Abstract
Due to the diversity of the phenomenon, dolphin cooperation has attracted considerable research interest in both wild populations and those under human care. Dolphins cooperate in various contexts, including group hunting, alloparental care, social learning, social play and alliance formation for securing mates. This investigation focused on the effect of group size and partner choice in a cooperative task using systematic group testing. A cooperative enrichment device was made of a PVC tube containing fish and ice that was temporarily sealed with two PVC caps with rope handles attached. The device was designed to be operated by pairs of dolphins, opened by simultaneous pull of its two handles. The analysis focused on two behaviours, cooperative opening and cooperative play with the device. Testing focused on an adult male dolphin group including four to six individuals and using a single or two devices. Altogether five group testing arrangements and a pairwise testing phase were conducted. Out of the six dolphins, five showed active involvement. All ten possible pairs of the five active dolphins were successful in opening and playing with the device cooperatively. Cooperation increased with group size, but the social networks showed no significant differences among group arrangements. However, the cooperative pairs showed a significant difference in success rate during pairwise vs group testing, while demonstrating a strong partner preference. This study provides the first evidence for partner choice with regards to cooperation in male dolphins.
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References
Bagley KC, Winship K, Bolton T, Foerder P (2020) Personality and affiliation in a cooperative task for bottlenose dolphin (Tursiops truncatus) dyads. Int J Comp Psychol. https://doi.org/10.5070/P4331043587
Bender CE, Herzing DL, Bjorklund DF (2009) Evidence of teaching in atlantic spotted dolphins (Stenella frontalis) by mother dolphins foraging in the presence of their calves. Anim Cogn 12:43–53. https://doi.org/10.1007/s10071-008-0169-9
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57:289–300
Benoit-Bird KJ, Au WW (2009) Cooperative prey herding by the pelagic dolphin, Stenella longirostris. J Acoust Soc Am 125:125–137. https://doi.org/10.1121/1.2967480
Cheney DL (2011) Extent and limits of cooperation in animals. Proc Natl Acad Sci 108:10902–10909. https://doi.org/10.1073/pnas.1100291108
Cheng K, Byrne RW (2018) Why human environments enhance animal capacities to use objects: evidence from keas (nestor notabilis) and apes (gorilla gorilla, pan paniscus, pongo abelii, pongo pygmaeus). J Comp Psychol 132:419–426. https://doi.org/10.1037/com0000121
Clutton-Brock T (2009) Cooperation between non-kin in animal societies. Nature 462:51–57. https://doi.org/10.1038/nature08366
Connor RC (2007) Dolphin social intelligence: complex alliance relationships in bottlenose dolphins and a consideration of selective environments for extreme brain size evolution in mammals. Phil Trans R Soc B Biol Sci 362:587–602. https://doi.org/10.1098/rstb.2006.1997
Connor RC, Krützen M (2015) Male dolphin alliances in shark bay: changing perspectives in a 30-year study. Anim Behav 103:223–235. https://doi.org/10.1016/j.anbehav.2015.02.019
Connor RC, Smolker RA, Richards AF (1992) Two levels of alliance formation among male bottlenose dolphins (Tursiops sp.). Proc Natl Acad Sci 89:987–990. https://doi.org/10.1073/pnas.89.3.987
Connor RC, Heithaus MR, Barre LM (1999) Superalliance of bottlenose dolphins. Nature 397:571
Connor RC, Mann J, Read A, Wells RJ (2000) The bottlenose dolphin: social relationships in a fission-fusion society. In: Mann J, Connor RC, Tyack P, Whitehead H (eds) Cetacean societies: field studies of whales and dolphins. University of Chicago Press, Chicago (IL), pp 91–126
Connor RC, Heithaus MR, Barre LM (2001) Complex social structure, alliance stability and mating access in a bottlenose dolphin ‘super-alliance.’ Proc R Soc B Biol Sci 268:263–267. https://doi.org/10.1098/rspb.2000.1357
Connor RC, Smolker R, Bejder L (2006) Synchrony, social behaviour and alliance affiliation in Indian ocean bottlenose dolphins, tursiops aduncus. Anim Behav 72:1371–1378. https://doi.org/10.1016/j.anbehav.2006.03.014
Connor RC, Cioffi WR, Randić S, Allen SJ, Watson-Capps J, Krützen M (2017) Male alliance behaviour and mating access varies with habitat in a dolphin social network . Sci Rep 7:46354. https://doi.org/10.1038/srep46354
Covas R, Doutrelant C (2019) Testing the sexual and social benefits of cooperation in animals . Trends Ecol Evol 34:112–120. https://doi.org/10.1016/j.tree.2018.11.006
Engleby LK, Powell JR (2019) Detailed observations and mechanisms of mud ring feeding by common bottlenose dolphins (Tursiops truncatus truncatus) in Florida Bay, Florida, USA. Mar Mamm Sci 35:1162–1172. https://doi.org/10.1111/mms.12583
Eskelinen HC, Winship KA, Jones BL, Ames AE, Kuczaj SA (2016) Acoustic behavior associated with cooperative task success in bottlenose dolphins (Tursiops truncatus). Anim Cogn 19:789–797. https://doi.org/10.1007/s10071-016-0978-1
Fessler DM, Holbrook C (2016) Synchronized behavior increases assessments of the formidability and cohesion of coalitions. Evol Hum Behav 37:502–509. https://doi.org/10.1016/j.evolhumbehav.2016.05.003
Friard O, Gamba M (2016) BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evol 7:1325–1330. https://doi.org/10.1111/2041-210X.12584
Gazda SK, Connor RC, Edgar RK, Cox F (2005) A division of labour with role specialization in group-hunting bottlenose dolphins (Tursiops truncatus) off Cedar Key, Florida. Proc R Soc B Biol Sci 272:135–140. https://doi.org/10.1098/rspb.2004.2937
Gerber L et al (2020) Affiliation history and age similarity predict alliance formation in adult male bottlenose dolphins. Behav Ecol 31:361–370. https://doi.org/10.1093/beheco/arz195
Gero S, Engelhaupt D, Rendell L, Whitehead H (2009) Who cares? Between-group variation in alloparental caregiving in sperm whales. Behav Ecol 20:838–843. https://doi.org/10.1093/beheco/arp068
Ikeda H, Komaba M, Komaba K, Matsuya A, Kawakubo A, Nakahara F (2018) Social object play between captive bottlenose and Risso’s dolphins. PLoS ONE. https://doi.org/10.1371/journal.pone.0196658
Jaakkola K, Guarino E, Donegan K, King SL (2018) Bottlenose dolphins can understand their partner’s role in a cooperative task. Proc R Soc B Biol Sci 285:20180948. https://doi.org/10.1098/rspb.2018.0948
Jiménez PJ, Alava JJ (2015) Strand-feeding by coastal bottlenose dolphins (Tursiops truncatus) in the Gulf of Guayaquil, Ecuador. Lat Am J Aquat Mamm 10:33–37. https://doi.org/10.5597/lajam00191
Kuczaj SA, Eskelinen HC (2014) Why do dolphins play? Anim Behav Cogn 1:113–127. https://doi.org/10.12966/abc.05.03.2014
Kuczaj SA II, Yeater D, Highfill L (2012) How selective is social learning in dolphins? Int J Comp Psychol 25(3):221–236
Kuczaj Winship SAKA, Eskelinen HC (2015) Can bottlenose dolphins (Tursiops truncatus) cooperate when solving a novel task? Anim Cogn 18:543–550. https://doi.org/10.1007/s10071-014-0822-4
Langergraber KE, Mitani JC, Watts DP, Vigilant L (2013) Male–female socio-spatial relationships and reproduction in wild chimpanzees. Behav Ecol Sociobiol 67:861–873. https://doi.org/10.1007/s00265-013-1509-6
Lehmann J, Korstjens AH, Dunbar RIM (2007) Fission-fusion social systems as a strategy for coping with ecological constraints: a primate case. Evol Ecol 21:613–634. https://doi.org/10.1007/s10682-006-9141-9
Lewis JS, Wartzok D, Heithaus MR (2011) Highly dynamic fission–fusion species can exhibit leadership when traveling. Behav Ecol Sociobiol 65:1061–1069. https://doi.org/10.1007/s00265-010-1113-y
Lewis JS, Wartzok D, Heithaus M, Krützen M (2013) Could relatedness help explain why individuals lead in bottlenose dolphin groups? PLoS ONE 8:e58162. https://doi.org/10.1371/journal.pone.0058162
Mackey AD, Makecha RN, Kuczaj SA (2014) The developement of social play in bottlenose dolphins (Tursiops truncatus). Anim Behav Cogn 1:19–35. https://doi.org/10.12966/abc.02.02.2014
Mani A, Mullainathan S, Shafir E, Zhao J (2013) Poverty impedes cognitive function. Science 341:976–980. https://doi.org/10.1126/science.1238041
Mann J, Smuts BB (1998) Natal attraction: allomaternal care and mother-infant separations in wild bottlenose dolphins. Anim Behav 55:1097–1113. https://doi.org/10.1006/anbe.1997.0637
Mann J, Sargeant B, Minor M (2007) Calf inspections of fish catches in bottlenose dolphins (Tursiops sp.): opportunities for oblique social learning? Mar Mamm Sci 23:197–202. https://doi.org/10.1111/j.1748-7692.2006.00087.x
Matrai E, Ng AKW, Chan MMH, Gendron SM, Dudzinski KM (2020) Testing use of a potential cognitive enrichment device by an Indo-Pacific bottlenose dolphin (Tursiops aduncus). Zoo Biol 39:156–167. https://doi.org/10.1002/zoo.21536
Matrai E, Kwok ST, Boos M, Pogany A (2021) Cognitive enrichment device provides evidence for intersexual differences in collaborative actions in Indo-Pacific bottlenose dolphins (Tursiops aduncus). Anim Cogn. https://doi.org/10.1007/s10071-021-01510-7
McAuliffe K, Thornton A (2015) The psychology of cooperation in animals. J Zool 295:23–35. https://doi.org/10.1111/jzo.12204
McCue LM, Cioffi WR, Heithaus MR, Barrè L, Connor RC (2020) Synchrony, leadership, and association in male Indo-pacific bottlenose dolphins (Tursiops aduncus). Ethology 126:741–750. https://doi.org/10.1111/eth.13025
Möller LM, Beheregaray LB, Harcourt RG, Krützen M (2001) Alliance membership and kinship in wild male bottlenose dolphins (Tursiops aduncus) of southeastern Australia. Proc R Soc London Ser B Biol Sci 268:1941–1947. https://doi.org/10.1098/rspb.2001.1756
Mullainathan S, Shafir E (2013) Scarcity: why having too little means so much. Allen Lane, London
Nowak MA (2006) Five rules for the evolution of cooperation. Science 314:1560–1563. https://doi.org/10.1126/science.1133755
Oliveira ECDS, Tardin RH, Poletto FR, Simão SM (2013) Coordinated feeding behavior of the Guiana dolphin, Sotalia guianensis (Cetacea: Delphinidae), in southeastern Brazil: a comparison between populations. Zoologia (curitiba) 30:585–591. https://doi.org/10.1590/S1984-46702013005000013
Owen E, Wells R, Hofmann S (2002) Ranging and association patterns of paired and unpaired adult male Atlantic bottlenose dolphins, Tursiops truncatus, in Sarasota, Florida, provide no evidence for alternative mating strategies. Can J Zool 80:2072–2089. https://doi.org/10.1139/z02-195
Packer C (1977) Reciprocal altruism in papio anubis. Nature 265:441–443. https://doi.org/10.1038/265441a0
Parsons KM, Durban JW, Claridge DE, Balcomb KC, Noble LR, Thompson PM (2003) Kinship as a basis for alliance formation between male bottlenose dolphins, Tursiops truncatus, in the Bahamas. Anim Behav 66:185–194. https://doi.org/10.1006/anbe.2003.2186
Pennisi E (2005) How did cooperative behaviour evolve? Science 309:93–93. https://doi.org/10.1126/science.309.5731.93
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 27 July 2021
Samuels A, Gifford T (1997) A quantitative assessment of dominance relations among bottlenose dolphins. Mar Mamm Sci 13:70–99. https://doi.org/10.1111/j.1748-7692.1997.tb00613.x
Schreier AL, Swedell L (2012) Ecology and sociality in a multilevel society: ecological determinants of spatial cohesion in hamadrayas baboons. Am J Phys Anthropol 148:580–588. https://doi.org/10.1002/ajpa.22076
Silber GK, Fertl D (1995) Intentional beaching by bottlenose dolphins (Tursiops truncatus) in the Colorado River Delta, Mexico. Aquat Mamm 21:183–186
Smolker RA, Richards AF, Connor RC, Pepper JW (1992) Sex differences in patterns of association among Indian Ocean bottlenose dolphins. Behaviour 123:38–69. https://doi.org/10.1163/156853992X00101
Tardin RHO, Especie MA, Nery MF, D’Azeredo FT, Simão SM (2011) Coordinated feeding tactics of the Guiana dolphin, Sotalia guianensis (Cetacea: Delphinidae), in Ilha Grande Bay, Rio de Janeiro. Brazil Zoologia (curitiba, Impresso) 28:291–296. https://doi.org/10.1590/s1984-46702011000300002
Torres LG, Read AJ (2009) Where to catch a fish? The influence of foraging tactics on the ecology of bottlenose dolphins (Tursiops truncatus) in Florida Bay, Florida. Mar Mamm Sci 25:797–815. https://doi.org/10.1111/j.1748-7692.2009.00297.x
van Schaik CP, van Jaram H (1994) Male bonds: afilliative relationships among nonhuman primate males. Behaviour 130:309–337. https://doi.org/10.1163/156853994X00587
Watts DP (1998) Coalitionary mate guarding by male chimpanzees at Ngogo, Kibale National Park, Uganda. Behav Ecol Sociobiol 44:43–55. https://doi.org/10.1007/s002650050513
Wells RS, Scott MD, Irvine AB (1987) The social structure of free-ranging bottlenose dolphins. In: Genoways HH (ed) Current mammalogy. Springer, Boston, pp 247–305. https://doi.org/10.1007/978-1-4757-9909-5_7
Wiszniewski J, Brown C, Möller LM (2012) Complex patterns in male alliance formation in a dolphin social network. J Mamm 93:239–250. https://doi.org/10.1644/10-MAMM-A-366.1
Yamamoto C, Kashiwagi N, Otsuka M, Sakai M, Tomonaga M (2019) Cooperation in bottlenose dolphins: bidirectional coordination in a rope-pulling task. PeerJ 7:e7826. https://doi.org/10.7717/peerj.7826
Zuolo F (2020) Cooperation with animals? What is and what is not. J Agric Environ Ethics 33:315–335. https://doi.org/10.1007/s10806-020-09826-z
Acknowledgements
We thank the Marine Mammal Department of Ocean Park Hong Kong for their support during our experiment. We would also like to thank Xiao Lin for his valuable comments regarding the data analysis. Special thanks to S. A. Kuczaj, who provided invaluable help on planning the experiment and for his inspiration and encouragement.
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This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. ÁP was supported by the János Bolyai Research Scholarship of the Hungarian Academy of Sciences and the ÚNKP-20-5 New National Excellence Program of the Ministry for Innovation and Technology from the source of the National Research, Development and Innovation Fund.
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The project was approved by the Animal Welfare, Ethics and Care Committee of Ocean Park Conservation. Ocean Park gained accreditation from the Association of Zoos and Aquariums (AZA), it is also a member of the World Association of Zoos and Aquariums (WAZA). The animal welfare standards at the Park were also approved by the American Humane Association under its Humane Conservation™.
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Matrai, E., Kwok, S.T., Boos, M. et al. Group size, partner choice and collaborative actions in male Indo-Pacific bottlenose dolphins (Tursiops aduncus). Anim Cogn 25, 179–193 (2022). https://doi.org/10.1007/s10071-021-01541-0
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DOI: https://doi.org/10.1007/s10071-021-01541-0