Skip to main content

Advertisement

SpringerLink
Log in

Sexual segregation when foraging in an extremely social killer whale population

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Resident, fish-eating killer whales in the northeastern Pacific Ocean live in multi-generational matrilines containing both sexes. The degree of maternal fidelity and natal philopatry in this killer whale society is extreme even by the standards of lions, elephants or any highly social mammal. Benefits of group living include cooperative foraging and alloparental care, but few studies have explored how killer whales avoid within-group competition for prey. This study measured focal animal behaviour from one population in its legally designated critical habitat. Adult males and females overlapped spatially whilst resting, travelling and socialising, but during feeding bouts, females foraged nearshore in shallower waters, whilst adult males distributed foraging effort throughout the study area, with no statistically significant depth preference. We postulate that sex-biased dispersal in foraging ecology reflects physiological capacity for deeper diving in males than females, which may be either a driver or consequence of extreme sexual dimorphism in the species; alternative interpretations exist. Killer whales appear to be a cosmopolitan species complex including populations that range widely in body size and diet. Our physiological limitation theory could be tested with other ecotypes. For the northern resident killer whale population we studied, we postulate that our finding may indicate a mechanism to avoid or reduce competition for food within the family unit whilst ensuring group cohesion. Investigating sex differences in foraging habitat informs area-based management and conservation of this threatened population, but studies on other ecotypes are needed to improve our understanding of the evolution of sociality in this species.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alanärä A, Burns MD, Metcalfe NB (2001) Intraspecific resource partitioning in brown trout: the temporal distribution of foraging is determined by social rank. J Anim Ecol 70:980–986

    Article  Google Scholar 

  • Ashe E, Noren D, Williams R (2010) Animal behaviour and marine protected areas: incorporating behavioural data into the selection of marine protected areas for an endangered killer whale population. Anim Conserv 13:196–203

    Article  Google Scholar 

  • Bain D (1989) An evaluation of evolutionary processes: studies of natural selection, dispersal, and cultural evolution in killer whales (Orcinus orca). PhD Thesis, University of California, Santa Cruz

  • Baird R (2000) The killer whale—foraging specializations and group hunting. In: Mann J, Connor RC, Tyack PL, Whitehead H (eds) Cetacean societies: field studies of dolphins and whales. University of Chicago Press, Chicago, pp 127–153

    Google Scholar 

  • Baird R, Hanson M, Dill L (2005) Factors influencing the diving behaviour of fish-eating killer whales: sex differences and diel and interannual variation in diving rates. Can J Zool 83:257–267

    Article  Google Scholar 

  • Beauchamp G (2012) Foraging speed in staging flocks of semipalmated sandpipers: evidence for scramble competition. Oecologia 169:975–980

    Article  PubMed  Google Scholar 

  • Beauchamp G (2014) Social predation: how group living benefits predators and prey. Academic, New York

    Google Scholar 

  • Beck C, Iverson S, Bowen W, Blanchard W (2007) Sex differences in grey seal diet reflect seasonal variation in foraging behaviour and reproductive expenditure: evidence from quantitative fatty acid signature analysis. J Anim Ecol 76:490–502

    Article  PubMed  Google Scholar 

  • Breed G, Bowen W, McMillan J, Leonard M (2006) Sexual segregation of seasonal foraging habitats in a non-migratory marine mammal. Proc R Soc Lond B 273:2319–2326

    Article  Google Scholar 

  • Brent LJN, Franks DW, Foster EA, Balcomb KC, Cant MA, Croft DP (2015) Ecological knowledge, leadership, and the evolution of menopause in killer whales. Curr Biol 25:746–750

    Article  PubMed  CAS  Google Scholar 

  • Browning NE, Cockcroft VG, Worthy GA (2014) Resource partitioning among South African delphinids. J Exp Mar Biol Ecol 457:15–21

    Article  Google Scholar 

  • Candy J, Quinn T (1999) Behavior of adult Chinook salmon (Oncorhynchus tshawytscha) in British Columbia coastal waters determined from ultrasonic telemetry. Can J Zool 77:1161–1169

    Article  Google Scholar 

  • Clark CW, Mangel M (1986) The evolutionary advantages of group foraging. Theor Popul Biol 30:45–75

    Article  Google Scholar 

  • Conradt L (1998) Could asynchrony in activity between the sexes cause intersexual social segregation in ruminants? Proc R Soc Lond B 265:1359–1368

    Article  CAS  Google Scholar 

  • Conradt L, Roper T (2000) Activity synchrony and social cohesion: a fission-fusion model. Proc R Soc Lond B 267:2213–2218

    Article  CAS  Google Scholar 

  • Conradt L, Roper T (2005) Consensus decision making in animals. Trends Ecol Evol 20:449–456

    Article  PubMed  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/

  • COSEWIC (2008) COSEWIC assessment and update status report on the killer whale Orcinus orca, southern resident population, northern resident population, West Coast transient population, offshore population and Northwest Atlantic/Eastern Arctic population, in Canada, Committee on the Status of Endangered Wildlife in Canada, Ottawa, www.sararegistry.gc.ca/status/status_e.cfm

  • Dechmann DK, Heucke SL, Giuggioli L, Safi K, Voigt CC, Wikelski M (2009) Experimental evidence for group hunting via eavesdropping in echolocating bats. Proc R Soc Lond B 276:2721–2728

    Article  Google Scholar 

  • Ekstrom C (2014) MESS: Miscellaneous Esoteric Statistical Scripts. R package version 0.3-2, http://CRAN.R-project.org/package=MESS

  • Felleman F, Heimlich-Boran J, Osborne RW (1991) The feeding ecology of killer whales (Orcinus orca) in the Pacific Northwest. In: Pryor K, Norris K (eds) Dolphin societies: discoveries and puzzles. University of California Press., pp 113–147

    Google Scholar 

  • Fernández R, MacLeod CD, Pierce GJ, Covelo P, López A, Torres-Palenzuela J, Valavanis V, Santos MB (2013) Inter specific and seasonal comparison of the niches occupied by small cetaceans off north-west Iberia. Cont Shelf Res 64:88–98

    Article  Google Scholar 

  • Ford J, Ellis G (2002) Reassessing the social organization of resident killer whales in British Columbia. Proceedings of the 4th International Orca Symposium and Workshop, France

  • Ford J, Ellis G (2006) Selective foraging by fish-eating killer whales Orcinus orca in British Columbia. Mar Ecol-Prog Ser 316:185–199

    Article  Google Scholar 

  • Ford J, Ellis G, Balcomb K (1994) Killer whales: the natural history and genealogy of Orcinus orca in British Columbia and Washington. UBC Press, Vancouver

    Google Scholar 

  • Ford J, Ellis G, Barrett-Lennard L, Morton A, Palm R, Balcomb K III (1998) Dietary specialization in two sympatric populations of killer whales (Orcinus orca) in coastal British Columbia and adjacent waters. Can J Zool 76(1456):1471

    Google Scholar 

  • Ford J, Ellis G, Balcomb K (2000) Killer whales: the natural history and genealogy of Orcinus orca in British Columbia and Washington. UBC Press, Vancouver

    Google Scholar 

  • Ford J, Ellis G, Olesiuk P, Balcomb K (2010) Linking killer whale survival and prey abundance: food limitation in the oceans’ apex predator? Biol Lett 6:139–142

    Article  PubMed  PubMed Central  Google Scholar 

  • Foster E, Franks D, Mazzi S, Darden S, Balcomb K, Ford J, Croft D (2012a) Adaptive prolonged postreproductive life span in killer whales. Science 337:1313

    Article  PubMed  CAS  Google Scholar 

  • Foster E, Franks D, Morrell L, Balcomb K, Parsons K, van Ginneken A, Croft D (2012b) Social network correlates of food availability in an endangered population of killer whales, Orcinus orca. Anim Behav 83:731–736

    Article  Google Scholar 

  • Friedlaender A, Lawson G, Halpin P (2009) Evidence of resource partitioning between humpback and minke whales around the western Antarctic Peninsula. Mar Mamm Sci 25:402–415

    Article  Google Scholar 

  • Grand TC, Dill LM (1999) The effect of group size on the foraging behaviour of coho salmon: reduction of predation or increased competition? Anim Behav 58:443–451

    Article  PubMed  Google Scholar 

  • Guinet C, Domenici P, de Stephanis R, Barrett-Lennard L, Ford JKB, Verborgh P (2007) Killer whale predation on bluefin tuna: exploring the hypothesis of the endurance-exhaustion technique. Mar Ecol-Prog Ser 347:111–119

    Article  Google Scholar 

  • Hedrick A, Temeles E (1989) The evolution of sexual dimorphism in animals: hypotheses and tests. Trends Ecol Evol 4:136–138

    Article  PubMed  CAS  Google Scholar 

  • Hoelzel AR (1993) Foraging behaviour and social group dynamics in Puget Sound killer whales. Anim Behav 45:581–591

    Article  Google Scholar 

  • Højsgaard S, Halekoh U, Yan J (2006) The R package geepack for generalized estimating equations. J Stat Softw 15:1–11

    Google Scholar 

  • Janson CH (1988) Food competition in brown capuchin monkeys (Cebus apella): quantitative effects of group size and tree productivity. Behaviour 105:53–76

    Article  Google Scholar 

  • Jarman P (1974) The social organisation of antelope in relation to their ecology. Behaviour 48:215–267

    Article  Google Scholar 

  • Johnstone R, Cant M (2010) The evolution of menopause in cetaceans and humans: the role of demography. Proc R Soc Lond B 277:3765–3771

    Article  Google Scholar 

  • Kie J, Bowyer R (1999) Sexual segregation in white-tailed deer: density-dependent changes in use of space, habitat selection, and dietary niche. J Mammal 80:1004–1020

    Article  Google Scholar 

  • Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford

    Google Scholar 

  • Le Boeuf B, Crocker D, Costa D, Blackwell S, Webb P, Houser D (2000) Foraging ecology of northern elephant seals. Ecol Monogr 70:353–382

    Article  Google Scholar 

  • Leung E, Chilvers B, Nakagawa S, Moore A, Robertson B (2012) Sexual segregation in juvenile New Zealand sea lion foraging ranges: implications for intraspecific competition, population dynamics and conservation. PLoS One 7, e45389

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lusseau D, Williams R, Wilson B, Grellier K, Barton T, Hammond P, Thompson P (2004) Parallel influence of climate on the behaviour of Pacific killer whales and Atlantic bottlenose dolphins. Ecol Lett 7:1068–1076

    Article  Google Scholar 

  • Lusseau D, Bain DE, Williams R, Smith JC (2009) Vessel traffic disrupts the foraging behavior of southern resident killer whales Orcinus orca. Endanger Species Res 6:211–221

  • Lyrholm T, Leimar O, Johanneson B, Gyllensten U (1999) Sex-biased dispersal in sperm whales: contrasting mitochondrial and nuclear genetic structure of global populations. Proc R Soc Lond B 266:347–354

    Article  CAS  Google Scholar 

  • McCullough DR, Hirth DH, Newhouse SJ (1989) Resource partitioning between sexes in white-tailed deer. J Wildlife Manage 53:277–283

    Article  Google Scholar 

  • McIntyre T, Tosh C, Plötz J, Bornemann H, Bester M (2010) Segregation in a sexually dimorphic mammal: a mixed-effects modelling analysis of diving behaviour in southern elephant seals. Mar Ecol-Prog Ser 412:293–304

    Article  Google Scholar 

  • McNamara J, Mace R, Houston A (1987) Optimal daily routines of singing and foraging in a bird singing to attract a mate. Behav Ecol Sociobiol 20:399–405

    Article  Google Scholar 

  • Miller P, Shapiro A, Deecke V (2010) The diving behaviour of mammal-eating killer whales (Orcinus orca): variations with ecological not physiological factors. Can J Zool 88:1103–1112

    Article  Google Scholar 

  • NMFS (National Marine Fisheries Service) (2008) Recovery plan for southern resident killer whales (Orcinus orca). National Marine Fisheries Service, Northwest Region, Seattle, Washington

    Google Scholar 

  • DFO (Fisheries and Oceans Canada) (2011) Recovery strategy for the northern and southern resident killer whales (Orcinus orca) in Canada. Species at Risk Act Recovery Strategy Series, Fisheries and Oceans Canada, Ottawa, http://www.sararegistry.gc.ca/document/doc1341a/ind_e.cfm

  • Pan W (2001) Akaike’s information criterion in generalized estimating equations. Biometrics 57:120–125

    Article  PubMed  CAS  Google Scholar 

  • Parsons K, Balcomb K, Ford J, Durban J (2009) The social dynamics of southern resident killer whales and conservation implications for this endangered population. Anim Behav 77:963–971

    Article  Google Scholar 

  • Pearson D, Shine R, How R (2002) Sex‐specific niche partitioning and sexual size dimorphism in Australian pythons (Morelia spilota imbricata). Biol J Linn Soc 77:113–125

    Article  Google Scholar 

  • Pitcher TJ, Magurran AE, Winfield IJ (1982) Fish in larger shoals find food faster. Behav Ecol Sociobiol 10:149–151

    Article  Google Scholar 

  • Ralls K, Mesnick S (2002) Sexual dimorphism. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Elsevier, Amsterdam, pp 1071–1078

    Google Scholar 

  • Ruckstuhl K (1999) To synchronise or not to synchronise: a dilemma for young bighorn males? Behaviour 136:805–818

    Article  Google Scholar 

  • Ruckstuhl K (2007) Sexual segregation in vertebrates: proximate and ultimate causes. Integr Comp Biol 47:245–257

    Article  PubMed  CAS  Google Scholar 

  • Rypstra AL, Tirey RS (1991) Prey size, prey perishability and group foraging in a social spider. Oecologia 86:25–30

    Article  Google Scholar 

  • Schreer J, Kovacs K (1997) Allometry of diving capacity in air-breathing vertebrates. Can J Zool 75:339–358

    Article  Google Scholar 

  • Senior P, Butlin RK, Altringham JD (2005) Sex and segregation in temperate bats. Proc R Soc Lond B 272:2467–2473

    Article  Google Scholar 

  • Similä T, Ugarte F (1993) Surface and underwater observations of cooperatively feeding killer whales in northern Norway. Can J Zool 71:1494–1499

    Article  Google Scholar 

  • Slatkin M (1984) Ecological causes of sexual dimorphism. Evolution 38:622–630

    Article  Google Scholar 

  • Staniland I, Robinson S (2008) Segregation between the sexes: Antarctic fur seals, Arctocephalus gazella, foraging at South Georgia. Anim Behav 75:1581–1590

    Article  Google Scholar 

  • Wessel P, Smith W (1996) A global, self‐consistent, hierarchical, high‐resolution shoreline database. J Geophys Res-Sol Ea 101:8741–8743

    Article  Google Scholar 

  • Williams R, Ashe E (2007) Killer whale evasive tactics vary with boat number. J Zool 272:390–397

    Article  Google Scholar 

  • Williams R, Noren D (2009) Swimming speed, respiration rate, and estimated cost of transport in adult killer whales. Mar Mamm Sci 25:327–350

    Article  Google Scholar 

  • Williams R, Bain D, Ford J, Trites A (2002a) Behavioural responses of male killer whales to a ‘leapfrogging’ vessel. J Cetacean Res Manage 4:305–310

    Google Scholar 

  • Williams R, Trites A, Bain D (2002b) Behavioural responses of killer whales (Orcinus orca) to whale-watching boats: opportunistic observations and experimental approaches. J Zool 256:255–270

    Article  Google Scholar 

  • Williams R, Lusseau D, Hammond P (2006) Estimating relative energetic costs of human disturbance to killer whales (Orcinus orca). Biol Conserv 133:301–311

    Article  Google Scholar 

  • Williams R, Krkošek M, Ashe E, Branch TA, Clark S, Hammond PS, Hoyt E, Noren DP, Rosen D, Winship A (2011) Competing conservation objectives for predators and prey: estimating killer whale prey requirements for Chinook salmon. PLoS One 6, e26738

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wrangham RW, Gittleman J, Chapman CA (1993) Constraints on group size in primates and carnivores: population density and day-range as assays of exploitation competition. Behav Ecol Sociobiol 32:199–210

    Article  Google Scholar 

Download references

Acknowledgments

We thank our colleagues at Bion Research and BC Parks for data collection. We thank David Bain, Volker Deecke, John Ford, David Lusseau and Naomi Rose for stimulating discussions on this topic. We thank Doug Sandilands for providing the base map in Fig. 1. We thank the anonymous reviewers and the Editor for their helpful comments and suggestions to improve the quality of the manuscript.

Funding statement

Funding of raw data collection was provided by contracts from BC Parks to Bion Research, Beaveridge Consulting, and Cetus Research and Conservation Society. RW was supported by a Marie Curie International Incoming Fellowship within the Seventh European Community Framework Programme (Project CONCEAL, FP7, PIIF-GA-2009-253407).

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of animals were followed.

Author information

Authors and Affiliations

  1. Sea Mammal Research Unit, Scottish Oceans Institute, University of St. Andrews, St. Andrews, Fife, KY16 8LB, Scotland, UK

    Amber Beerman, Erin Ashe & Rob Williams

  2. Biomathematics and Statistics Scotland, Dundee Unit, Invergowrie, Dundee, DD2 5DA, Scotland, UK

    Katharine Preedy

Authors
  1. Amber Beerman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Erin Ashe
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Katharine Preedy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rob Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Amber Beerman.

Additional information

Communicated by L. Rendell

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

Supplementary material. (DOCX 22 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Beerman, A., Ashe, E., Preedy, K. et al. Sexual segregation when foraging in an extremely social killer whale population. Behav Ecol Sociobiol 70, 189–198 (2016). https://doi.org/10.1007/s00265-015-2038-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-015-2038-2

Keywords

Search

Navigation