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Influence of environmental, social and behavioural variables on the whistling of the common bottlenose dolphin (Tursiops truncatus)

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Abstract

Bottlenose dolphin communication has been studied extensively. Nevertheless, the combined effect of several variables on whistle structure has yet to be clearly understood. Here, we investigated the influence of underwater noise, boat presence, behaviour, group size and calf presence on the whistles of a small population of common bottlenose dolphins (Tursiops truncatus). Surface behaviour and acoustic data were collected in Sardinia (Italy-Western Mediterranean Sea) between 2015 and 2017. Whistle frequency parameters (minimum, maximum, start, end frequencies and frequency range), duration, number of inflection points and number of harmonics were correlated with the ambient noise levels recorded prior to the whistle display and to behavioural and social factors by means of GAM models. Whistle frequencies varied as a function of the interaction between noise and boat presence, mainly when the noise increased at lower frequencies. Dolphin whistles also varied according to group size, which was further affected by the presence of calves, and behaviours characterised by high levels of arousal such as feeding. The study provides sufficient evidence to support that multiple factors need to be considered when investigating whistle structure as the species is capable of adopting different strategies depending on environmental, social and behavioural context. Finally, this data indicates that communication within a small population of bottlenose dolphins is vulnerable to acoustic pollution, thereby highlighting the need for further investigation into the effects of different noises on whistle structure, as well as the consistency of patterns across different populations.

Significance statement

Exploring a dolphin’s ability to adapt its communication to environmental context is crucial to understanding the consequences of ocean noise increase, especially in highly anthroposised areas such as the Mediterranean Sea. This is one of the few studies that investigate how noise and boat traffic affect bottlenose dolphin whistles whilst considering the concomitant effect of other variables such as behaviour, group size and composition. We demonstrated that dolphins vary their whistles as a function of increasing noise and boat presence, group size and calf presence, and during specific behaviour which requires intense contact between individuals. Finally, the results showed that other variables should be considered to fully understand those which influence whistle structure and adaptability.

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References

  • Acevedo-Gutièrrez A, Stienessen SC (2004) Bottlenose dolphins (Tursiops truncatus) increase number of whistles when feeding. Aquat Mamm 30:357–362

    Google Scholar 

  • Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 49:227–267

    CAS  PubMed  Google Scholar 

  • Au WWL, Hastings MC (2008) Principle of marine bioacoustics. Springer, New York

    Google Scholar 

  • Blumstein DT (2006) The multi-predator hypothesis and the evolutionary persistence of antipredator behavior. Ethology 112:209–217

    Google Scholar 

  • Boisseau O (2005) Quantifying the acoustic repertoire of a population: the vocalisations of free-ranging bottlenose dolphins in Fiordland, New Zealand. J Acoust Soc Am 117:2318–2329

    PubMed  Google Scholar 

  • Bradbury JV, Vehrencamp SL (1998) Principles of animal communication. Sinauer, Sunderland

    Google Scholar 

  • Branstetter BK, Black A, Bakhtiari K (2013) Discrimination of mixed-directional whistles by a bottlenose dolphin (Tursiops truncatus). J Acoust Soc Am 134:2274–2285

    PubMed  Google Scholar 

  • Briefer EF (2012) Vocal expression of emotions in mammals: mechanisms of production and evidence. J Zool 288:1–20

    Google Scholar 

  • Brumm H, Zollinger SA (2011) The evolution of the Lombard effect: 100 years of psychoacoustic research. Behaviour 148:1173–1198

    Google Scholar 

  • Buckstaff KC (2004) Effects of watercraft noise on the acoustic behavior of bottlenose dolphins, Tursiops truncatus, in Sarasota Bay, Florida. Mar Mammal Sci 20:709–725

    Google Scholar 

  • Caldwell MC, Caldwell DK (1968) Vocalization of naive captive dolphins in small groups. Science 159:1121–1123

    CAS  PubMed  Google Scholar 

  • Caldwell MC, Caldwell DK (1979) The whistle of the Atlantic bottlenosed dolphin (Tursiops truncatus) ontogeny. In: Winn HE, Olla BL (eds) Behavior of marine animals: Current perspectives in research, vol 3. Cetaceans Plenum Press, New York, pp 369–401

    Google Scholar 

  • 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

    Google Scholar 

  • Cook MLH, Sayigh LS, Blum JE, Wells RS (2004) Signature-whistle production in undisturbed free-ranging bottlenose dolphins (Tursiops truncatus). Proc R Soc Lond 271:1043–1049

    Google Scholar 

  • Díaz Lopez B (2011) Whistle characteristics in free-ranging bottlenose dolphins (Tursiops truncatus) in the Mediterranean Sea: influence of behaviour. Mamm Biol 76:180–189

    Google Scholar 

  • Díaz López B, Shirai JAB (2009) Mediterranean common bottlenose dolphin’s repertoire and communication use. In: Pearce G, Correa LM (eds) Dolphins: Anatomy, Behavior, and Threats. Nova Science Publishers Inc, New York, pp 129–148

    Google Scholar 

  • Díaz Lopez B, Addis A, Fabiono F (2013) Ecology of common bottlenose dolphin along the North-Western Sardinian coastal waters (Italy). Thalassas 29:35–44

    Google Scholar 

  • Ellison WT, Southall BL, Clark CW, Frankel AS (2012) A new context-based approach to assess marine mammal behavioral responses to anthropogenic sounds. Conserv Biol 26:21–28

    CAS  PubMed  Google Scholar 

  • Erbe C, Liong S, Koessler MV, Duncan AJ, Gourlay T (2016) Underwater sound of rigid-hulled inflatable boats. J Acoust Soc Am 139:EL223–EL227. https://doi.org/10.1121/1.4954411

    Article  PubMed  Google Scholar 

  • Esch HC, Sayigh LS, Blum JE, Wells RS (2009) Whistles as potential indicators of stress in bottlenose dolphins (Tursiops truncatus). J Mammal 90:638–650

    Google Scholar 

  • Fichtel C, Manser M (2010) Vocal communication in social groups. In: Kappeler P (ed) Animal Behaviour: Evolution and Mechanisms. Springer, Berlin, pp 29–54

    Google Scholar 

  • Fitch WT, Hauser M (2002) Unpacking “honesty”: vertebrate vocal production and the evolution of acoustic signals. In: Simmons AM, Fay RR, Popper AN (eds) Acoustic communication. Springer, New York, pp 65–37

    Google Scholar 

  • Fox J, Weisberg S (2011) An {R} Companion to Applied Regression, 2nd edn. Sage, Thousand Oaks http://socserv.socsci.mcmaster.ca/jfox/Books/Companion

    Google Scholar 

  • Frid A, Dill L (2002) Human-caused disturbance stimuli as a form of predation risk. Conserv Ecol 6:11

    Google Scholar 

  • Gillam EH, Ulanovsky N, McCracken GF (2007) Rapid jamming avoidance in biosonar. Proc R Soc Lond B 274:651–660

    Google Scholar 

  • Gridley T, Cockcroft VG, Hawkins ER, Lemon Blewitt M, Morisaka T, Janik VM (2014) Signature whistles in free-ranging populations of Indo-Pacific bottlenose dolphins, Tursiops aduncus. Mar Mammal Sci 30:512–527

    Google Scholar 

  • Guerra M, Dawson SM, Brough TE, Rayment WJ (2014) Effects of boats on the surface and acoustic behaviour of an endangered population of bottlenose dolphins. Endanger Species Res 24:221–236

    Google Scholar 

  • Hase K, Miyamoto T, Kobayasi KI, Hiryu S (2016) Rapid frequency control of sonar sounds by the FM bat, Miniopterus fuliginosus, in response to spectral overlap. Behav Process 128:126–133

    Google Scholar 

  • Hastie TJ, Tibshirani RJ (1990) Generalized Additive Models. Chapman & Hall, London

    Google Scholar 

  • Hawkins ER, Gartside DF (2010) Whistle emissions of Indo-Pacific bottlenose dolphins (Tursiops aduncus) differ with group composition and surface behaviors. J Acoust Soc Am 127:2652–2663

    PubMed  Google Scholar 

  • Hefner RS, Hefner HE (1992) Hearing in large mammals: sound-localization acuity in cattle (Bos taurus) and goats (Capra hircus). J Comp Psychol 106:107–113

    Google Scholar 

  • 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

    Google Scholar 

  • Hernandez EN, Solangi M, Kuczaj SA (2010) Time and frequency parameters of bottlenose dolphin whistles as predictors of surface behavior in the Mississippi Sound. J Acoust Soc Am 127:3232–3238

    PubMed  Google Scholar 

  • Herzing DL (1996) Vocalizations and associated underwater behaviour of free-ranging Atlantic spotted dolphins, Stenella frontalis and bottlenose dolphins, Tursiops truncatus. Aquat Mamm 22:61–79

    Google Scholar 

  • Hiley HM, Perry S, Hartley S, King SL (2017) What’s occurring? Ultrasonic signature whistle use in Welsh bottlenose dolphins (Tursiops truncatus). Bioacoustics 26:25–35

    Google Scholar 

  • Holt MM, Noren DP, Veirs V, Emmons CK, Veirs S (2009) Speaking up: killer whales (Orcinus orca) increase their call amplitude in response to vessel noise. J Acoust Soc Am 125:EL27–EL32. https://doi.org/10.1121/1.3040028

    Article  PubMed  Google Scholar 

  • Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211

    Google Scholar 

  • Janik VM (2000) Whistle matching in wild bottlenose dolphins (Tursiops truncatus). Science 289:1355–1357

    CAS  PubMed  Google Scholar 

  • Janik VM, Sayigh LS (2013) Communication in bottlenose dolphins: 50 years of signature whistle research. J Comp Physiol A 199:479–489

    Google Scholar 

  • Janik VM, Slater PJB (1998) Context-specific use suggests that bottlenose dolphin signature whistles are cohesion calls. Anim Behav 56:829–838

    CAS  PubMed  Google Scholar 

  • Janik VM, Dehnhardt D, Todt D (1994) Signature whistle variations in a bottlenosed dolphin, Tursiops-truncatus. Behav Ecol Sociobiol 35:243–248

    Google Scholar 

  • Janik VM, Sayigh LS, Wells RS (2006) Signature whistle shape conveys identity information to bottlenose dolphins. Proc Natl Acad Sci USA 103:8293–8297

    CAS  PubMed  Google Scholar 

  • Janik VM, King SL, Sayigh LS, Wells RS (2013) Identifying signature whistles from recordings of groups of unrestrained bottlenose dolphins (Tursiops truncatus). Mar Mamm Sci 29:109–122

    Google Scholar 

  • Jensen FH (2011) Acoustic behavior of bottlenose dolphins and pilot whales. PhD Dissertation, Zoophysiology Department of Biological Science, University of Aarhus, Denmark

  • King SL, Janik VM (2015) Come dine with me: Food-associated social signalling in wild bottlenose dolphins (Tursiops truncatus). Anim Cogn 18:969–974

    PubMed  Google Scholar 

  • King SL, Sayigh LS, Wells RS, Fellner W, Janik VM (2013) Vocal copying of individually distinctive signature whistles in bottlenose dolphins. Proc R Soc B 280:20130053

    PubMed  Google Scholar 

  • Kriesell H, Elwen SH, Nastasi A, Gridley T (2014) Identification and characteristics of signature whistles in wild bottlenose dolphins (Tursiops truncatus) from Namibia. PLoS ONE 9:e106317

    PubMed  PubMed Central  Google Scholar 

  • La Manna G, Manghi M, Pavan G, Lo Mascolo F, Sara G (2013) Behavioural strategy of common bottlenose dolphins (Tursiops truncatus) in response to different kinds of boats in the waters of Lampedusa Island (Italy). Aquat Conserv 23:745–757

    Google Scholar 

  • La Manna G, Manghi M, Perretti F, Sarà G (2016) Behavioural response of brown meagre (Sciaena umbra) to boat noise. Mar Pollut Bull 110:324–334

    PubMed  Google Scholar 

  • Lammers MO, Au WWL (2003) Directionality in the whistles of Hawaiian spinner dolphins (Stenella longirostris): A signal feature to cue direction of movement? Mar Mamm Sci 19:249–264

    Google Scholar 

  • Lammers MO, Oswald JN (2015) Analyzing the acoustic communication of dolphins. In: Herzing D, Johnson CM (eds) Dolphin Communication and Cognition: Past. Present and Future. The MIT Press, Cambridge, pp 107–137

    Google Scholar 

  • Luís AR, Couchinho MN, dos Santos ME (2014) Changes in the acoustic behavior of resident bottlenose dolphins near operating vessels. Mar Mamm Sci 30:1417–1426

    Google Scholar 

  • Lusseau D (2003) Male and female bottlenose dolphins (Tursiops spp.) have different strategies to avoid interactions with tour boats in Doubtful Sound, New Zealand. Mar Ecol Prog Ser 257:267–274

    Google Scholar 

  • Mann J (1999) Behavioural sampling methods for cetaceans: a review and critique. Mar Mamm Sci 15:102–122

    Google Scholar 

  • Mann J (2000) Unraveling the dynamics of social life: Long term studies and observational methods. In: Mann J, Connor R, Tyack PL, Whitehead H (eds) Cetacean Societies: Field Studies of Dolphins and Whales. University of Chicago Press, Chicago, pp 45–64

    Google Scholar 

  • Marley SA, Salgado Kent CP, Erbe C, Parnum IM (2017) Effects of vessel traffic and underwater noise on the movement, behaviour and vocalisations of bottlenose dolphins in an urbanised estuary. Sci Rep 7:13437

    PubMed  PubMed Central  Google Scholar 

  • May Collado LJ, Quinones-Lebron SG (2014) Dolphin changes in whistle structure with watercraft activity depends on their behavioral state. J Acoust Soc Am 135:193–198

    Google Scholar 

  • May Collado LJ, Wartzok D (2008) A comparison of bottlenose dolphin whistles in the Atlantic ocean: factors promoting whistle variation. J Mammal 89:1229–1240

    Google Scholar 

  • Mello I, Amundin M (2005) Whistle production pre-and post-partum in bottlenose dolphins (Tursiops truncatus) in human care. Aquat Mamm 31:169–175

    Google Scholar 

  • Merchant ND, Fristrup KM, Johnson MP, Tyack PL, Witt ML, Blondel P, Parks SE (2015) Measuring acoustic habitats. Methods Ecol Evol 2015:257–265

    Google Scholar 

  • Miller PJO (2002) Mixed-directionality of killer whale stereotyped calls: A direction of movement cue? Behav Ecol Sociobiol 52:262–270

    Google Scholar 

  • Monticelli PF, Tokumaru RS, Ades C (2004) Isolation induced changes in guinea pig (Cavia porcellus) pup distress whistles. An Acad Bras Cienc 76:368–372

    PubMed  Google Scholar 

  • Owings D, Morton E (1998) Animal vocal communication: a new approach. Cambridge University Press, Cambridge

    Google Scholar 

  • Parks SE, Johnson M, Nowacek D, Tyack P (2011) Individual right whales call louder in increased environmental noise. Biol Lett 7:33–35

    PubMed  Google Scholar 

  • Picciulin M, Sebastianutto L, Fortuna CM, Mackelworth P, Holcer D, Rako Gospić N (2015) Are the 1/3-octave 63- and 125-Hz band noise levels predictive of vessel activity? The case in the Cres–Lošinj Archipelago (Northern Adriatic Sea, Croatia). In: Popper AN, Hawkins (eds) The Effects of Noise on Aquatic Life II. Springer Science + Business Media, New York, pp 821–828

    Google Scholar 

  • Quick NJ, Janik VM (2008) Whistle rates of wild bottlenose dolphins (Tursiops truncatus): influences of group size and behavior. J Comp Psychol 122:305–311

    PubMed  Google Scholar 

  • R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.r-project.org/

    Google Scholar 

  • Radford A, Purser J, Bruintjes R, Voellmy IK, Everley KA, Wale MA, Holles S, Simpson SD (2015) Beyond a simple effect: variable and changing responses to anthropogenic noise. In: Popper AN, Hawkins A (eds) The Effects of Noise on Aquatic Life II. Springer, New York, pp 901–907

    Google Scholar 

  • Rako Gospić N, Picciulin M (2016) Changes in whistle structure of resident bottlenose dolphins in relation to underwater noise and boat traffic. Mar Pollut Bull 105:193–198

    Google Scholar 

  • Rako Gospić N, Fortuna CM, Holcer D, Mackelworth PC, Nimak-Wood M, Plesli G, Sebastianutto L, Vilibi I, Wiemann A, Picciulin M (2013) Leisure boating noise as a trigger for the displacement of the bottlenose dolphins of the Cres–Lošinj archipelago (northern Adriatic Sea, Croatia). Mar Pollut Bull 68:77–84

    Google Scholar 

  • Rasmussen MH, Lammers M, Beedholm K, Miller A (2006) Source levels and harmonic content of whistles in white-beaked dolphins (Lagenorhynchus albirostris). J Acoust Soc Am 120:510–517

    CAS  PubMed  Google Scholar 

  • Romeu B, Cantor M, Bezamat C, Simões-Lopes PC, Daura-Jorge FG (2017) Bottlenose dolphins that forage with artisanal fishermen whistle differently. Ethology 2017:1–10

    Google Scholar 

  • Sayigh LS, Esch HC, Wells RS, Janik VM (2007) Facts about signature whistles of bottlenose dolphins (Tursiops truncatus). Anim Behav 74:1631–1642

    Google Scholar 

  • Schultz KW, Cato DH, Corkeron PJ, Bryden MM (1995) Low frequency narrow-band sounds produced by bottlenose dolphins. Mar Mammal Sci 11:503–509

    Google Scholar 

  • Shane SH (1990) Behavior and ecology of the bottlenose dolphin at Sanibel Island, Florida. In: Leatherwood SR, Reeves RR (eds) The Bottlenose Dolphin. Academic Press Inc, San Diego, pp 245–265

    Google Scholar 

  • Skyrms B (2009) Evolution of signalling systems with multiple senders and receivers. Philos Trans R Soc B 364:771–779

    Google Scholar 

  • Smolker R, Mann J, Smuts B (1993) The use of signature whistles during separations and reunions among wild bottlenose dolphin mothers and calves. Behav Ecol Sociobiol 33:393–402

    Google Scholar 

  • Turl CW (1993) Low-frequency sound detection by a bottlenose dolphin. J Acoust Soc Am 94:3006

    CAS  PubMed  Google Scholar 

  • Tyack P (1986) Whistle repertoires of two bottlenosed dolphins, Tursiops truncatus: mimicry of signature whistles? Behav Ecol Sociobiol 18:251–257

    Google Scholar 

  • Tyack PL (1997) Development and social functions of signature whistles in bottlenose dolphins Tursiops truncatus. Bioacoustics 8:21–46

    Google Scholar 

  • Tyack PL, Sayigh LS (1997) Vocal learning in cetaceans. In: Snowdon C, Hausberger M (eds) Social influences on vocal development. Cambridge University Press, Cambridge, pp 208–233

    Google Scholar 

  • van Ginkel C, Becker DM, Gowans S, Simard P (2017) Whistling in a noisy ocean: bottlenose dolphins adjust whistle frequencies in response to real-time ambient noise levels. Bioacoustics 27:391–405

    Google Scholar 

  • Venables WN, Ripley BD (2002) Modern Applied Statistics with S, 4th edn. Springer, New York

    Google Scholar 

  • Watwood SL, Tyack PL, Wells RS (2004) Whistle sharing in paired male bottlenose dolphins, Tursiops truncatus. Behav Ecol Sociobiol 55:531–543

    Google Scholar 

  • Watwood SL, Owen ECG, Tyack PL, Wells RS (2005) Signature whistle use by temporarily restrained and free-swimming bottlenose dolphins, Tursiops truncatus. Anim Behav 69:1373–1386

    Google Scholar 

  • Wells RS (2003) Dolphin social complexity: Lessons from long-term study and life history. In: de Waal FBM, Tyack PL (eds) Animal Social Complexity: Intelligence, Culture, and Individualized Societies. Harvard University Press, Cambridge, pp 32–56

    Google Scholar 

  • Wiener SG, Bayart F, Faull KF, Levine S (1990) Behavioral and physiological responses to maternal separation in squirrel monkeys (Saimiri sciureus). Behav Neurosci 104:108–115

    CAS  PubMed  Google Scholar 

  • Wood SN (2017) Generalized Additive Models: An Introduction with R, 2nd edn. Chapman and Hall/CRC, New York

    Google Scholar 

  • Würsig B, Jefferson RA (1990) Methods of photo-identification for small cetaceans. In: Hammond PS, Mizroch SA, Donovan GP (eds) Individual recognition of cetaceans: use pf photo-identification and other techniques to estimate population paramters. Report of the International Whaling Commission, Special Issue, vol 12. Histon, Cambridge, pp 43–52

    Google Scholar 

  • Zuur AF, Ieno EN (2016) A protocol for conducting and presenting results of regression-type analyses. Methods Ecol Evol 7:636:645

    Google Scholar 

  • Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GS (2009) Mixed effects models and extensions in ecology with R. Springer Science and Business Media, New York

    Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14

    Google Scholar 

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The project was carried on with the logistic and financial support of Progetto Natura and Nauta-rcs.

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Correspondence to Gabriella La Manna.

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This work was approved by MareTerra Onlus, University of Sassari and Blue World Institute. All procedures performed in the study were in accordance with the ethical standards of the involved institution.

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La Manna, G., Rako-Gòspic, N., Manghi, M. et al. Influence of environmental, social and behavioural variables on the whistling of the common bottlenose dolphin (Tursiops truncatus). Behav Ecol Sociobiol 73, 121 (2019). https://doi.org/10.1007/s00265-019-2736-2

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