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Maternal kinship and fisheries interaction influence killer whale social structure

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Abstract

The primary prey of killer whales (Orcinus orca) in the Strait of Gibraltar is the bluefin tuna (Thunnus thynnus). All killer whales observed in this area hunt tuna by chasing individual fish until they become exhausted and can be overcome. However, a subset of pods also interact with a dropline tuna fishery which has developed since 1995. Here, we investigated the social structure within and among social units (pods). Our data suggested that social structure was shaped by maternal kinship, which appears to be a species-specific trait, but also by foraging behavior, which is less common at the intra-population level. At the start of the study, only one cohesive pod interacted with the fishery, which during the course of the study underwent fission into two socially differentiated pods. Social structure within these two fishery-interacting pods was more compact and homogenous with stronger associations between individuals than in the rest of the population. Three other pods were never seen interacting with the fishery, despite one of these pods being regularly sighted in the area of the fishery during the summer. Sociality can influence the spread of the novel foraging behaviors and may drive population fragmentation, which, in this example, is already a critically small community. Observations of social changes in relation to changes in foraging at the earliest stages of diversification in foraging behavior and social segregation may provide insights into the processes that ultimately result in the formation of socially isolated discrete ecotypes in killer whales.

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References

  • Aloncle H (1964) Note sur le thon rouge de la Baie Ibéro-Marocaine. Bull Inst Pêches Marit Maroc 12:43–59

    Google Scholar 

  • Ansmann IC, Parra GJ, Chilvers BL, Lanyon JM (2012) Dolphins restructure social system after reduction of commercial fisheries. Anim Behav 84:575–581

    Article  Google Scholar 

  • Baird RW, Whitehead H (2000) Social organization of mammal-eating killer whales: group stability and dispersal patterns. Can J Zool 78:2096–2105

    Article  Google Scholar 

  • Barthélemy M, Barrat A, Pastor-Satorras R, Verpignani A (2005) Characterization and modeling of weighted networks. Physica 346:34–43

    Article  Google Scholar 

  • Beck S, Kuningas S, Esteban R, Foote AD (2012) The influence of ecology on sociality in the killer whale (Orcinus orca). Behav Ecol 23:246–253

    Article  Google Scholar 

  • Bejder L, Fletcher D, Bräger S (1998) A method for testing association patterns of social animals. Anim Behav 56:719–725

    Article  PubMed  Google Scholar 

  • Bigg MA (1987) Killer whales: a study of their identification, genealogy, and natural history in British Columbia and Washington State. Phantom Press, Nanaimo

    Google Scholar 

  • Bigg MA, Olesiuk PF, Ellis GM et al (1990) Social organization and genealogy of resident killer whales (Orcinus orca) in the coastal waters of British Columbia and Washington State. RIWC 12:383–405

    Google Scholar 

  • Borenstein E, Feldman M, Aoki K (2008) Evolution of learning in fluctuating environments: when selection favors both social and exploratory individual learnings. Evolution 62:586–602

    Article  PubMed  Google Scholar 

  • Boyd R, Richerson P (1985) Culture and the evolutionary process. University of Chicago Press, Chicago

    Google Scholar 

  • Breck SW, Williams CL, Beckmann JP et al (2008) Using genetic relatedness to investigate the development of conflict behavior in black bears. J Mammal 89:428–434

    Article  Google Scholar 

  • Brent LJN, Franks DW, Foster EA et al (2015) Ecological knowledge, leadership, and the evolution of menopause in killer whales. Curr Biol 25:746–750

    Article  PubMed  CAS  Google Scholar 

  • Cairns SJ, Schwager SJ (1987) A comparison of association indices. Anim Behav 35:1454–1469

  • Caro T (1994) Cheetahs of the Serengeti plains: group living in an asocial species. University Press, Chicago

    Google Scholar 

  • Casinos A, Vericad JR (1976) The cetaceans of the Spanish coasts: a survey. Mammalia 40:267–290

    Article  Google Scholar 

  • Cetti F (1777) Storia naturale di Sardegna, III. Anfibi e Pesci. Tip. Giuseppe Piattoli, Cagliari

  • Charif R, Ramey R, Landbauer WI et al (2005) Spatial relationships and matrilineal kinship in African savanna elephant (Loxodonta africana) clans. Behav Ecol 57:327–338

    Article  Google Scholar 

  • Cheney D, Seyfarth R (1990) The representation of social relations by monkeys. Cognition 37:167–196

    Article  PubMed  CAS  Google Scholar 

  • Chilvers BL, Corkeron PJ (2001) Trawling and bottlenose dolphins’ social structure. Proc R Soc Lond B 268:1901–1905

    Article  CAS  Google Scholar 

  • Chiyo PI, Moss CJ, Alberts SC (2012) The influence of life history milestones and association networks on crop-raiding behavior in male African elephants. PLoS One 7:e31382

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Craighead J, Summer J, Mitchell J (1995) The grizzly bears of Yellowstone: their ecology in the Yellowstone ecosystem. Island Press, Washington, DC

    Google Scholar 

  • Croft DP, Madden JR, Franks DW, James R (2011) Hypothesis testing in animal social networks. Trends Ecol Evol 26:502–507

    Article  PubMed  Google Scholar 

  • Csardi G, Nepusz T (2006) The igraph software package for complex network research. Int J Complex Syst 1695:1–9

    Google Scholar 

  • Daura-Jorge FG, Cantor M, Ingram SN et al (2012) The structure of a bottlenose dolphin society is coupled to a unique foraging cooperation with artisanal fishermen. Biol Lett 8:702–705

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • de la Serna JM, de Urbina J (2010) Interacción de la orca (Orcinus orca), con las pesquerías de atún rojo (Thunnus Thynnus) en el área del Estrecho de Gibraltar. Collections Vol Sci Pap ICCAT 65:744–754

    Google Scholar 

  • de la Serna JM, Alot E, Majuelos E, Rioja P (2004) La migración trófica post reproductiva del atún rojo (Thunnus thynnus) a través del estrecho de Gibraltar. Collections Vol Sci Pap ICCAT 56:1196–1209

    Google Scholar 

  • de Stephanis R, Cornulier T, Verborgh P et al (2008) Summer spatial distribution of cetaceans in the Strait of Gibraltar in relation to the oceanographic context. Mar Ecol Prog Ser 353:275–288

    Article  Google Scholar 

  • Dekker D, Krackhardt D, Snijders TAB (2007) Sensitivity of MRQAP tests to collinearity and autocorrelation conditions. Psychometrika 72:563–581

    Article  PubMed  PubMed Central  Google Scholar 

  • Efron B, Gong G (1983) A leisurely look at the bootstrap, the jackknife, and cross-validation. Am Stat 37:36–48

    Google Scholar 

  • Engh A, Esch K, Smale L, Holekamp K (2000) Mechanisms of maternal rank “inheritance” in the spotted hyaena. Anim Behav 60:323–332

    Article  PubMed  Google Scholar 

  • Esteban R, Verborgh P, Gauffier P et al (2013) Identifying key habitat and seasonal patterns of a critically endangered population of killer whales. J Mar Biol Assoc UK 94:1317–1325

    Article  Google Scholar 

  • Farine DR (2013) Animal social network inference and permutations for ecologists in R using asnipe. Methods Ecol Evol 4:1187–1194

    Article  Google Scholar 

  • Felleman F, Heimlich-Boran S, Osborne RW (1998) The feeding ecology of killer whales (Orcinus orca) in the Pacific Northwest. In: Pyor K, Norris K (eds) Dolphin societies: discoveries and puzzles. University of California Press, Berkeley, pp 113–147

    Google Scholar 

  • Finn H, Donaldson R, Calver M (2008) Feeding flipper: a case study of a human dolphin interaction. Pac Conserv Biol 14:215–225

    Google Scholar 

  • Foote AD, Vilstrup JT, de Stephanis R et al (2011) Genetic differentiation among North Atlantic killer whale populations. Mol Ecol 20:629–641

    Article  PubMed  Google Scholar 

  • Ford JKB, Ellis GM, Balcomb KC (1994) Killer whales: the natural history and genealogy of Orcinus orca in the waters of British Columbia and Washington State. UBC Press, Vancouver

    Google Scholar 

  • Foster EA, Franks DW, Morrell LJ et al (2012) Social network correlates of food availability in an endangered population of killer whales, Orcinus orca. Anim Behav 83:731–736

    Article  Google Scholar 

  • Fragaszy D, Perry S, Laland K, Kendal J (2003) What the models say about social learning. In: Fragaszy D, Perry S (eds) The biology of traditions: models and evidence. Cambridge University Press, Cambridge, pp 33–55

    Chapter  Google Scholar 

  • Freeman L (1977) A set of measures of centrality based on betweenness. Sociometry 40:35–41

    Article  Google Scholar 

  • Galef B (1992) The question of animal culture. Hum Nat 3:151–178

    Article  Google Scholar 

  • Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407

    Article  Google Scholar 

  • Ginsberg JR, Young TP (1992) Measuring association between individuals or groups in behavioural studies. Anim Behav 44:377–379

    Article  Google Scholar 

  • Guinet C, Domenici P, de Stephanis R et al (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 

  • Guinet C, Tixier P, Gasco N (2014) Long-term studies of Crozet Island killer whales are fundamental to understanding the economic and demographic consequences of their depredation behaviour on the Patagonian toothfish fishery. ICES J Mar Sci 72:1587–1597

    Article  Google Scholar 

  • Handcock MS, Hunter DR, Butts CT et al (2003) Statnet: software tools for the statistical modeling of network data, version 2. Seattle, WA

  • Harms E (1997) Association patterns and pod cohesion in northern resident killer whales (Orcinus orca). MSc thesis, University of British Columbia, Vancouver

  • Heimlich-Boran S (1986) Cohesive relationships among Puget sound killer whales. In: Kirkevold BC, Lockard JS (eds) Behavioral biology of killer whales. Alan R. Liss, New York, pp 251–284

    Google Scholar 

  • Hockings KJ, Anderson JR, Matsuzawa T (2012) Socioecological adaptations by chimpanzees, Pan troglodytes verus, inhabiting an anthropogenically impacted habitat. Anim Behav 83:801–810

    Article  Google Scholar 

  • Horozco A (1598) Historia de la ciudad de Cádiz. El Excmo. Ayuntamiento de esta M.N.. M. L. y M. H. Ciudad

  • ICCAT (2011) Report of the 2010 ICCAT bluefin tuna stock assessment session. Madrid, Spain

  • ICCAT (2014a) Report of the 2014 ICCAT bluefin tuna stock assessment session. Madrid, Spain

  • ICCAT (2014b) Report of the 2014 Atlantic bluefin tuna stock assessment session. Madrid, Spain

  • Ivkovich T, Filatova OA, Burdin AM et al (2010) The social organization of resident-type killer whales (Orcinus orca) in Avacha Gulf, Northwest Pacific, as revealed through association patterns and acoustic similarity. Mamm Biol 75:198–210

    Google Scholar 

  • Kamada T, Kawai S (1989) An algorithm for drawing general undirected graphs. Inf Process Lett 31:7–15

    Article  Google Scholar 

  • Kappeler PM, Barrett L, Blumstein DT, Clutton-Brock TH (2013) Constraints and flexibility in mammalian social behaviour: introduction and synthesis. Philos Trans Roy Soc B 368:20120337

    Article  Google Scholar 

  • Klopfer P (1961) Observational learning in birds: the establishment of behavioural modes. Behaviour 14:71–80

    Article  Google Scholar 

  • Laland KN, Galef B (2009) The question of animal culture. Harvard Universitiy Press, London

    Google Scholar 

  • Laland KN, Janik VM (2006) The animal cultures debate. Trends Ecol Evol 21:542–547

    Article  PubMed  Google Scholar 

  • Laland KN, O’Brien MJ (2012) Cultural niche construction: an introduction. Biol Theory 6:191–202

    Article  Google Scholar 

  • Lozano F (1958) Los escómbridos de las aguas españolas y marroquíes y su pesca. Trab Inst Esp Ocean 25:254

    Google Scholar 

  • Lusseau D, Newman MEJ (2004) Identifying the role that animals play in their social networks. Proc R Soc Lond B 271:S477–S481

    Article  Google Scholar 

  • Lusseau D, Williams R, Wilson B et al (2004) Parallel influence of climate on the behaviour of Pacific killer whales and Atlantic bottlenose dolphins. Ecol Lett 7:1068–1076

    Article  Google Scholar 

  • Matkin CO, Ellis G, Olesiuk PF, Saulitis E (1999) Association patterns and inferred genealogies of resident killer whales, Orcinus orca, in Prince William Sound, Alaska. Fish Bull 97:900–919

    Google Scholar 

  • Mazur R, Seher V (2008) Socially learned foraging behaviour in wild black bears, Ursus americanus. Anim Behav 75:1503–1508

    Article  Google Scholar 

  • McCarthy T, Seavoy R (1994) Reducing nonsport losses attributable to food conditioning: human and bear behavior modification in an urban environment. Int C Bear 9:75–84

    Google Scholar 

  • McComb K, Moss C, Durant S et al (2001) Matriarchs as repositories of social knowledge in African elephants. Science 292:491–494

    Article  PubMed  CAS  Google Scholar 

  • McGrew W (2004) The cultured chimpanzee: reflections on cultural primatology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Nel J (1999) Social learning in canids: an ecological perspective. In: Box HO, Gibson KR (eds) Mammalian social learning: comparative and ecological perspectives. Cambridge University Press, Cambridge, pp 259–278

    Google Scholar 

  • Newman M (2004) Analysis of weighted networks. Phys Rev E 70:056131

    Article  CAS  Google Scholar 

  • Olesiuk PF, Bigg MA, Ellis G (1990) Life history and population dynamics of northern resident killer whales (Orcinus orca) in British Columbia. RIWC Spec Issue 12:209–244

    Google Scholar 

  • Ottensmeyer CA, Whitehead H (2003) Behavioural evidence for social units in long-finned pilot whales. Can J Zool 81:1327–1338

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

    Article  Google Scholar 

  • Poncelet E, Barbraud C, Guinet C (2010) Population dynamics of killer whales (Orcinus orca) in Crozet Archipelago, southern Indian Ocean: a mark-recapture study from 1977 to 2002. J Cetac Res Manage 11:41–48

    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/

  • Ravier C, Fromentin JMM (2001) Long-term fluctuations in the eastern Atlantic and Mediterranean bluefin tuna population. ICES J Mar Sci 58:1299–1317

    Article  Google Scholar 

  • Riesch R, Barrett-Lennard LG, Ellis GM et al (2012) Cultural traditions and the evolution of reproductive isolation: ecological speciation in killer whales? Biol J Linn Soc 106:1–17

    Article  Google Scholar 

  • Rodríguez-Roda J (1964) Talla, peso y edad de los atunes, Thunnus thynnus (L.), capturados por la almadraba de Barbate (costa sudatlántica de España) en 1963 y comparación con el período 1956 a 1962. Investig Pesq 26:3–48

    Google Scholar 

  • Samuels A, Bejder L (2004) Chronic interaction between humans and free-ranging bottlenose dolphins near Panama City Beach, Florida. J Cetac Res Manage 6:69–77

    Google Scholar 

  • Sargeant BL, Mann J (2009) Developmental evidence for foraging traditions in wild bottlenose dolphins. Anim Behav 78:715–721

    Article  Google Scholar 

  • Schaller G (1972) The Serengeti lion. University of Chicago Press, Chicago

    Google Scholar 

  • Scheel D, Saulitis EVA, Matkin CO (2001) Distribution of killer whale pods in Prince William Sound 1984–1996. Mar Mammal Sci 17:555–569

    Article  Google Scholar 

  • Sella M (1929) Migrazioni e habitat del tonno (Thunnus thynnus L) studiati col metodo degli ami, con osservazioni su l’accrescimento, sul regime delle tonnare ecc. Mem R Com Talassogr Ital 156:511–542

    Google Scholar 

  • Seyfarth R (1980) The distribution of grooming and related behaviours among adult female vervet monkeys. Anim Behav 28:798–813

    Article  Google Scholar 

  • Similä T (1997) Sonar observations of killer whales (Orcinus orca) feeding on herring schools. Aquat Mamm 23:119–126

    Google Scholar 

  • Srour A (1994) Développement de la nouvelle pêcherie artisanale au thon rouge dans la région de Ksar sghir. Note Inf ISPM 26:10–11

    Google Scholar 

  • Sundaresan SR, Fischhoff IR, Dushoff J (2009) Avoiding spurious findings of nonrandom social structure in association data. Anim Behav 77:1381–1385

    Article  Google Scholar 

  • Taniello JFA, Bakker TCM (2015) Minimizing observer bias in behavioral research: blinded methods reporting requirements for Behavioral Ecology and Sociobiology. Behav Ecol Sociobiol 69:1573–1574

    Article  Google Scholar 

  • Taylor NGN, McAllister MMK, Lawson GGL et al (2011) Atlantic bluefin tuna: a novel multistock spatial model for assessing population biomass. PLoS One 6:e27693

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Templeton J, Kamil A, Balda R (1999) Sociality and social learning in two species of corvids. Comput Phsycol 113:450–455

    CAS  Google Scholar 

  • Thornton A, Clutton-Brock T (2011) Social learning and the development of individual and group behaviour in mammal societies. Philos T Roy Soc B 366:978–987

    Article  Google Scholar 

  • Tixier P, Authier M, Gasco N, Guinet C (2014) Influence of artificial food provisioning from fisheries on killer whale reproductive output. Anim Conserv 18:207–218

    Article  Google Scholar 

  • Tosh CA, de Bruyn PJN, Bester MN (2008) Preliminary analysis of the social structure of killer whales, Orcinus orca, at subantarctic Marion Island. Mar Mammal Sci 24:929–940

    Google Scholar 

  • Tregenza T (1995) Building on the ideal free distribution. Adv Ecol Res 26:253–307

    Article  Google Scholar 

  • van der Post D, Hogeweg P (2009) Cultural inheritance and diversification of diet in variable environments. Anim Behav 78:155–166

    Article  Google Scholar 

  • Whitehead H (1995) Investigating structure and temporal scale in social organizations using identified individuals. Behav Ecol 6:199–208

    Article  Google Scholar 

  • Whitehead H (2008) Analysing animal societies. Quantitative methods for vertebrate social analysis. The University of Chicago Press, Chicago

    Book  Google Scholar 

  • Whitehead H (2009) SOCPROG programs: analysing animal social structures. Behav Ecol Sociobiol 63:765–778

    Article  Google Scholar 

  • Whitehead H, Rendell L (2004) Movements, habitat use and feeding success of cultural clans of South Pacific sperm whales. J Anim Ecol 73:190–196

    Article  Google Scholar 

  • Whitehead H, Weilgart L (2000) The sperm whale: social females and roving males. In: Mann J, Connor RC, Tyack P, Whitehead H (eds) Cetacean societies: field studies of dolphins and whales. University of Chicago Press, Chicago, pp 154–172

    Google Scholar 

  • Whiten A, van Schaik CP (2007) The evolution of animal “cultures” and social intelligence. Philos T Roy Soc B 362:603–620

    Article  Google Scholar 

  • Whiten A, Hiden R, Laland K, Stringer C (2011) Culture evolves. Philos T Roy Soc B 3666:938–948

    Article  Google Scholar 

  • Whittaker D, Knight R (1998) Understanding wildlife responses to humans. Wildl Soc B 26:312–317

    Google Scholar 

  • Williams R, Lusseau D (2006) A killer whale social network is vulnerable to targeted removals. Biol Lett 2:497–500

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilson S, Block B (2009) Habitat use in Atlantic bluefin tuna Thunnus thynnus inferred from diving behavior. Endanger Species Res 10:355–367

    Article  Google Scholar 

  • Zhang L, Wang N (2003) An initial study on habitat conservation of Asian elephant (Elephas maximus), with a focus on human elephant conflict in Simao, China. Biol Conserv 112:453–459

    Article  Google Scholar 

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Acknowledgments

We would like to specially thank CIRCE volunteers and research assistants that helped in the field work of CIRCE and EBD-CSIC. This work was funded by Loro Parque Foundation, CEPSA, Ministerio de Medio Ambiente, Fundación Biodiversidad, LIFE+ Indemares (LIFE07NAT/E/000732) and LIFE “Conservación de Cetáceos y tortugas de Murcia y Andalucía” (LIFE02NAT/E/8610), and “Plan Nacional I+D+I ECOCET” (CGL2011-25543) of the Spanish “Ministerio de Economía y Competitividad.” RdS and JG were supported by the Spanish Ministry of Economy and Competitiveness, through the Severo Ochoa Programme for Centres of Excellence in R+D+I (SEV-2012-0262),” and also RdS by the “Subprograma Juan de la Cierva.” Thanks are also due to the IFAW for providing the software Logger 2000. We would also like to thank the referees that have highly improved the quality of this manuscript.

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Authors and Affiliations

  1. CIRCE (Conservation, Information and Research on Cetaceans), C/Cabeza de Manzaneda 3, Algeciras-Pelayo, 11390, Cádiz, Spain

    R. Esteban, P. Verborgh, P. Gauffier & R. de Stephanis

  2. GEMA Grupo de Ecología Marina Aplicada, Estación Biológica de Doñana CSIC, C/Américo Vespucio s/n, Isla de la Cartuja, 41092, Sevilla, Spain

    J. Giménez

  3. Centre for GeoGenetics, The Natural History Museum of Denmark, Øster Voldgade 5-7, 1350, Copenhagen K, Denmark

    A. D. Foote

  4. Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, 752 36, Uppsala, Sweden

    A. D. Foote

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  1. R. Esteban
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  2. P. Verborgh
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  3. P. Gauffier
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Correspondence to R. Esteban.

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The data were collected on wild, free-ranging killer whales. The research team had a special permit from the Spanish Ministry of Environment to approach the whales and enter the restricted area established by the Spanish Royal Decree for protection of cetaceans (R.D. 1727/2007). During the encounters with whales, efforts were made to photograph all members of the group of animals seen during a sighting and avoid disturbance. If whales displayed boat avoidance behavior, encounters were ended.

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Esteban, R., Verborgh, P., Gauffier, P. et al. Maternal kinship and fisheries interaction influence killer whale social structure. Behav Ecol Sociobiol 70, 111–122 (2016). https://doi.org/10.1007/s00265-015-2029-3

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