Skip to main content

A Mix of Species: Associations of Heterospecifics Among Primates and Dolphins

  • Chapter
  • First Online:

Part of the book series: Primatology Monographs ((PrimMono))

Abstract

Among mammals, associations of two or more species are likely to involve taxa that are also gregarious intraspecifically, such as primates and delphinids. Although these two groups generally differ in habitat, diet, and the stability of their social units, they share mixed-species association as a conspicuous aspect of their behavior. We compare the general features of such associations in both groups and review the evidence for particular adaptive explanations and proximate mechanisms. On the whole, delphinid associations seem more likely to involve fluid individual membership and hybridization. Random chance seems unlikely to explain many associations in both taxa, but it can be challenging to rule out a shared attraction to environmental features as a driver. Both antipredator and foraging-benefit functions of mixed-species grouping are more directly supported for primates than for dolphins but are plausible adaptive explanations for both groups. Costs of association are better supported in primates, which face feeding competition and increased energetic burden; for dolphins, these costs appear to be minimal, and direct heterospecific social interactions, including harassment, may be more important. Vocal and visual signals may mediate associations, but comparatively little is known about such proximate mechanisms in comparison to adaptive function. Future study of delphinid associations will benefit from some of the approaches taken by primatologists, including the comparison of animals in and out of association, the correlation of association with environmental variables, and the comparison of different communities with different demographic or ecological characteristics.

figure a

A dusky dolphin (right) and common dolphin (left) swim closely together in a mixed-species group in Admiralty Bay, New Zealand. (Photograph credit: Chris Pearson)

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

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

    Article  Google Scholar 

  • Acevedo-Gutiérrez A, DiBerardinis A, Larkin S, Larkin K, Forestell P (2005) Social interactions between tucuxis and bottlenose dolphins in Gandoca-Manazanillo, Costa Rica. LAJAM 4:49–54

    Article  Google Scholar 

  • Au DW (1991) Polyspecific nature of tuna schools: shark, dolphin, and seabird associates. Fish Bull 89:342–354

    Google Scholar 

  • Au DW, Pitman RL (1986) Seabird interactions with dolphins and tuna in the eastern tropical Pacific. Condor 88:304–317

    Article  Google Scholar 

  • Baraff LS, Asmutis-Silvia RA (1998) Long-term association of an individual long-finned pilot whale and Atlantic white-sided dolphin. Mar Mamm Sci 14:155–161

    Article  Google Scholar 

  • Bearzi M (2005) Dolphin sympatric ecology. Mar Ecol Res 1:165–175

    Google Scholar 

  • Bearzi M (2006) California sea lions use dolphins to locate food. J Mammal 87:606–617

    Article  Google Scholar 

  • Bérubé M (2009) Hybridism. In: Perrin WF, Würsig B, Thewissen JGM, Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals, 2nd edn. Elsevier/Academic, Amsterdam, pp 588–592

    Chapter  Google Scholar 

  • Bicca-Marquez JC, Garber PA (2003) Experimental field study of the relative costs and benefits to wild tamarins (Saguinus imperator and S. fuscicollis) of exploiting contestable food patches as single- and mixed-species troops. Am J Primatol 60:139–153

    Article  Google Scholar 

  • Boinski S, Scott PE (1988) Association of birds with monkeys in Costa Rica. Biotropica 20:136–143

    Article  Google Scholar 

  • Brownell RL Jr, Ralls K (1986) Potential for sperm competition in baleen whales. Rep Int Whaling Comm 8:97–112, Special issue

    Google Scholar 

  • Buchanan-Smith HM, Hardie SM (1997) Tamarin mixed-species groups: an evaluation of a combined captive and field approach. Folia Primatol (Basel) 68:272–286

    Article  Google Scholar 

  • Buzzard PJ (2010) Polyspecific association of Cercopithecus campbelli and C. petaurista with C. diana: what are the costs and benefits? Primates 51:307–314

    Article  PubMed  Google Scholar 

  • Camphuysen K, Webb A (1999) Multi-species feeding associations in North Sea seabirds: jointly exploiting a patchy environment. Ardea 87:177–198

    Google Scholar 

  • Chapman CA, Chapman LJ (2000) Interdemic variation in mixed-species association patterns: common diurnal primates in Kibale National Park, Uganda. Behav Ecol Sociobiol 47:129–139

    Article  Google Scholar 

  • Clua É, Grosvalet F (2001) Mixed-species feeding aggregation of dolphins, large tunas and seabirds in the Azores. Aquat Living Resour 14:11–18

    Article  Google Scholar 

  • Cords M (1987) Mixed-species association of Cercopithecus monkeys in the Kakamega Forest, Kenya. Univ Calif Publ Zool 117:1–109

    Google Scholar 

  • Cords M (1990a) Mixed-species association of East African guenons: general patterns or specific examples? Am J Primatol 21:101–114

    Article  Google Scholar 

  • Cords M (1990b) Vigilance and mixed species association in some East African forest guenons. Behav Ecol Sociobiol 26:297–300

    Article  Google Scholar 

  • Cords M (2000) Mixed-species association and group movement. In: Boinski S, Garber P (eds) On the move: how and why animals travel in groups. University of Chicago Press, Chicago, pp 73–99

    Google Scholar 

  • Das K, LePoint G, Loizeau V, DeBacker V, Dauby P, Bouquegneau JM (2000) Tuna and dolphin associations in the North Atlantic: evidence of different ecological niches from stable isotope and heavy metal measurements. Mar Pollut Bull 40:102–109

    Article  CAS  Google Scholar 

  • Detwiler KM, Burrell AS, Jolly CJ (2005) Conservation implications of hybridization in African cercopithecine monkeys. Int J Primatol 26:661–684

    Article  Google Scholar 

  • Dickman CR (1992) Commensal and mutualistic interactions among terrestrial vertebrates. Trends Ecol Evol 7:194–197

    Article  CAS  PubMed  Google Scholar 

  • Dudzinski KM, Thomas JA, Gregg JD (2009) Communication. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals, 2nd edn. Elsevier/Academic, Amsterdam, pp 260–269

    Chapter  Google Scholar 

  • Eckardt W, Zuberbühler K (2004) Cooperation and competition in two forest monkeys. Behav Ecol 14:400–411

    Article  Google Scholar 

  • Fleury MC, Gautier-Hion A (1997) Better to live with allogenerics than to live alone? The case of single male Cercopithecus pogonias in troops of Colobus satanas. Int J Primatol 18:967–974

    Article  Google Scholar 

  • Frantzis A, Herzing DL (2002) Mixed-species associations of striped dolphins (Stenella coeruleoalba), short-beaked common dolphins (Delphinus delphis), and Risso’s dolphins (Grampus griseus) in the Gulf of Corinth (Greece, Mediterranean Sea). Aquat Mamm 28:188–197

    Google Scholar 

  • Freed BZ (2006) Polyspecific associations of crowned lemurs and Sanford’s lemurs in Madagascar. In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptation. Springer, New York, pp 111–131

    Chapter  Google Scholar 

  • Garber PA (1988) Diet, foraging patterns and resource defense in a mixed species troop of Saguinus mystax and S. fuscicollis in Amazonian Peru. Behaviour 105:18–34

    Article  Google Scholar 

  • Garber PA, Bicca-Marquez JC (2001) Evidence of predator sensitive foraging and traveling in single-and mixed-species tamarin troops. In: Miller L (ed) Eat or be eaten: predator-sensitive foraging among primates. Cambridge University Press, Cambridge, pp 138–153

    Google Scholar 

  • Gautier-Hion A (1988) Polyspecific associations among forest guenons: ecological, behavioural and evolutionary aspects. In: Gautier-Hion A, Bourliere F, Gautier JP, Kingdon J (eds) A primate radiation: evolutionary biology of the African guenons. Cambridge University Press, Cambridge, pp 452–476

    Google Scholar 

  • Gautier-Hion A, Quris R, Gautier JP (1983) Monospecific vs. polyspecific life: a comparative study of foraging and anti-predatory tactics in a community of Cercopithecus monkeys. Behav Ecol Sociobiol 12:325–335

    Article  Google Scholar 

  • Gautier-Hion A, Tutin CE (1988) Simultaneous attack by adult males of a polyspecific troop of monkeys against a crowned eagle. Folia primatol. 51:149–151

    Article  CAS  PubMed  Google Scholar 

  • Glos J, Dausmann KH, Linsenmair KE (2007) Mixed-species social aggregations in Madagascan tadpoles: determinants and species composition. J Nat Hist 41:1965–1977

    Article  Google Scholar 

  • Gowans S, Würsig B, Karczmarski L (2008) The social structure and strategies of delphinids: predictions based on an ecological framework. Adv Mar Biol 53:195–294

    Article  Google Scholar 

  • Hankerson SJ, Dietz JM, Raboy BE (2006) Associations between golden-headed lion tamarins and the bird community in the Atlantic Forest of southern Bahia. Int J Primatol 27:487–495

    Article  Google Scholar 

  • Herzing DL, Johnson CM (1997) Interspecific interactions between Atlantic spotted dolphins (Stenella frontalis) and bottlenose dolphins (Tursiops truncatus) in the Bahamas, 1985–1995. Aquat Mamm 23:85–99

    Google Scholar 

  • Herzing DL, Moewe K, Brunnick BJ (2003) Interspecies interactions between Atlantic spotted dolphins, Stenella frontalis, and bottlenose dolphins, Tursiops truncatus, on Great Bahama Bank, Bahamas. Aquat Mamm 29:335–341

    Article  Google Scholar 

  • Heymann EW (1997) The relationship between body size and mixed-species troops of tamarins (Saguinus spp.). Folia Primatol (Basel) 68:287–295

    Article  CAS  Google Scholar 

  • Heymann EW, Buchanan-Smith HM (2000) The behavioural ecology of mixed-species troops of callitrichine primates. Biol Rev 75:169–190

    Article  CAS  PubMed  Google Scholar 

  • Holenweg AK, Noë R, Schabel M (1996) Waser’s gas model applied to associations between red colobus and Diana monkeys. Folia Primatol (Basel) 67:125–136

    Google Scholar 

  • Honer OP, Leumann L, Noe R (1997) Dyadic associations of red colobus and Diana monkey groups in the Tai National Park, Ivory Coast. Primates 38:281–291

    Article  Google Scholar 

  • Hutchinson JMC, Waser PM (2007) Use, misuse and extension of “ideal gas” models of animal encounter. Biol Rev 82:335–359

    Article  PubMed  Google Scholar 

  • Janik VM (2000) Food-related bray calls in wild bottlenose dolphins (Tursiops truncatus). Proc R Soc Lond 267:923–927

    Article  CAS  Google Scholar 

  • Jefferson TA, Stacey PM, Baird RW (1991) A review of killer whale interactions with other marine mammals: predation to co-existence. Mamm Rev 21:151–180

    Article  Google Scholar 

  • Kenagy GJ, Trombulak SC (1986) Size and function of mammalian testes in relation to body size. J Mammal 67:1–22

    Article  Google Scholar 

  • King AJ, Cowlishaw G (2009) Foraging opportunities drive interspecific associations between rock kestrels and desert baboons. J Zool 277:111–118

    Article  Google Scholar 

  • Kiszka JJ (2007) Atypical associations between dugongs (Dugong dugon) and dolphins in a tropical lagoon. J Mar Biol Assoc UK 87:101–104

    Article  Google Scholar 

  • Kiszka J, Perrin WF, Pusineri C, Ridoux V (2011) What drives island-associated tropical dolphins to form mixed-species associations in the southwest Indian Ocean? J Mammal 92:1105–1111

    Article  Google Scholar 

  • Lopes M, Ferrari S (1994) Foraging behavior of a tamarin group (Saguinus fuscicollis wedeli) and interactions with marmosets (Callithrix emiliae). Int J Primatol 15:373–387

    Article  Google Scholar 

  • Markowitz T (2004) Social organization of the New Zealand dusky dolphin. Ph.D. Dissertation, Wildlife and Fisheries Sciences, Texas A&M University, College Station

    Google Scholar 

  • May-Collado L (2010) Changes in whistle structure of two dolphin species during interspecific associations. Ethology 116:1065–1074

    Article  Google Scholar 

  • McGraw WS, Bshary R (2002) Association of terrestrial mangabeys (Cercocebus atys) with arboreal monkeys: experimental evidence for the effects of reduced ground predator pressure on habitat use. Int J Primatol 23:311–325

    Article  Google Scholar 

  • Minta SC, Minta KA, Lott DF (1992) Hunting associations between badgers (Taxidea taxus) and coyotes (Canis latrans). J Mammal 73:814–820

    Article  Google Scholar 

  • Noë R, Bshary R (1997) The formation of red colobus–Diana monkey associations under predation pressure from chimpanzees. Proc R Soc Lond B 264:253–259

    Article  Google Scholar 

  • Noren SR (2008) Infant carrying behaviour in dolphins: costly parental care in an aquatic environment. Funct Ecol 22:284–288

    Article  Google Scholar 

  • Norris KS, Dohl TD (1980) The structure and functions of cetacean schools. In: Herman LM (ed) Cetacean behavior: mechanisms and functions. Wiley, New York, pp 211–261

    Google Scholar 

  • Norris KS, Würsig B, Wells RS, Würsig M (1994) The Hawaiian spinner dolphin. University of California Press, Berkeley, p 408

    Google Scholar 

  • Pearson H (2011) Sociability of female bottlenose dolphins (Tursiops spp.) and chimpanzees (Pan troglodytes): understanding evolutionary pathways toward social convergence. Evol Anthropol 20:85–95

    Article  PubMed  Google Scholar 

  • Peres CA (1992a) Prey-capture benefits in a mixed-species group of Amazonian tamarins, Saguinus fuscicollis and S. mystax. Behav Ecol Sociobiol 31:339–347

    Article  Google Scholar 

  • Peres CA (1992b) Consequences of joint territoriality in a mixed-species group of tamarin monkeys. Behaviour 123:220–246

    Article  Google Scholar 

  • Peres CA (1993) Anti-predator benefits in a mixed-species group of Amazonian tamarins. Folia Primatol (Basel) 61:61–76

    Article  CAS  Google Scholar 

  • Perrin WF, Warner RR, Fiscus CH, Holts DB (1973) Stomach contents of porpoise, Stenella spp., and yellowfin tuna, Thunnus albacares, in mixed-school aggregations. Fish Bull 71:1077–1092

    Google Scholar 

  • Perryman WL, Foster TC (1980) Preliminary report on predation by small whales, mainly the false killer whale, Pseudorca crassidens, on dolphins (Stenella spp. and Delphinus delphis) in the eastern tropical Pacific. Administrative report LJ-80-05. National Marine Fisheries Service, La Jolla

    Google Scholar 

  • Pinheiro T, Ferrari SF, Lopes MA (2011) Polyspecific associations between squirrel monkeys (Saimiri sciureus) and other primates in eastern Amazonia. Am J Primatol 73:1145–1151

    Article  PubMed  Google Scholar 

  • Podolsky RM (1990) Effects of mixed-species association on resource use by Saimiri sciureus and Cebus apella. Am J Primatol 21:147–158

    Article  Google Scholar 

  • Porter LM (2001) Benefits of polyspecific association for the Goeldi’s monkey (Callimico goeldi). Am J Primatol 54:143–158

    Article  CAS  PubMed  Google Scholar 

  • Porter LM, Garber PA (2007) Niche expansion of a cryptic primate, Callimico goeldii, while in mixed species troops. Am J Primatol 69:1340–1353

    Article  PubMed  Google Scholar 

  • Porter LM, Sterr SM, Garber PA (2007) Habitat use and ranging behavior of Callimico goeldi. Int J Primatol 28:1035–1058

    Article  Google Scholar 

  • Psarakos S, Herzing DL, Marten K (2003) Mixed-species associations between pantropical spotted dolphins (Stenella attenuata) and Hawaiian spinner dolphins (Stenella longirostris) in Oahu, Hawaii. Aquat Mamm 29:390–395

    Article  Google Scholar 

  • Quérouil S, Silva MA, Cascão I, Magalhães S, Seabra MI, Machete MA, Santos RS (2008) Why do dolphins from mixed-species associations in the Azores? Ethology 114:1183–1194

    Article  Google Scholar 

  • Rehg JA (2006) Seasonal variation in polyspecific associations among Callimico goeldii, Saguinus labiatus, and S. fuscicollis in Acre, Brazil. Int J Primatol 27:1399–1428

    Article  Google Scholar 

  • Reyes JC (1996) A possible case of hybridism in wild dolphins. Mar Mamm Sci 12:301–307

    Article  Google Scholar 

  • Ross HM, Wilson B (1996) Violent interactions between bottlenose dolphins and harbour porpoises. Proc R Soc Lond 263:283–286

    Article  Google Scholar 

  • Scott MD, Cattanach KL (1998) Diel patterns in aggregations of pelagic dolphins and tuna in the eastern Pacific. Mar Mamm Sci 14:401–422

    Article  Google Scholar 

  • Seavy NE, Apodaca CK, Balcomb SR (2001) Associations of crested guineafowl Guttera pucherani and monkeys in Kibale National Park, Uganda. Ibis 143:310–312

    Article  Google Scholar 

  • Semeniuk CAD, Dill LM (2006) Anti-predator benefits of mixed-species groups of cowtail stingrays (Pastinachus sephen) and whiprays (Himantura uarnak) at rest. Ethology 112:33–43

    Article  Google Scholar 

  • Skorupa JP (1983) Monkeys and matrices: a second look. Oecologia (Berl) 57:391–396

    Article  Google Scholar 

  • Smultea MA, Bacon CE (2012) A comprehensive report of aerial marine mammal monitoring in the Southern California range complex: 2008–2012. EV5 Environmental. Naval Facilities Engineering Command Southwest (NAVFAC SW), San Diego

    Google Scholar 

  • Sockol MD, Raichlen DA, Ponzer H (2007) Chimpanzee locomotor energies and the origin of human bipedalism. Proc Natl Acad Sci USA 104:12265–12269

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Srinivasan M, Markowitz TM (2010) Predator threats and dusky dolphin survival strategies. In: Würsig B, Würsig M (eds) The dusky dolphin: master acrobat off different shores. Elsevier/Academic Press, Amsterdam, pp 133–150

    Chapter  Google Scholar 

  • Stensland E, Angerbjorn A, Berggren P (2003) Mixed species groups in mammals. Mamm Rev 33:205–223

    Article  Google Scholar 

  • Stockin KA, Binedell V, Wiseman N, Brunton DH, Orams MB (2009) Behavior of free-ranging common dolphins (Delphinus sp.) in the Hauraki Gulf, New Zealand. Mar Mamm Sci 25:283–301

    Article  Google Scholar 

  • Strier KB (2006) Primate behavioral ecology, 3rd edn. Allyn & Bacon, Boston

    Google Scholar 

  • Struhsaker TTS (1981) Polyspecific associations among tropical rain-forest primates. Z Tierpsychol 57:268–304

    Article  Google Scholar 

  • Teelen S (2007) Influence of chimpanzee predation on associations between red colobus and red-tailed monkeys at Ngogo, Kibale National Park, Uganda. Int J Primatol 28:593–606

    Article  Google Scholar 

  • Terborgh J (1983) Five New World primates. Freeman, New York

    Google Scholar 

  • Tutin CEG (1999) Fragmented living: behavioral ecology of primates in a forest fragment in the Lopé Reserve, Gabon. Primates 40:249–265

    Article  CAS  PubMed  Google Scholar 

  • Vaughn RL, Shelton DE, Timm LL, Watson LA, Würsig B (2007) Dusky dolphin (Lagenorhynchus obscurus) feeding tactics and multi-species associations. N Z J Mar Freshw Res 41:391–400

    Article  Google Scholar 

  • Vaughn RL, Würsig B, Shelton DS, Timms LL, Watson LA (2008) Dusky dolphins influence prey accessibility for seabirds in Admiralty Bay, New Zealand. J Mammal 89:1051–1058

    Article  Google Scholar 

  • Vaughn RL, Würsig B, Packard J (2010) Dolphin prey herding: prey ball mobility relative to dolphin group and prey ball size, multispecies associates, and feeding duration. Mar Mamm Sci 26:213–225

    Article  Google Scholar 

  • Waser PM (1982) Primate polyspecific associations: do they occur by chance? Anim Behav 30:1–8

    Article  Google Scholar 

  • Waser PM (1984) “Chance” and mixed-species associations. Behav Ecol Sociobiol 15:197–202

    Article  Google Scholar 

  • Waser PM, Case TJ (1981) Monkeys and matrices: on the coexistence of “omnivorous” forest primates. Oecologia (Berl) 49:102–108

    Article  Google Scholar 

  • Waterman JM, Roth JD (2007) Interspecific associations of Cape ground squirrels with two mongoose species: benefit or cost? Behav Ecol Sociobiol 61:1675–1683

    Article  Google Scholar 

  • Weller DW, Würsig B, Whitehead H, Norris JC, Lynn SK, Davis RW, Clauss N, Brown P (1996) Observations of an interaction between sperm whales and short-finned pilot whales in the Gulf of Mexico. Mar Mamm Sci 12:588–594

    Article  Google Scholar 

  • Whitesides GH (1989) Interspecific associations of Diana monkeys, Cercopithecus diana, in Sierra Leone, West Africa: biological significance or chance? Anim Behav 37:760–776

    Article  Google Scholar 

  • Williams TM (1999) The evolution of cost efficient swimming in marine mammals: limits to energetic optimization. Philos Trans R Soc Lond 354:193–220

    Article  Google Scholar 

  • Windfelder T (2001) Interspecific communication in mixed-species groups of tamarins: evidence from playback experiments. Anim Behav 61:1193–1201

    Article  Google Scholar 

  • Wolters S, Zuberbühler K (2003) Mixed-species associations of Diana and Campbelli’s monkeys: the costs and benefits of a forest phenomenon. Behaviour 140:371–385

    Article  Google Scholar 

  • Würsig B, Würsig M (1980) Behavior and ecology of the dusky dolphin, Lagenorhynchus obscurus, in the South Atlantic. Fish Bull 77:871–890

    Google Scholar 

  • Würsig B, Würsig M (2010) The dusky dolphin: master acrobat off different shores. Elsevier/Academic, Amsterdam

    Google Scholar 

  • Würsig B, Wells RS, Norris KS (1994) Food and feeding. In: Norris KS, Würsig B, Wells RS, Würsig M (eds) The Hawaiian spinner dolphin. University of California Press, Berkeley, pp 216–231

    Google Scholar 

  • Würsig B, Duprey N, Weir J (2007) Dusky dolphins (Lagenorhynchus obscurus) in New Zealand waters: present knowledge and research goals. DOC Research and Development Series 270. Department of Conservation, Wellington

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marina Cords .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Japan

About this chapter

Cite this chapter

Cords, M., Würsig, B. (2014). A Mix of Species: Associations of Heterospecifics Among Primates and Dolphins. In: Yamagiwa, J., Karczmarski, L. (eds) Primates and Cetaceans. Primatology Monographs. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54523-1_21

Download citation

Publish with us

Policies and ethics