Abstract
Toothed whales are the ideal model to validate the hypothesis that the complexity of sound communication relates to sociality. Compared to the numerous studies on several toothed whale species with complex social systems, there are very few studies on sound communication in species with simple social systems, such as narrow-ridged finless porpoises (Neophocaena asiaeorientalis). The sounds and behaviors of six captive narrow-ridged finless porpoises (two males and four females) were recorded at the Toba Aquarium, Japan, to reveal the existence of sound communication in this species. We compared the frequency and probability of the production of various sound types in three recording groups and between behaviors. We identified two novel sound types that were separate from echolocation clicks. The “packet sound” was a pulse sequence with repeated pulse packets (sound series of a few pulses with irregular, short inter-pulse intervals) and was produced by the one-porpoise group. The “burst pulses” was a pulse train in which the inter-pulse intervals were significantly shorter than those in packet sounds and were produced during contact behaviors. We considered that these two sound types were the communication sounds in narrow-ridged finless porpoises.
Similar content being viewed by others
Data availability
The datasets generated and/or analyzed during the current study are available from the corresponding author upon reasonable request.
References
Akamatsu T, Wang D, Nakamura K, Wang K (1998) Echolocation range of captive and free-ranging baiji (Lipotes vexillifer), finless porpoise (Neophocaena phocaenoides), and bottlenose dolphin (Tursiops truncatus). J Acoust Soc Am 104:2511–2516
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–266
Caldwell MC, Caldwell DK (1968) Vocalization of naive captive dolphins in small groups. Science 159:1121–1123
Chehida YB, Thumloup J, Schumacher C, Harkins T, Aguilar A, Borrell A, Ferreira M, Rojas-Bracho L, Robertson KM, Taylor BL, Víkingsson GA, Weyna A, Romiguier J, Morin PA, Fontaine MC (2020) Mitochondrial genomics reveals the evolutionary history of the porpoises (Phocoenidae) across the speciation continuum. Sci Rep 10:1–18
Clausen KT, Wahlberg M, Beedholm K, Deruiter K, Madsen PT (2010) Click communication in harbour porpoises. Bioacoustics 20:1–28
Connor RC, Heithaus MR, Barre LM (1999) Superalliance of bottlenose dolphins. Nature 397:571–572
Connor RC, Wells RS, Mann J, Read AJ (2000) The bottlenose dolphin: Social relationships in a fission-fusion society. In: Mann J, Connor RC, Tyack PL, Whitehead H (eds) Cetacean societies: field studies of dolphins and whales. University of Chicago Press, Chicago, pp 91–126
Dawson SM (1991) Clicks and communication: the behavioural and social contexts of Hector’s dolphin vocalizations. Ethology 88:265–276
de Waal FB, Yoshihara D (1983) Reconciliation and redirected affection in rhesus monkeys. Behaviour 85:224–241
Elliser CR, MacIver KH, Green M (2017) Group characteristics, site fidelity, and photo-identification of harbor porpoises, Phocoena phocoena, in Burrows Pass, Fidalgo Island, Washington. Mar Mamm Sci 34:365–384
Finneran JJ (2013) Dolphin “packet” use during long-range echolocation tasks. J Acoust Soc Am 133:1796–1810
Ford JKB (1989) Acoustic behaviour of resident killer whales (Orcinus orca) off Vancouver Island, British Columbia. Can J Zool 67:727–745
Ford JKB (1991) Vocal traditions among resident killer whales (Orcinus orca) in coastal waters of British Columbia. Can J Zool 69:1454–1483
Frankel AS, Yin S (2010) A description of sounds recorded from melon-headed whales (Peponocephala electra) off Hawaii. J Acoust Soc Am 127:3248–3255
Freeberg TM (2006) Social complexity can drive vocal complexity: group size influences vocal information in Carolina chickadees. Psychol Sci 17:557–561
Freeberg TM, Dunbar RI, Ord TJ (2012) Social complexity as a proximate and ultimate factor in communicative complexity. Philos Trans R Soc Lond B Biol Sci 367:1785–1801
Gowans S, Würsig B, Karczmarski L (2007) The social structure and strategies of delphinids: predictions based on an ecological framework. Adv Mar Biol 53:195–294
Grueter CC, Qi X, Zinner D, Bergman T, Li M, Xiang Z, Zhu P, Migliano AB, Miller A, Krützen M, Fischer J, Rubenstein DI, Vidya TNC, Li B, Cantor M, Swedell L (2020) Multilevel organisation of animal sociality. Trends Ecol Evol 35:834–847
Henderson EE, Hildebrand JA, Smith MH (2011) Classification of behavior using vocalizations of Pacific white-sided dolphins (Lagenorhynchus obliquidens). J Acoust Soc Am 130:557–567
Janik VM (2009) Acoustic communication in delphinids. In: Naguib M, Janik VM (eds) Advances in the study of behavior. Academic Press, Burlington, pp 123–157
Janik VM (2013) Cognitive skills in bottlenose dolphin communication. Trends Cogn Sci 17:157–159
Janik VM, Slater PJB (1998) Context-specific use suggests that bottlenose dolphin signature whistles are cohesion calls. Anim Behav 56:829–838
Jones B, Zapetis M, Samuelson MM, Ridgway S (2019) Sounds produced by bottlenose dolphins (Tursiops): a review of the defining characteristics and acoustic criteria of the dolphin vocal repertoire. Bioacoustics 29:399–440
Kamminga C, Stuart C, Silber GK (1996) Investigations on cetacean sonar XI: Intrinsic comparison of the wave shapes of some members of the Phocoenidae family. Aquat Mamm 22:45–55
Kasuya T (2017) Small cetaceans of Japan: Exploitation and biology. CRC Press, Boca Raton
Kondo N, Watanabe S (2009) Contact calls: Information and social function. Jpn Psychol Res 51:197–208
Krams I, Krama T, Freeberg TM, Kullberg C, Lucas JR (2012) Linking social complexity and vocal complexity: a parid perspective. Philos Trans R Soc B Biol Sci 367:1879–1891
Ladegaard M, Mulsow J, Houser DS, Jensen FH, Johnson M, Madsen PT, Finneran JJ (2019) Dolphin echolocation behaviour during active long-range target approaches. J Exp Biol. https://doi.org/10.1242/jeb.189217
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. The MIT Press, Cambridge, pp 107–137
Lammers MO, Au WWL, Herzing DL (2003) The broadband social acoustic signaling behavior of spinner and spotted dolphins. J Acoust Soc Am 114:1629–1639
Le Roux A, Cherry MI, Manser MB (2009) The vocal repertoire in a solitary foraging carnivore, Cynictis penicillata, may reflect facultative sociality. Sci Nat 96:575–584
Li S, Wang K, Wang D, Akamatsu T (2005) Echolocation signals of the free-ranging Yangtze finless porpoise (Neophocaena phocaenoides asiaeorientialis). J Acoust Soc Am 117:3288–3296
Li S, Wang K, Wang D, Dong S, Akamatsu T (2008) Simultaneous production of low- and high-frequency sounds by neonatal finless porpoises. J Acoust Soc Am 124:716–718
Lima SGC, Sousa-Lima RS, Tokumaru RS, Nogueira-Filho SLG, Nogueira SSC (2018) Vocal complexity and sociality in spotted paca (Cuniculus paca). PLoS ONE. https://doi.org/10.1371/journal.pone.0190961
Luís AR, Couchinho MN, Dos Santos ME (2016) A quantitative analysis of pulsed signals emitted by wild bottlenose dolphins. PLoS ONE. https://doi.org/10.1371/journal.pone.0157781
Martin MJ, Gridley T, Elwen SH, Jensen FH (2018) Heaviside’s dolphins (Cephalorhynchus heavisidii) relax acoustic crypsis to increase communication range. Proc R Soc B Biol Sci. https://doi.org/10.1098/rspb.2018.1178
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
May-Collado LJ, Agnarsson I, Wartzok D (2007) Phylogenetic review of tonal sound production in whales in relation to sociality. BMC Evol Biol 7:1–20
McComb K, Semple S (2005) Coevolution of vocal communication and sociality in primates. Biol Lett 1:381–385
Mishima Y, Morisaka T, Itoh M, Matsuo I, Sakaguchi A (2015) Individuality embedded in the isolation calls of captive beluga whales (Delphinapterus leucas). Zool Lett 1:1–13
Mishima Y, Morisaka T, Mishima Y, Sunada T, Miyamoto Y (2018) Redefinition and sexual difference of contact calls in belugas (Delphinapterus leucas). Aquat Mamm 44:538–554
Mishima Y, Morisaka T, Ishikawa M, Karasawa Y, Yoshida Y (2019) Pulsed call sequences as contact calls in Pacific white-sided dolphins (Lagenorhynchus obliquidens). J Acoust Soc Am 146:409–424
Morisaka T, Yoshida Y, Akune Y, Mishima H, Nishimoto S (2013) Exchange of “signature” calls in captive belugas (Delphinapterus leucas). J Ethol 31:141–149
Nakamura K, Akamatsu T, Shimazaki K (1998) Threat clicks of captive harbor porpoises, Phocoena phocoena. Bull Fac Fish Hokkaido Univ 49:91–105
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
Oliveira C, Wahlberg M, Silva MA, Johnson M, Antunes R, Wisniewska DM, Fais A, Gonçalves J, Madsen PT (2016) Sperm whale codas may encode individuality as well as clan identity. J Acoust Soc Am 139:2860–2869
Overstrom NA (1983) Association between burst-pulse sounds and aggressive behavior in captive Atlantic bottlenosed dolphins (Tursiops truncatus). Zoo Biol 2:93–103
Panova EM, Belikov RA, Agafonov AV, Bel’Kovich VM, (2012) The relationship between the behavioral activity and the underwater vocalization of the beluga whale (Delphinapterus leucas). Oceanology 52:79–87
R Core Team (2021) R: A language and environment for statisticl computing. R foundation for statitical computing. Vienna, Austria. https://www.R-project.org/. Accessed Dec 2021
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 121:1213–1218
Rendall D, Cheney DL, Seyfarth RM (2000) Proximate factors mediating “contact” calls in adult female baboons (Papio cynocephalus ursinus) and their infants. J Comp Psychol 114:36–46
Sakai M, Wang D, Wang K, Li S, Akamatsu T (2011) Do porpoises choose their associates? A new method for analyzing social relationships among cetaceans. PLoS One. https://doi.org/10.1371/journal.pone.0028836
Schleich C, Busch C (2002) Acoustic signals of a solitary subterranean rodent Ctenomys talarum (Rodentia: Ctenomyidae): physical characteristics and behavioural correlates. J Ethol 20:123–131
Selbmann A, Deecke VB, Fedutin ID, Filatova OA, Miller PJ, Svavarsson J, Samarra FI (2020) A comparison of Northeast Atlantic killer whale (Orcinus orca) stereotyped call repertoires. Mar Mamm Sci 37:268–289
Sendo S, Morisaka T, Wakabayashi I, Murakami K, Yoshioka M (2021) Stable affiliative social relationships among captive narrow-ridged finless porpoises. Mamm Sci 61:169–177 ((In Japanese))
Serres A, Xu C, Hao Y, Wang D (2021) The click production of captive yangtze finless porpoises (Neophocaena asiaeorientalis asiaorientalis) is influenced by social and environmental factors. Animals 11:1–15
Sibly RM, Nott HMR, Fletcher DJ (1990) Splitting behaviour into bouts. Anim Behav 39:63–69
Simard P, Mann D, Gowans S (2008) First report of burst-pulse vocalizations from white-beaked dolphins (Lagenorhynchus albirostris). J Acoust Soc Am 123:3779–3779
Slater PJB, Lester NP (1982) Minimising errors in splitting behaviour into bouts. Behaviour 79:153–161
Sørensen PM, Wisniewska DM, Jensen FH, Johnson M, Teilmann J, Madsen PT (2018) Click communication in wild harbour porpoises (Phocoena phocoena). Sci Rep 8:1–11
Tamaki N, Morisaka T, Taki M (2006) Does body contact contribute towards repairing relationships? The association between flipper-rubbing and aggressive behavior in captive bottlenose dolphins. Behav Processes 73:209–215
Teilmann J, Larsen F, Desportes G (2007) Time allocation and diving behaviour of harbour porpoises (Phocoena phocoena) in Danish and adjacent waters. J Cetacean Res Manag 9:201–210
Turl CW, Penner RH (1989) Differences in echolocation click patterns of the beluga (Delphinapterus leucas) and the bottlenose dolphin (Tursiops truncatus). J Acoust Soc Am 86:497–502
Tyack PL (1999) Communication and cognition. In: Reynolds JE, Rommel SA (eds) Biology of marine mammals. Smithsonian Institution Press, London, pp 287–323
Vaughn-Hirshorn RL, Hodge KB, Würsig B, Sappenfield RH (2012) Characterizing dusky dolphin sounds from Argentina and New Zealand. J Acoust Soc Am 132:498–506
Walmsley SF, Rendell L, Hussey NE, Marcoux M (2020) Vocal sequences in narwhals (Monodon monoceros). J Acoust Soc Am 147:1078–1091
Wang D (1996) A preliminary study on sound and acoustic behavior of the Yangtze River finless porpoise, Neophocaena phocaenoides. Acta Hydrobiol Sinica 20:127–133
Wang JY, Reeves R (2017) Neophocaena asiaeorientalis. The IUCN red list of threatened species 2017:e.T41754A50381766
Watkins WA, Schevill WE (1977) Sperm whale codas. J Acoust Soc Am 62:1485–1490
Weilgart L, Whitehead H (1997) Group-specific dialects and geographical variation in coda repertoire in South Pacific sperm whales. Behav Ecol Sociobiol 40:277–285
Wu HP, Hao YJ, Yu XY, Xian YJ, Zhao QZ, Chen DQ, Kuang XA, Kou ZB, Feng KK, Gong WM, Wang D (2010) Variation in sexual behaviors in a group of captive male Yangtze finless porpoises (Neophocaena phocaenoides asiaeorientalis): Motivated by physiological changes? Theriogenology 74:1467–1475
Yamamoto C, Morisaka T, Furuta K, Ishibashi T, Yoshida A, Taki M, Mori Y, Amano M (2015) Post-conflict affiliation as conflict management in captive bottlenose dolphins (Tursiops truncatus) Sci Rep. doi: https://doi.org/10.1038/srep14275
Yoshida YM, Morisaka T, Sakai M, Iwasaki M, Wakabayashi I, Seko A, Kasamatsu M, Akamatsu T, Kohshima S (2014) Sound variation and function in captive Commerson’s dolphins (Cephalorhynchus commersonii). Behav Processes 108:11–19
Yoshida YM, Morisaka T, Nakahara F, Saito S (2016) Receiving sensitivity of the hydrophones attached to acrylic plate ─ towards simplification of dolphin sound study at aquariums ─. Bull Inst Oceanic Res & Develop, Tokai Univ 37:1–6 ((In Japanese))
Acknowledgements
We are grateful to K. Okude, Y. Wakai, S. Mitani, and the staff of the Toba Aquarium for their support. We would also like to thank Dr. C. Yamamoto of the Cetacean Research Center, Mie University, and the members of the Laboratory of Fish Stock Enhancement at Mie University for their helpful comments. This research was supported by the Collaborative Research Program of the Wildlife Research Center, Kyoto University (2019-A-15) for T.T. This work was supported by JSPS KAKENHI (Grant Number 15H05709) for T.M.
Funding
This study was funded by the Collaborative Research Program of the Wildlife Research Center, Kyoto University (2019-A-15) for T.T., and JSPS KAKENHI (Grant Number 15H05709) for T.M.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest directly relevant to the content of this work.
Ethical approval
This study was conducted in accordance with the guidelines for ethological studies of the Japan Ethological Society. The narrow-ridged finless porpoise subjects were not relocated for our study, but for aquarium purposes, such as producing offspring and artificial rearing. They behaved freely throughout the study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Terada, T., Morisaka, T., Wakabayashi, I. et al. Communication sounds produced by captive narrow-ridged finless porpoises (Neophocaena asiaeorientalis). J Ethol 40, 245–256 (2022). https://doi.org/10.1007/s10164-022-00755-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10164-022-00755-0