Abstract
Social living, long lifespan and advanced cognitive skills provided favourable conditions for the development of pro-social behaviours and cooperative activities in cetacean. Dolphins have been observed to collaborate for various purposes, finding food, finding mates or raising and teaching younger individuals. This study investigated the potential impact of demographic factors (sex and age), social factors (relatedness and group size), and individual experience in a cooperative problem solving task. A cognitive enrichment device was tested with 22 dolphins in 11 group settings. The device consisted of a tube, containing ice and fish, sealed by two caps with rope handles and designed to be operated by pairs of dolphins. The investigation focused on the differences in trial outcome (success rate of cooperative opening of the device) and on cooperative play (dolphin pairs engaging in synchronous swim with the device). From the five potential factors, sex showed the highest impact. Cooperative openings were more than four times more frequent in males than in females (75% vs 17%, respectively), and cooperative play was exclusively displayed by adult males. Given the strong correlation between cooperative opening and cooperative play, we argue the two behaviours can be regarded as parts of a cooperative action chain. This study provides the first evidence for intersexual differences in collaborative actions in dolphins under systematic testing conditions.
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References
Aureli F, de Waal FB (2000) Natural conflict resolution. University of California Press, Oakland
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
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
Clark FE (2011) Great ape cognition and captive care: can cognitive challenges enhance well-being? Appl Anim Behav Sci 135:1–12. https://doi.org/10.1016/j.applanim.2011.10.010
Clark FE (2013) Marine mammal cognition and captive care: a proposal for cognitive enrichment in zoos and aquariums. J Zoo Aquar Res 1:1–6. https://doi.org/10.19227/jzar.v1i1.19
Clark FE (2017) Cognitive enrichment and welfare: Current approaches and future directions. Anim Behav Cogn 4:52–71. https://doi.org/10.12966/abc.05.02.2017
Clark FE, Davies SL, Madigan AW, Warner AJ, Kuczaj SA (2013) Cognitive enrichment for bottlenose dolphins (Tursiops truncatus): evaluation of a novel underwater maze device. Zoo Biol 32:608–619. https://doi.org/10.1002/zoo.21096
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. Philos 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 R, Whitehead H (2005) Alliances II. Rates of encounter during resource utilization: a general model of intrasexual alliance formation in fission–fusion societies. Anim Behav 69:127–132. https://doi.org/10.1016/j.anbehav.2004.02.022
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 (2000a) 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, Wells RS, Mann J, Read AJ (2000b) 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
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
Diaz-Aguirre F, Parra GJ, Passadore C, Möller L (2018) Kinship influences social bonds among male southern Australian bottlenose dolphins (Tursiopscf. australis). Behav Ecol Sociobiol. https://doi.org/10.1007/s00265-018-2621-4
Drea CM, Carter AN (2009) Cooperative problem solving in a social carnivore. Anim Behav 78:967–977. https://doi.org/10.1016/j.anbehav.2009.06.030
Duffield DA, Wells RS (1991) The combined application of chromosome, protein and molecular data for the investigation of social unit structure and dynamics in Tursiops truncatus. Genetic Ecology of Whales and Dolphins. Rep Int Whal Comm Special 13:155–169
Elliser CR, Herzing DL (2014) Long-term social structure of a resident community of Atlantic spotted dolphins, Stenella frontalis, in the Bahamas 1991–2002. Mar Mamm Sci 30:308–328. https://doi.org/10.1111/mms.12039
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
Frère CH, Krützen M, Mann J, Connor RC, Bejder L, Sherwin WB (2010) Social and genetic interactions drive fitness variation in a free-living dolphin population. Proc Natl Acad Sci 107:19949–19954. https://doi.org/10.1073/pnas.1007997107
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
Hartman KL, Visser F, Hendriks AJE (2008) Social structure of Risso’s dolphins (Grampus griseus) at the Azores: a stratified community based on highly associated social units. Can J Zool 86:4. https://doi.org/10.1139/Z07-138
Hirata S, Fuwa K (2007) Chimpanzees (Pan troglodytes) learn to act with other individuals in a cooperative task. Primates 48:13–21. https://doi.org/10.1007/s10329-006-0022-1
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 13:e0196658. 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
King SL, Allen SJ, Connor RC, Jaakkola K (2016) Cooperation or dolphin ‘tug-of-war’? Comment on Kuczaj et al. and Eskelinen et al. Anim Cogn 19:1227–1229
Krützen M, Sherwin WB, Connor RC, Barre LM, Van de Casteele T, Mann J, Brooks R (2003) Contrasting relatedness patterns in bottlenose dolphins (Tursiops sp.) with different alliance strategies. Proc R Soc B Biol Sci 270:497–502. https://doi.org/10.1098/rspb.2002.2229
Krützen M, Barré LM, Connor RC, Mann J, Sherwin WB (2004) ‘O father: where art thou?’—Paternity assessment in an open fission–fusion society of wild bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia. Mol Ecol 13:1975–1990. https://doi.org/10.1111/j.1365-294X.2004.02192.x
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, Makecha R, Trone M, Paulos RD, Ramos JA (2006) Role of peers in cultural innovation and cultural transmission: evidence from the play of dolphin calves. Int J Comp Psychol 19:223–240. https://escholarship.org/uc/item/4pn1t50s
Kuczaj SA II, Gory JD, Xitco MJ Jr (2009) How intelligent are dolphins? A partial answer based on their ability to plan their behavior when confronted with novel problems. Jpn J Anim Psychol 59:99–115. https://doi.org/10.2502/janip.59.1.9
Kuczaj SA II, Xitco MJ Jr, Gory JD (2010) Can dolphins plan their behavior? Int J Comp Psychol 23:664–670
Kuczaj SA II, Yeater D, Highfill L (2012) How selective is social learning in dolphins? Int J Comp Psychol 25(3):221–236
Kuczaj SA II, Winship KA, 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
Mackey AD, Makecha RN, Kuczaj SA II (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
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
Melis AP, Hare B, Tomasello M (2006) Chimpanzees recruit the best collaborators. Science 311:1297–1300. https://doi.org/10.1126/science.1123007
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 Lond Ser B Biol Sci 268:1941–1947. https://doi.org/10.1098/rspb.2001.1756
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 61:109–117. https://doi.org/10.1007/s00265-006-0241-x
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. Zool (Curitiba) 30:585–591. https://doi.org/10.1590/S1984-46702013005000013
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
Paulos RD, Trone M, Kuczaj SA II (2010) Play in wild and captive cetaceans. Int J Comp Psychol 23:701–722
Pearson HC (2011) Sociability of female bottlenose dolphins (Tursiops spp.) and chimpanzees (Pan troglodytes): understanding evolutionary pathways toward social convergence . Evol Anthropol Issues News Rev 20:85–95. https://doi.org/10.1002/evan.20296
Péron F, Rat-Fischer L, Lalot M, Nagle L, Bovet D (2011) Cooperative problem solving in African grey parrots (Psittacus erithacus). Anim Cogn 14:545–553. https://doi.org/10.1007/s10071-011-0389-2
Plotnik JM, Lair R, Suphachoksahakun W, de Waal FB (2011) Elephants know when they need a helping trunk in a cooperative task. Proc Natl Acad Sci 108:5116–5121. https://doi.org/10.1073/pnas.1101765108
Sakai M, Morisaka T, Kogi K, Hishii T, Kohshima S (2010) Fine-scale analysis of synchronous breathing in wild Indo-Pacific bottlenose dolphins (Tursiops aduncus). Behav Process 83:48–53
Senigaglia V, de Stephanis R, Verborgh P, Lusseau D (2012) The role of synchronized swimming as affiliative and anti-predatory behavior in long-finned pilot whales. Behav Proc 91:8–14
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. Zool (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
Tsai YJJ, Mann J (2013) Dispersal, philopatry, and the role of fission-fusion dynamics in bottlenose dolphins. Mar Mamm Sci 29:261–279. https://doi.org/10.1111/j.1748-7692.2011.00559.x
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
Whitehead H, Connor R (2005) Alliances I. how large should alliances be? Anim Behav 69:117–126. https://doi.org/10.1016/j.anbehav.2004.02.021
Wright S (1922) Coefficients of inbreeding and relationship. Am Nat 56:330–338. https://doi.org/10.1086/279872
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
Acknowledgements
We thank the Marine Mammal Department of Ocean Park Hong Kong for their support during our experiment. We would also like to Ella Cherring, Hoi Ching Lam, Mei Yan Low, Ka Man Lau, Ying Ting Ng and Man Sum Tong for their valuable help with data collection and video analysis. Special thanks to S. A. Kuczaj, who provided invaluable help on planning the experiment and for his inspiration and encouragement. The project was approved by the Animal Welfare, Ethics and Care Committee of Ocean Park Conservation. This work was supported by the Research Department of Ocean Park Hong Kong. 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 ConservationTM.
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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-19-4 New National Excellence Program of the Ministry of Innovation and Technology, Hungary.
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Matrai, E., Kwok, S.T., Boos, M. et al. Cognitive enrichment device provides evidence for intersexual differences in collaborative actions in Indo-Pacific bottlenose dolphins (Tursiops aduncus). Anim Cogn 24, 1215–1225 (2021). https://doi.org/10.1007/s10071-021-01510-7
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DOI: https://doi.org/10.1007/s10071-021-01510-7