007.11.002
Hausberger M (1997) Social influences on song acquisition and song sharing in European starlings. In: Snowdon CT, Hausberger M (eds) Social influences on vocal development. Cambridge University Press, Cambridge, pp 128–156. https://doi.org/10.1017/CBO9780511758843
Hausberger M, Black JM (1990) Do females turn males on and off in barnacle goose social display? Ethology 84:232–238. https://doi.org/10.1111/j.1439-0310.1990.tb00799.x
Hawkins ER, Gartside DF (2010) Whistle emissions of Indo-Pacific bottlenose dolphins (Tursiops aduncus) differ with group composition and surface behaviours. J Acoust Soc Am 127:2652–2663. https://doi.org/10.1121/1.3308465
Heiler J, Elwen SH, Kriesell HJ, Gridley T (2016) Changes in bottlenose dolphin whistle parameters related to vessel presence, surface behaviour and group composition. Anim Behav 117:167–177. https://doi.org/10.1016/j.anbehav.2016.04.014
Herman LM, Tavolga WN (1980) The communication systems of Cetaceans. In: Herman LM (ed) Cetacean Behaviour: Mechanisms and Functions. Wiley, New York, pp 149–209
Hernandez EN, Solangi M, Kuczaj ST (2010) Time and frequency parameters of bottlenose dolphin whistles as predictors of surface behaviour in the Mississippi Sound. J Acoust Soc Am 127:3232–3238. https://doi.org/10.1121/1.3365254
Herzing DL (1996) Vocalizations and associated underwater behaviour of free-ranging Atlantic spotted dolphins, Stenella frontalis and bottlenose dolphins, Tursiops truncatus. Aquat Mamm 22:61–80. https://doi.org/10.12966/abc.02.02.2015
Herzing DL (2000) Acoustics and social behaviour of wild dolphins: implications for a sound society. In: Au WWL, Fay RR, Popper AN (eds) . Springer, New York, pp 225–272
Herzing DL (2013) Clicks, whistles and pulses: passive and active signal use in dolphin communication. Acta Astronaut 105:534–537. https://doi.org/10.1016/j.actaastro.2014.07.003
Herzing DL (2015) Making sense of it all: Multimodal dolphin communication. In: Herzing DL, Johnson CM (eds) Dolphin communication and cognition: Past, present, and future. MIT Press, Cambridge, pp 139–171. https://doi.org/10.7551/mitpress/9939.003.0009
Herzing DL, dos Santos M (2004) Functional aspects of echolocation in dolphins. In: Thomas JA, Moss CF, Vater M (eds) Echolocation in bats and dolphins. University of Chicago Press, Chicago, pp 386–393
Hiley HM, Perry S, Hartley S, King S (2017) What’s occurring? Ultrasonic signature whistle use in Welsh bottlenose dolphins (Tursiops truncatus). Bioacoustics 26:25–35. https://doi.org/10.1080/09524622.2016.1174885
Janik VM (2000) Food–related bray calls in wild bottlenose dolphins (Tursiops truncatus). Proc Royal Soc B 267:923–927. https://doi.org/10.1098/rspb.2000.1091
Janik VM (2009) Acoustic communication in delphinids. Adv Study Behav 40:123–157. https://doi.org/10.1016/S0065-3454(09)40004-4
Janik VM (2014) Cetacean vocal learning and communication. Curr Opin Neurobiol 28:60–65. https://doi.org/10.1016/j.conb.2014.06.010
Janik VM (2015) Play in dolphins. Curr Biol 25:R7–R8. https://doi.org/10.1016/j.cub.2014.09.010
Janik VM, Sayigh LS (2013) Communication in bottlenose dolphins: 50 years of signature whistle research. J Comp Physiol A 199:479–489. https://doi.org/10.1007/s00359-013-0817-7
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 29:399–440. https://doi.org/10.1080/09524622.2019.1613265
Kaplan JD, Reiss D (2017) Whistle acoustic parameters in Atlantic spotted dolphins (Stenella frontalis) and bottlenose dolphins (Tursiops truncatus) in two locations in the Bahamas and comparisons with other populations. Aquat Mamm 43:364. https://doi.org/10.1578/AM.43.4.2017.364
King SL, Connor RC, Montgomery SH (2022) Social and vocal complexity in bottlenose dolphins. Trends Neurosci 45:881–883. https://doi.org/10.1016/j.tins.2022.09.006
Koda H, Shimooka Y, Sugiura H (2008) Effects of caller activity and habitat visibility on contact call rate of wild Japanese macaques (Macaca fuscata). Am J Primatol 70:1055–1063. https://doi.org/10.1002/ajp.20597
Kremers D, Jaramillo MB, Böye M, Lemasson A, Hausberger M (2014) Nocturnal vocal activity in captive bottlenose dolphins (Tursiops truncatus): could dolphins have presleep choruses ? Anim Behav Cogn 1:464–469. https://doi.org/10.12966/abc.11.04.2014
Kuczaj SA, Yeater DB (2006) Dolphin imitation: who, what, when, and why? Aquat Mamm 32:413. https://doi.org/10.1578/AM.32.4.2006.413
Lammers MO, Oswald JN (2015) Analyzing the acoustic communication of dolphins. In: Herzing DL, Johnson CM (eds) Dolphin communication and cognition: Past, present, and future. MIT Press, Cambridge, pp 107–137
Lammers MO, Au WWL, Herzing DL (2003) The broadband social acoustic signaling behaviour of spinner and spotted dolphins. J Acoust Soc Am 114:1629–1639. https://doi.org/10.1121/1.1596173
Lammers MO, Schotten M, Au WWL (2006) The spatial context of free-ranging Hawaiian spinner dolphins (Stenella longirostris) producing acoustic signals. J Acoust Soc Am 119:1244–1250. https://doi.org/10.1121/1.2151804
Lang TG, Smith HAP (1965) Communication between dolphins in separate tanks by way of an electronic acoustic link. Science 150:1839–1844. https://doi.org/10.1126/science.150.3705.1839
Leighty KA, Soltis J, Wesolek CM, Savage A (2008) Rumble vocalizations mediate interpartner distance in African elephants, Loxodonta africana. Anim Behav 76:1601–1608. https://doi.org/10.1016/j.anbehav.2008.06.022
Lilly JC (1962) Vocal behaviour of the bottlenose dolphin. Proc Am Philos Soc 106:520–529
Lilly JC, Miller AC (1961) Sounds Emitted by the Bottlenose Dolphin: The audible emissions of captive dolphins under water or in air are remarkably complex and varied. Science 3465:1689–1693. https://doi.org/10.1126/science.133.3465.1689
Lima A, Lemasson A, Boye M, Hausberger M (2017) Temporal distribution of bottlenose dolphin social and vocal activities in a zoological park. Zoo Biol 36:1–9. https://doi.org/10.1002/zoo.21387
Lopez-Marulanda J, Roynette N, Blanchard T, Adam O, Delfour F (2019) Acoustic localization method applied to the analysis of dolphin calf acoustical exploratoy behaviour within its social group. Int J Comp Psychol 32. https://doi.org/10.46867/ijcp.2019.32.00.13
Lopez-Marulanda J, Rodel HG, Colpaert N, Vanderheul S, Adam O, Delfour F (2022) Contexts of emission of non-signature whistles in bottlenose dolphins (Tursiops truncatus) under human care. Behav Process 181:104255. https://doi.org/10.1016/j.beproc.2020.104255
Luís AR, Couchinho MN, Miguel N, dos Santos ME (2014) Changes in the acoustic behaviour of resident bottlenose dolphins near operating vessels. Mar Mammal Sci 4:1417–1426. https://doi.org/10.1111/mms.12125
Luís AR, Couchinho MN, Dos Santos ME (2016) A quantitative analysis of pulsed signals emitted by wild bottlenose dolphins. PLoS ONE 11:0157781. https://doi.org/10.1371/journal.pone.0157781
Luís AR, Alves IS, Sobreira FV, Couchinho MN, Dos Santos ME (2019) Brays and bits: information theory applied to acoustic communication sequences of bottlenose dolphins. Bioacoustics 28(3):286–296. https://doi.org/10.1080/09524622.2018.1443285
Manser MB (2010) The generation of functionally referential and motivational vocal signals in mammals. In: Brudzynski SM (ed) Handbook of behavioural neuroscience. Elsevier, Amsterdam, pp 477–486. https://doi.org/10.1016/B978-0-12-374593-4.00043-7
Martin MJ, Elwen SH, Kassanjee R, Gridley T (2019) To buzz or burst-pulse? The functional role of Heaviside’s dolphin, Cephalorhynchus heavisidii, rapidly pulsed signals. Anim Behav 150:273–284. https://doi.org/10.1016/j.anbehav.2019.01.007
McCowan B (1995) A new quantitative technique for categorizing whistles using simulated signals and whistles from captive bottlenose dolphins (Delphinidae, Tursiops truncatus). Ethology 100:177–193
McCowan B, Reiss D (1997) Vocal learning in captive bottlenose dolphins: A comparison with humans and nonhuman animals. In: Snowdown CT, Hausberger M (eds) Social influences on vocal development. Cambridge University Press, Cambridge, pp 178–207. https://doi.org/10.1017/CBO9780511758843.010
Mendl M, Burman OHP, Paul E (2010) An integrative and functional framework for the study of animal emotion and mood. Proc Royal Soc B 277:2895–2904. https://doi.org/10.1098/rspb.2010.0303
Miller LA, Pristed J, Brtel M, Surlykke A (1995) The click-sounds of narwhals (Monodon monoceros) in Inglefield Bay, Northwest Greenland. Mar Mamm Sci 4:491–502. https://doi.org/10.1111/j.1748-7692.1995.tb00672.x
Moore SE, Ridgway SH (1996) Patterns of dolphin sound production and ovulation. Aquat Mamm 22:175–184
Nakamura K, Akamatsu T, Shimazaki K (1998) Threat clicks of captive harbor porpoises, Phocoena phocoena. Bull Fish Sci Hokkaido Univ 41:91–105
Nowacek DP, Christiansen F, Bejder L, Goldbogen JA, Friedlaender AS (2016) Studying cetacean behaviour: new technological approaches and conservation applications. Anim Behav 120:235–244. https://doi.org/10.1016/j.anbehav.2016.07.019
Ordóñez-gómez J, Santillan-Doherty AM, Hammerschidt K (2019) Acoustic variation of spider monkey (Ateles geoffroyi) contact calls is related to caller isolation and affects listeners’ responses. PLoS ONE 14:e0213914. https://doi.org/10.1371/journal.pone.0213914
Ouattara K, Lemasson A, Zuberbühler K (2009) Campbell’s monkeys concatenate vocalizations into context-specific call sequences. PNAS 106:22026–22031. https://doi.org/10.1073/pnas.0908118106
Overstrom N (1983) Association between burst-pulse sounds and aggressive behaviour in captive Atlantic bottlenose dolphins (Tursiops truncatus). Zoo Biol 2:93–103. https://doi.org/10.1002/zoo.1430020203
Papale E, Perez-Gil M, Castrillon J, Perez-Gil E, Ruiz L, Servidio A, Tejedor M, Giacoma C, Martín V (2016) Context specificity of Atlantic spotted dolphin acoustic signals in the Canary Islands. Ethol Ecol Evol 29:311–329. https://doi.org/10.1080/03949370.2016.1171256
Perazio CE, Kuczaj SA II (2017) Vocalizations produced by bottlenose dolphins (Tursiops truncatus) during mouth actions in aggressive and non-aggressive contexts. Int J Comp Psychol 30:1–16. https://doi.org/10.46867/ijcp.2017.30.00.07
Pougnault L, Levréro F, Leroux M, PauletJ BP, Dentressangle F, Deruti L, Mulot B, Lemasson A (2022) Social pressure drives « conversational rules » in great apes. Biol Rev 97:749–765. https://doi.org/10.1111/brv.12821
Probert R, Bastian A, Elwen SH, James BS, Gridley T (2021) Vocal correlates of arousal in bottlenose dolphins (Tursiops spp.) in human care. PloS ONE 16:e0250913. https://doi.org/10.1371/journal.pone.0250913
Quick NJ, Janik VM (2008) Whistle rates of wild bottlenose dolphins (Tursiops truncatus): influences of group size and behaviour. J Comp Psychol 122:305. https://doi.org/10.1037/0735-7036.122.3.305
Quick NJ, Janik VM (2012) Bottlenose dolphins exchange signature whistles when meeting at sea. Proc Biol Sci 279:2539–2545. https://doi.org/10.1098/rspb.2011.2537
Rachinas-Lopes P, Luís AR, Borges AF, Neto M, dos Santos ME (2017) Whistle stability and variation in captive bottlenose dolphins (Tursiops truncatus) recorded in isolation and social contexts. Aquat Mamm 43:1–13. https://doi.org/10.1578/AM.43.1.2017.1
Radford AN, Ridley AR (2006) Recruitment calling: a novel form of extended parental care in an altricial species. Curr Biol 16:1700–1704. https://doi.org/10.1016/j.cub.2006.06.053
Ralston JV, Herman LM (1989) Dolphin auditory perception. In: Dooling RJ, Hulse SH (eds) The comparative psychology of audition: perceiving complex sounds. Psychology Press, New York, pp 295–327
Rankin S, Oswald J, Barlow J, Lammers M (2007) Patterned burst-pulse vocalizations of the northern right whale dolphin, Lissodelphis borealis. J Acoust Soc Am 121:1213. https://doi.org/10.1121/1.2404919
Reiss D (1988) Observations on the development of echolocation in young bottlenose dolphins. In: Nachtigall PE, PWB M (eds) Animal Sonar. Plenum Press, New York (NY), pp 121–127
Russell VL, Buerkner P, Herve M, Jung M, Love J, Miguez F, Riebl H, Singmann H (2022) emmeans: estimated marginal means, aka least-squares means. https://CRAN.R-project.org/package=emmeans
Ridgway S, Samuelson D, Van Alstyne K, Price D (2015) On doing two things at once: dolphin brain and nose coordinate sonar clicks, buzzes, and emotional squeals with social sounds during fish capture. J Exp Biol 218:3987–3995. https://doi.org/10.1242/jeb.130559
Ryabov VA (2016) The study of acoustic signals and the supposed spoken language of the dolphins. St Petersbg 2:231–239. https://doi.org/10.1016/j.spjpm.2016.08.004
Samarra FIP (2015) Variations in killer whale food-associated calls produced during different prey behavioural contexts. Behav Process 116:33–42. https://doi.org/10.1016/j.beproc.2015.04.013
Scarpaci C, Bigger CSW, Corkeron PJ, Nugegoda D (2000) Bottlenose dolphins (Tursiops truncatus) increase whistling in the presence of swim-with-dolphin’ tour operations. J Cetacean Res Manag 2:183–185. https://doi.org/10.47536/jcrm.v2i3.504
Schwartz C, Tressler J, Keller H, Vanzant M, Ezell S, Smotherman S (2007) The tiny difference between foraging and communication buzzes uttered by the Mexican free-tailed bat, Tadarida brasiliensis. J Comp Physiol 193:853–863. https://doi.org/10.1007/s00359-007-0237-7
Schwing R, Nelson XJ, Wein A, Parsons S (2017) Positive emotional contagion in a New Zealand parrot. Curr Biol 27:213–214. https://doi.org/10.1016/j.cub.2017.02.020
Sekiguchi Y, Khoshima S (2003) Resting behaviours of captive bottlenose dolphins (Tursiops truncatus). Physiol Behav 79:643–653. https://doi.org/10.1016/S0031-9384(03)00119-7
Shapiro AD (2006) Preliminary evidence for signature vocalizations among free-ranging narwhals (Monodon monoceros). J Acoust Soc Am 120:1695. https://doi.org/10.1121/1.2226586
Silk JB, Seyfarth RM, Cheney DL (2016) Strategic use of affiliative vocalizations by wild female baboons. PLoS ONE 11:e0163978. https://doi.org/10.1371/journal.pone.0163978
Sjare BL, Smith TG (1986) The vocal repertoire of white whales, Delphinapterus leucas, summering in Cunningham Inlet, Northwest Territories. Can J Zool 64:407–415. https://doi.org/10.1139/z86-063
Slocombe KE, Zuberbühler K (2005) Functionally referential communication in a chimpanzee. Curr Biol 15:1779–1784. https://doi.org/10.1016/j.cub.2005.08.068
Smith WJ (1965) Message, meaning, and context in ethology. Am Nat 99:405–409
Smolker RA, Mann J, Sluts BB (1993) Use of signature whistles during separations and reunions by wild bottlenose dolphin mothers and infants. Behav Ecol Sociobiol 33:393–402. https://doi.org/10.1007/BF00170254
Therrien SC, Thomas JA, Therrien RE, Stacey R (2012) Time of day and social change affect underwater sound production by bottlenose dolphins (Tursiops truncatus) at the Brookfield Zoo. Aquat Mamm 38:65–75. https://doi.org/10.1578/AM.38.1.2012.65
Thomas RE, Fristrup KM, Tyack PL (2002) Linking the sounds of dolphins to their locations and behaviour using video and multichannel acoustic recordings. J Acoust Soc Am 112:1692–1701. https://doi.org/10.1121/1.1494805
Thomsen HM, Balsby TJS, Dabelsteen T (2019) The imitation dilemma: can parrots maintain their vocal individuality when imitating conspecifics? Behaviour 156:787–814. https://doi.org/10.1163/1568539X-00003548
Tyack PL (1981) Interactions between singing Hawaiian humpback whales and conspecifics nearby. Behav Ecol Sociobiol 8:105–116. https://doi.org/10.1002/j.2326-1951.1981.tb01986.x
Tyack PL (1986) Population biology, social behaviour and communication in whales and dolphins. Trends Ecol Evol 1:144–150. https://doi.org/10.1016/0169-5347(86)90042-X
Tyack PL (2000) Dolphins whistle a signature tune. Science 289:1310–1311. https://doi.org/10.1126/science.289.5483.1310
Tyack PL, Sayigh LS (1997) Vocal learning in cetaceans. In: Snowdown CT, Hausberger M (eds) Social influences on vocal development. Cambridge University Press, Cambridge, pp 208–233. https://doi.org/10.1017/CBO9780511758843.011
Vignal C, Mathevon N, Mottin S (2008) Mate recognition by female zebra finch: analysis of individuality in male call and first investigations on female decoding process. Behav Process 77:191–198. https://doi.org/10.1016/j.beproc.2007.09.003
Walker RH, King AJ, McNutt JW, Jorndan NR (2017) Sneeze to leave: African wild dogs (Lycaon pictus) use variable quorum thresholds facilitated by sneezes in collective decisions. Proc Royal Soc B 284:20170347. https://doi.org/10.1098/rspb.2017.0347
Watkins WA (1980) Click sounds from animals at sea. Springer, New York, p 1980
Watkins WA (1985) Investigations of sperm whale acoustic behaviours in the southeast Caribbean. Cetology 49:1–15
Watkins WA, Schevill WE (1974) Listening to Hawaiian spinner porpoises, Stenella longirostris, with a three-dimensional hydrophone array. J Mammal 55:319–328. https://doi.org/10.2307/1379001
Weaver A (2003) Conflict and reconciliation in captive bottlenose dolphins, Tursiops truncatus. Mar Mammal Sci 19:836–845. https://doi.org/10.1111/j.1748-7692.2003.tb01134.x
Weaver A, Kuczaj S (2016) Neither toy nor tool: Grass-wearing behavior among free-ranging bottlenose dolphins in Western Florida. Int J Comp Psychol ISCP 29:1–18. https://doi.org/10.46867/ijcp.2016.29.00.22
Weilgart LS, Whitehead H (1988) Distinctive vocalizations from mature male sperm whales (Physeter macrocephalus). Can J Zool 66:1931–1937. https://doi.org/10.1139/z88-28
Weir JN, Schneider JN, Anderson RE (2021) The squeaking vocalization of grey wolves (Canis lupus): individuality in a close-range affiliative mammalian vocalisation. Behaviour 159:501–535
Wisniewska DM, Johnson M, Nachtigall PE, Madsen PT (2014) Buzzing during biosonar-based interception of prey in the delphinids Tursiops truncatus and Pseudorca crassidens. J Exp Biol 217:4279–4282. https://doi.org/10.1242/jeb.113415
Yurk H, Barrett-Lennard L, Ford JKB, Matkin CO (2002) Cultural transmission within maternal lineages: vocal clans in resident killer whales in southern Alaska. Anim Behav 63:1103–1119. https://doi.org/10.1006/anbe.2002.3012
Acknowledgements
We are very grateful to Cité Marine (Planète Sauvage) staff for their time, effort, help and patience during the study. We would like to thank Stéphane Louazon for his technical support and EthoS colleagues.
Funding
The study was funded by Association Nationale de la Recherche et de la Technologie (CIFRE N° 436/2014; CIFRE N° 2020/1453), Planète Sauvage, National Center for Scientific Research (CNRS) and Université de Rennes.
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ADML, AL, MB and MH contributed to the study conception and design. ADML and MB collected the data. ADML, AG, AL, MH performed the statistical analyses. ADML, AG, AL, MH drafted the manuscript. All authors contributed to the final version of the manuscript.
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Alessandro Gallo and Alice De Moura Lima are the co-first authors.
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Gallo, A., De Moura Lima, A., Böye, M. et al. Study of repertoire use reveals unexpected context-dependent vocalizations in bottlenose dolphins (Tursiops truncatus). Sci Nat 110, 56 (2023). https://doi.org/10.1007/s00114-023-01884-3
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DOI: https://doi.org/10.1007/s00114-023-01884-3