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Demographic consequences of fisheries interaction within a killer whale (Orcinus orca) population

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Abstract

Individual heterogeneity in foraging behavior has been widely documented within predator populations. In highly social apex predators such as killer whales (Orcinus orca), specialization may occur at the matriline level. A small population of killer whales has been documented to occur around the Crozet Islands. These whales feed on a wide range of prey items including seals, penguins and large whales, as well as depredate the local Patagonian toothfish (Dissostichus eleginoides) longline fishery. The level of interactions with fisheries varies greatly between matrilines. Here, we present the results on the effects of such behavioral heterogeneity on the demographic trends of this killer whale population. We used photo-identification data from 1977 to 2011 in a mark–recapture framework to test the effect of varying levels of fisheries interactions on adult survival. We documented significant differences in survival between depredating and non-depredating whales, resulting in divergent intra-population demographic trends. These differences showed low survival, and thus a negative effect, for depredating whales when illegal fishing occurred (poachers used lethal methods to deter killer whales from depredating longlines). After illegal fishing stopped (2003–2011), the survival rates of depredating individuals exceeded the survival rates of non-depredating individuals, suggesting a positive influence of “artificial food provisioning”. This effect was further supported by a higher population growth rate for depredating whales. This study highlights the potential demographic costs and benefits that cetaceans face from depredating fisheries and addresses the demographic consequences of both intra-population feeding specialization and the influence of anthropogenic changes in resource availability.

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References

  • Begon M, Townsend CR, Harper JL (2006) Ecology: from individuals to ecosystems. Wiley-Blackwell, Oxford

    Google Scholar 

  • Benton TG, Plaistow SJ, Coulson TN (2006) Complex population dynamics and complex causation: devils, details and demography. Proc R Soc Lond Ser B 273:1173–1181. doi:10.1098/rspb.2006.3495

    Article  Google Scholar 

  • Bigg MA, Olesiuk PF, Ellis GM, Ford JKB, Balcomb KC (1990) Social organization and genealogy of resident killer whales in the coastal waters of British Columbia and Washington State. Rep Int Whal Comm Spec Issue 12:383–405

    Google Scholar 

  • Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28. doi:10.1086/343878

    Article  Google Scholar 

  • Botsford LW, Castilla JC, Peterson CH (1997) The management of fisheries and marine ecosystems. Science 277:509–515. doi:10.1126/science.277.5325.509

    Article  CAS  Google Scholar 

  • Branch TA, Watson R, Fulton EA, Jennings S, McGilliard CR, Pablico GT, Ricard D, Tracey SR (2010) The trophic fingerprint of marine fisheries. Nature 468:431–435. doi:10.1038/nature09528

    Article  CAS  Google Scholar 

  • Brault S, Caswell H (1993) Pod-specific demography of killer whales (Orcinus orca). Ecology 74:1444–1454. doi:10.2307/1940073

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Cairns DK (1987) Seabirds as indicators of marine food supplies. Biol Oceanogr 5:261–271

    Google Scholar 

  • Carothers AD (1973) Capture-recapture methods applied to a population with known parameters. J Anim Ecol 42(1):125–146. doi:10.2307/3408

    Article  Google Scholar 

  • Choquet R, Lebreton JD, Gimenez O, Reboulet AM, Pradel R (2009a) U-CARE: utilities for performing goodness of fit tests and manipulating CApture–REcapture data. Ecography 32:1071–1074

    Article  Google Scholar 

  • Choquet R, Rouan L, Pradel R (2009b) Program E-SURGE: a software application for fitting multievent models. In: Thomson DL, Cooch EG, Conroy MJ (eds) Modeling demographic processes in marked populations. Environmental and ecological statistics. Springer, New York, pp 847–868

    Google Scholar 

  • Clark CW, Yoshimura J (1993) Behavioral responses to variations in population size: a stochastic evolutionary game. Behav Ecol 4:282–288. doi:10.1093/beheco/4.3.282

    Article  Google Scholar 

  • Collins MA, Brickle P, Brown J, Belchier M (2010) The Patagonian toothfish: biology, ecology and fishery. Adv Mar Biol 58:227–300

    Article  Google Scholar 

  • Cormack RM (1964) Estimates of survival from the sighting of marked animals. Biometrika 51:429–438

    Article  Google Scholar 

  • Dahlheim ME, Waite JM (1993) Abundance and distribution of killer whales (Orcinus orca) in Alaska. Annual Report MMPA Assessment Program, Office of Protected Resources, NMFS, NOAA, Silver Spring

  • Dalla Rosa L, Secchi ER (2007) Killer whale (Orcinus orca) interactions with the tuna and swordfish longline fishery off southern and south-eastern Brazil: a comparison with shark interactions. J Mar Biol Assoc UK 87:135–140. doi:10.1017/S0025315407054306

    Article  Google Scholar 

  • Esteban R, Verborgh P, Gauffier P, Giménez J, Guinet C, De Stephanis R (2016a) Dynamics of killer whale, bluefin tuna and human fisheries in the Strait of Gibraltar. Biol Conserv 194:31–38

    Article  Google Scholar 

  • Esteban R, Verborgh P, Gauffier P, Giménez J, Foote AD, de Stephanis R (2016b) Maternal kinship and fisheries interaction influence killer whale social structure. Behav Ecol Sociobiol 70(1):111–122

    Article  Google Scholar 

  • Ford JKB, Ellis GM, Barrett-Lennard LG, Morton AB, Palm RS, Balcomb KC (1998) Dietary specialization in two sympatric populations of killer whales in coastal British Columbia and adjacent waters. Can J Zool 76(8):1456–1471. doi:10.1139/cjz-76-8-1456

    Article  Google Scholar 

  • Ford JKB, Ellis GM, Olesiuk PF, Balcomb KC (2009) Linking killer whale survival and prey abundance: food limitation in the oceans’ apex predator? Biol Lett 6:139–142. doi:10.1098/rsbl.2009.0468

    Article  Google Scholar 

  • Fuller TK, Sievert PR (2001) Carnivore demography and the consequences of changes in prey availability. In: Gittleman JL, Funk SM, Macdonald DW, Wayne RK (eds) Carnivore conservation. Cambridge University Press, Cambridge, pp 163–178

    Google Scholar 

  • Gaillard J-M, Pontier D, Allainé D, Lebreton J-D, Trouvilliez J, Clobert J (1989) An analysis of demographic tactics in birds and mammals. Oikos 56:59–76. doi:10.2307/3566088

    Article  Google Scholar 

  • Gaillard J-M, Festa-Bianchet M, Yoccoz NG (1998) Population dynamics of large herbivores: variable recruitment with constant adult survival. Trends Ecol Evol 13:58–63. doi:10.1016/S0169-5347(97)01237-8

    Article  CAS  Google Scholar 

  • Ganas J, Robbins MM, Nkurunungi JB, Kaplin BA, McNeilage A (2004) Dietary variability of mountain gorillas in Bwindi Impenetrable National Park, Uganda. Int J Primatol 25:1043–1072. doi:10.1023/B:IJOP.0000043351.20129.44

    Article  Google Scholar 

  • Gimenez O, Lebreton J-D, Choquet R (2003) Parameter redundancy in multistate capture-recapture model. Biometrical J 45:704–722. doi:10.1002/bimj.200390043

    Article  Google Scholar 

  • Gowans S, Whitehead H (2001) Photographic identification of northern bottlenose whales (Hyperoodon ampullatus): sources of heterogeneity from natural marks. Mar Mamm Sci 17:76–93. doi:10.1111/j.1748-7692.2001.tb00981.x

    Article  Google Scholar 

  • Grosbois V, Gimenez O, Gaillard JM, Pradel R, Barbraud C, Clobert J, Møller AP, Weimerskirch H (2008) Assessing the impact of climate variation on survival in vertebrate populations. Biol Rev 83:357–399. doi:10.1111/j.1469-185X.2008.00047.x

    Article  CAS  Google Scholar 

  • Guinet C (1991) Intentional stranding apprenticeship and social play in killer whales (Orcinus orca). Can J Zool 69:2712–2716. doi:10.1139/z91-383

    Article  Google Scholar 

  • Guinet C (1992) Predation behavior of killer whales around Crozet Islands. Can J Zool 70:1656–1667

    Article  Google Scholar 

  • Guinet C, Jouventin P, Weimerskirch H (1999) Recent population change of the southern elephant seal at iles Crozet and Iles Kerguelen: the end of the decrease? Antarct Sci 11:193–197. doi:10.1017/S0954102099000255

    Article  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. doi:10.3354/meps07035

    Article  Google Scholar 

  • Guinet C, Tixier P, Gasco N, Duhamel G (2015) 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(5):1587–1597

    Article  Google Scholar 

  • Hofbauer J, Sigmund K (1998) Evolutionary games and population dynamics. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Hucke-Gaete R, Moreno C, Arata J (2004) Operational interactions of sperm whales and killer whales with the Patagonian toothfish industrial fishery off southern Chile. Ccamlr Sci 11:127–140

    Google Scholar 

  • Jolly GM (1965) Explicit estimates from capture-recapture data with both death and immigration-stochastic models. Biometrika 52:225–247

    Article  CAS  Google Scholar 

  • Kendall WL, Nichols JD, Hines JE (1997) Estimating temporary emigration using capture-recapture data with Pollock’s robust design. Ecology 78(2):563–578. doi:10.2307/2265960

    Google Scholar 

  • Kokko H, Sutherland WJ (2001) Ecological traps in changing environments: ecological and evolutionary consequences of a behaviourally mediated Allee effect. Evol Ecol Res 3:537–551

    Google Scholar 

  • Krebs JR, Davies NB (1993) An introduction to behavioural ecology. Blackwell, Cambridge

    Google Scholar 

  • Kuningas S, Similä T, Hammond PS (2013) Population size, survival and reproductive rates of northern Norwegian killer whales (Orcinus orca) in 1986–2003. J Mar Biol Assoc UK 94(06):1277–1291. doi:10.1017/S0025315413000933

    Article  Google Scholar 

  • Lebreton JD, Pradel R (2002) Multistate recapture models: modelling incomplete individual histories. J Appl Stat 29(1–4):353–369. doi:10.1080/02664760120108638

    Article  Google Scholar 

  • Lebreton J-D, Burnham KP, Clobert J, Anderson DR (1992) Modelling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol Monogr 62:67–118. doi:10.2307/2937171

    Article  Google Scholar 

  • Leibold MA (1996) A graphical model of keystone predators in food webs: trophic regulation of abundance, incidence and diversity patterns in communities. Am Nat 147:784–812. doi:10.1086/285879

    Article  Google Scholar 

  • Lewison RL, Crowder LB, Read AJ, Freeman SA (2004) Understanding impacts of fisheries bycatch on marine megafauna. Trends Ecol Evol 19:598–604. doi:10.1016/j.tree.2004.09.004

    Article  Google Scholar 

  • Marcoux M, Whitehead H, Rendell L (2007) Sperm whale feeding variation by location, year, social group and clan: evidence from stable isotopes. Mar Ecol Prog Ser 333:309–314. doi:10.3354/meps333309

    Article  Google Scholar 

  • Matkin CO (1986) Killer whale interactions with the sablefish longline fishery in Prince William Sound, Alaska, 1985, with comments on the Bering Sea. Contract No. 010686. NMFS, NMML, Juneau, Alaska. 10

  • Matkin CO, Matkin DR, Ellis GM, Saulitis E, McSweeney D (1997) Movements of resident killer whales in southeastern Alaska and Prince William Sound, Alaska. Mar Mamm Sci 13:469–475. doi:10.1111/j.1748-7692.1997.tb00653.x

    Article  Google Scholar 

  • Matkin CO, Barrett-Lennard LG, Yurk H, Ellifrit D, Trites AW (2007) Ecotypic variation and predatory behavior among killer whales (Orcinus orca) off the eastern Aleutian Islands, Alaska. Fish Bull 105:74–87

    Google Scholar 

  • Morris WF, Doak DF (2002) Quantitative conservation biology: theory and practice of population viability analysis. Sinauer Associates, Sunderland

    Google Scholar 

  • Myers RA, Worm B (2003) Rapid worldwide depletion of predatory fish communities. Nature 423:280–283. doi:10.1038/nature01610

    Article  CAS  Google Scholar 

  • Nelson LJ, Anderson DR, Burnham KP (1980) The effect of band loss on estimates of annual survival. J Field Ornithol 51(1):30–38

    Google Scholar 

  • Nichols JD (1992) Capture-recapture models. Bioscience 42(2):94–102

    Article  Google Scholar 

  • Nichols JD, Stokes SL, Hines JE, Conroy MJ (1982) Additional comments on the assumption of homogeneous survival rates in modern bird banding estimation models. J Wildl Manag 46(4):953–962. doi:10.2307/3808228

    Article  Google Scholar 

  • Northridge SP (1991) An updated world review of interactions between marine mammals and fisheries. FAO Fisheries Technical Paper 251, Supplement 1. http://www.fao.org/docrep/003/T0452E/T0452E00.HTM. Accessed January 30 2017

  • Northridge SP, Hoffman RJ (1999) Marine mammal interactions with fisheries. In: Twiss JR, Reeves RR (eds) Conservation and management of marine mammals. Smithsonian Institution Press, Washington, pp 99–119

    Google Scholar 

  • O’Donoghue M, Boutin S, Krebs CJ, Hofer EJ (1997) Numerical responses of coyotes and lynx to the snowshoe hare cycle. Oikos 80:150–162. doi:10.2307/3546526

    Article  Google Scholar 

  • Olesiuk P, Bigg M, Ellis G (1990) Life history and population dynamics of resident killer whales (Orcinus orca) in the coastal waters of British Columbia and Washington State. Rep Int Whal Comm 12:209–242

    Google Scholar 

  • Olesiuk PF, Ellis GM, Ford JKB (2005) Life history and population dynamics of northern resident killer whales in British Columbia. Research document 2005/45, Ottawa, Canada: Canadian Science Advisory Secretariat, Fisheries and Oceans Canada. http://www.dfo-po.gc.ca/csas/Csas/Publications/ResDocs-DocRech/2005/2005_045_e.htm. Accessed January 30 2017

  • 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(4):963–971. doi:10.1016/j.anbehav.2009.01.018

    Article  Google Scholar 

  • Pollock KH, Raveling DG (1982) Assumptions of modern band-recovery models, with emphasis on heterogeneous survival rates. J Widl Manag 46(1):88–98. doi:10.2307/3808411

    Google Scholar 

  • Poncelet E, Barbraud C, Guinet C (2010) Population dynamics of killer whales in Crozet Archipelago, southern Indian Ocean: a mark recapture study from 1977 to 2002. J Cetacean Res Manag 11(1):41–48

    Google Scholar 

  • Pradel R (1993) Flexibility in survival analysis from recapture data: handling trap dependence. In: Lebreton J-D, North PM (eds) Marked individuals in the study of bird population. Birkhäuser Velag, Basel, pp 29–37

    Google Scholar 

  • Pruvost P, Duhamel G, Gasco N, Palomares MD (2015) A short history of the fisheries of Crozet islands. FCRR 23(1):31–37

    Google Scholar 

  • Purves MG, Agnew DJ, Balguerias E, Moreno CA, Watkins B (2004) Killer whale (Orcinus orca) and sperm whale (Physeter macrocephalus) interactions with longline vessels in the Patagonian toothfish fishery at South Georgia, South Atlantic. Ccamlr Sci 11:111–126

    Google Scholar 

  • R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Rausher MD (1984) Tradeoffs in performance on different hosts-evidence from within site and between site variation in the beetle Deloyala guttata. Evolution 38:582–595. doi:10.2307/2408708

    Article  Google Scholar 

  • Reisinger RR, Gröcke DR, Lübcker N, McClymont EL, Hoelzel AR, de Bruyn PN (2016) Variation in the diet of killer whales Orcinus orca at Marion Island, Southern Ocean. Mar Ecol Prog Ser 549:263–274

    Article  CAS  Google Scholar 

  • Rendell L, Whitehead H (2001) Culture in whales and dolphins. Behav Brain Sci 24:309. doi:10.1017/S0140525X0100396X

    Article  CAS  Google Scholar 

  • Roche C, Guinet C, Gasco N, Duhamel G (2007) Marine mammals and demersal longlines fishery interactions in Crozet and Kerguelen exclusive economic zones: an assessment of the depredation level. CCAMLR Sci 14:67–82

    Google Scholar 

  • Schakner ZA, Lunsford C, Straley J, Eguchi T, Mesnick SL (2014) Using models of social transmission to examine the spread of longline depredation behavior among sperm whales in the Gulf of Alaska. PLoS One 9:109079. doi:10.1371/journal.pone.0109079

    Article  Google Scholar 

  • Seber GAF (1965) A note on the multiple recapture census. Biometrika 52:249–259

    Article  CAS  Google Scholar 

  • Smout S, Rindorf A, Hammond PS, Harwood J, Matthiopoulos J (2013) Modelling prey consumption and switching by UK grey seals. ICES J Mar Sci 71:81–89. doi:10.1093/icesjms/fst109

    Article  Google Scholar 

  • Stubben CJ, Milligan BG (2007) Estimating and analyzing demographic models using popbio package in R. J Stat Softw 22:11

    Article  Google Scholar 

  • Tixier P (2012) Déprédation par les orques (Orcinus Orca) et les cachalots (Physeter Macrocephalus) sur les palangriers à la legine australe dans la ZEE de l’archipel de Crozet. Dissertation, University of Aix-Marseille II

  • Tixier P, Gasco N, Duhamel G, Guinet C (2010) Interactions of Patagonian toothfish fisheries with killer and sperm whales: an assessment of depredation levels and insights on possible mitigation solutions. CCAMLR Sci 17:179–195

    Google Scholar 

  • Tixier P, Gasco N, Guinet C (2014) Killer whales of the Crozet islands, photo-identification catalogue 2003–2011. Villiers en Bois: Centre d’Etudes Biologiques de Chizé-CNRS. doi:10.6084/m9.figshare.1085960 (accessed January 30 2017)

    Google Scholar 

  • Tixier P, Authier M, Gasco N, Guinet C (2015) Influence of artificial food provisioning from fisheries on killer whales reproductive output. Anim Conserv 18(2):207–208. doi:10.1111/acv.12161

    Article  Google Scholar 

  • Tremblay-Boyer L, Gascuel D, Watson R (2011) Modelling the effects of fishing on the biomass of the world’s oceans from 1950 to 2006. Mar Ecol Prog Ser 442:169–185

    Article  Google Scholar 

  • Trites AW, Christensen V, Pauly D (1997) Competition between fisheries and marine mammals for prey and primary production in the Pacific Ocean. J Northwest Atl Fish Soc 22:173–187

    Article  Google Scholar 

  • Tuck GN, Polacheck T, Croxall JP, Weimerskirch H (2001) Modelling the impact of fishery by-catches on albatross populations. J Appl Ecol 38:1182–1196. doi:10.1046/j.0021-8901.2001.00661.x

    Article  Google Scholar 

  • Turchin P (2003) Complex population dynamics: a theoretical/empirical synthesis. Princeton University Press, Princeton

    Google Scholar 

  • Ward EJ, Holmes EE, Balcomb KC (2009) Quantifying the effects of prey abundance on killer whale reproduction. J Appl Ecol 46:632–640. doi:10.1111/j.1365-2664.2009.01647.x

    Article  Google Scholar 

  • Wauters L, Swinnen C, Dhondt AA (1992) Activity budget and foraging behavior of red squirrels in coniferous and deciduous habitats. J Zool 227:71–86

    Article  Google Scholar 

  • Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst 15:393–425. doi:10.1146/annurev.ecolsys.15.1.393

    Article  Google Scholar 

  • White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:120–138

    Article  Google Scholar 

  • Whitehead H, Rendell L, Osborne RW, Würsig B (2004) Culture and conservation of non-humans with reference to whales and dolphins: review and new directions. Biol Conserv 120(3):427–437. doi:10.1016/j.biocon.2004.03.017

    Article  Google Scholar 

  • Whiten A (2000) Primate culture and social learning. Cognit Sci 24:477–508. doi:10.1016/S0364-0213(00)00027-6

    Article  Google Scholar 

  • Williams R, Lusseau D (2006) A killer whale social network is vulnerable to targeted removals. Biol Lett 2:497–500. doi:10.1098/rsbl.2006.0510

    Article  Google Scholar 

  • Williams BK, Nichols JD, Conroy MJ (2002) Analysis and management of animal populations. Academic Press, San Diego

    Google Scholar 

  • Yano K, Dahlheim ME (1995a) Killer whale, Orcinus orca, depredation on longline catches of bottom fish in the southeastern Bering Sea and adjacent waters. Fish Bull 93:355–372

    Google Scholar 

  • Yano K, Dahlheim ME (1995b) Behavior of killer whales Orcinus orca during longline fishery interactions in the southeastern Bering Sea and adjacent waters. Fish Sci 61:584–589

    Article  CAS  Google Scholar 

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Acknowledgements

This work was conducted as part of the 109 program (Resp. H. Weimerskirch) with the Institut Polaire Français (IPEV). Funding and logistic support was provided by the Terres Australes et Antarctiques Françaises (TAAF), the Réserve Naturelle des Terres Australes and the Reunion Island Fisheries Companies. We are grateful to the Muséum National d’Histoire Naturelle, Paris and especially P. Pruvost, A. Martin and C. Chazeau, for providing data from the “PECHEKER” database. Special thanks to all the photographers and fish observers who helped collect photo-identification images. We are extremely grateful to Dr. Holly Fearnbach for proofreading the manuscript and for her insightful comments. We thank N. G. Yoccoz and O. Gimenez for constructive comments on the methods used in the study. We also thank the reviewers for their insightful comments. The first author was financially supported by the French fishing association (SARPC), the TAAF administration (contract number 782095), and the Secrétariat d’état chargé de l’Outre Mer (contract number 782135).

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The first author was financially supported by the French fishing association (SARPC), the TAAF administration (contract number 782095), and the Secrétariat d’état chargé de l’Outre Mer (contract number 782135).

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Tixier, P., Barbraud, C., Pardo, D. et al. Demographic consequences of fisheries interaction within a killer whale (Orcinus orca) population. Mar Biol 164, 170 (2017). https://doi.org/10.1007/s00227-017-3195-9

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