Abstract
Toothed whales (odontocetes) feeding on fish caught on hooks in longline fisheries is a growing issue worldwide. The substantial impacts that this behaviour, called depredation, can have on the fishing economy, fish stocks and odontocetes populations, raise a critical need for mitigation solutions to be developed. However, information on when, where and how odontocete depredation occurs underwater is still limited, especially in demersal longline fisheries (fishing gear set on the seafloor). In the present study, we investigated depredation by killer whales (Orcinus orca) and sperm whales (Physeter macrocephalus) on demersal longlines in the French Patagonian toothfish fishery (Southern Ocean). Using a combination of animal-borne behavioural and longline-attached data loggers, we demonstrated that both species are able to depredate longlines on the seafloor. This study, therefore, suggests that odontocetes whales–longline interaction events at depth may be unrecorded when assessing depredation rates from surface observations during hauling phases only. This result has implications for the management of fisheries facing similar depredation issues as underestimated depredation rates may result in unaccounted fish mortality in fish-stock assessments. Therefore, while further research should be conducted to assess the extent of deep-sea whale–longline interaction events during soaking, the evidence that depredation can occur at any time during the whole fishing process as brought out by this study should be considered in future developments of mitigation solutions to the issue.
Similar content being viewed by others
References
Arangio, R. 2012. Minimising whale depredation on longline fishing. Australian Government-Fisheries Research and Development Corporation.
Barrett-Lennard, L.G., J.K. Ford, and K.A. Heise. 1996. The mixed blessing of echolocation: differences in sonar use by fish-eating and mammal-eating killer whales. Animal Behaviour 51: 553–565.
Bavouzet, G., F. Morandeau, M. Mouchel, S. Méhault, G. Duhamel, C. Guinet, J. Roullot, J.-P. Kinoo, et al. 2011. Rapport de la campagne casier Orcasav: Une campagne innovante de pêche aux casiers dans la ZEE de Crozet pour lutter contre la déprédation des orques et la mortalité aviaire.
Boyd, I.L. 2002. Integrated environment-prey-predator interactions off South Georgia: Implications for management of fisheries. Aquatic Conservation: Marine and Freshwater Ecosystems 12: 119–126. https://doi.org/10.1002/aqc.481.
Collins, M.A., P. Brickle, J. Brown, and M. Belchier. 2010. Chapter four—The patagonian toothfish: Biology, ecology and fishery. In Advances in marine biology, vol. 58, ed. M. Lesser, 227–300. New York: Academic Press.
Colto. 2016. TAC under MSC full assessmnet.
Dalla Rosa, L., and E.R. Secchi. 2007. Killer whale (Orcinus orca) interactions with the tuna and swordfish longline fishery off southern and south-eastern Brazil: A comparison with shark interactions. Journal of the Marine Biological Association of the United Kingdom 87: 135–140. https://doi.org/10.1017/s0025315407054306.
Donoghue, M., R. Reeves, and G.S. Stone. 2002. Report of the workshop on interactions between cetaceans and longline fisheries, Apia. Samoa. In: New England Aquarium Press.
Fais, A., N. Aguilar Soto, M. Johnson, C. Pérez-González, P.J.O. Miller, and P.T. Madsen. 2015. Sperm whale echolocation behaviour reveals a directed, prior-based search strategy informed by prey distribution. Behavioral Ecology and Sociobiology 69: 663–674. https://doi.org/10.1007/s00265-015-1877-1.
Forney, K.A., D.R. Kobayashi, D.W. Johnston, J.A. Marchetti, and M.G. Marsik. 2011. What’s the catch? Patterns of cetacean bycatch and depredation in Hawaii-based pelagic longline fisheries: Patterns of cetacean bycatch and depredation in Hawaii. Marine Ecology 32: 380–391. https://doi.org/10.1111/j.1439-0485.2011.00454.x.
Gasco, N. 2011. Contributions to marine science by fishery observers in the French EEZ of Kerguelen. by fishery observers in the French EEZ of Kerguelen. In Proceedings of the 1st international Science Symposium on the Kerguelen Plateau (Concarneau, 2010). The Kerguelen Plateau, Marine Ecosystem and Fisheries.
Gasco, N. 2013. Déprédation de la légine (Dissostichus eleginoides) par les orques (Orcinus orca), les cachalots (Physeter macrocephalus) et les otaries (Arctocephalus spp.) à Kerguelen et Crozet (Océan indien sud). Conséquences sur la gestion de la pêcherie et évaluation de solutions. Diplôme de l’Ecole Pratique des Hautes Etudes.
Gasco, N., P. Tixier, G. Duhamel, and C. Guinet. 2015. Comparison of two methods to assess fish losses due to depredation by killer whales and sperm whales on demersal longlines. CCAMLR Science 22: 1–14.
Gilman, E., N. Brothers, G. McPherson, and P. Dalzel. 2006. A review of cetacean interactions with longline gear. Journal of Cetacean Research and Management 8: 215–223.
Grilly, E., K. Reid, S. Lenel, and J. Jabour. 2015. The price of fish: A global trade analysis of Patagonian (Dissostichus eleginoides) and Antarctic toothfish (Dissostichus mawsoni)☆. Marine Policy 60: 186–196. https://doi.org/10.1016/j.marpol.2015.06.006.
Guénette, S., S.J. Heymans, V. Christensen, and A.W. Trites. 2006. Ecosystem models show combined effects of fishing, predation, competition, and ocean productivity on Steller sea lions (Eumetopias jubatus) in Alaska. Canadian Journal of Fisheries and Aquatic Sciences 63: 2495–2517. https://doi.org/10.1139/f06-136.
Guerra, M., L. Hickmott, J. van der Hoop, W. Rayment, E. Leunissen, E. Slooten, and M. Moore. 2017. Diverse foraging strategies by a marine top predator: Sperm whales exploit pelagic and demersal habitats in the Kaikōura submarine canyon. Deep Sea Research Part I: Oceanographic Research Papers 128: 98–108. https://doi.org/10.1016/j.dsr.2017.08.012.
Guinet, C., P. Tixier, N. Gasco, and G. Duhamel. 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 Journal of Marine Science 72: 1587–1597. https://doi.org/10.1093/icesjms/fsu221.
Hamer, D.J., S.J. Childerhouse, and N.J. Gales. 2012. Odontocete bycatch and depredation in longline fisheries: A review of available literature and of potential solutions. Marine Mammal Science 28: E345–E374.
Hucke-Gaete, R., C.A. Moreno, J. Arata, and B.W. Ctr. 2004. Operational interactions of sperm whales and killer whales with the Patagonian toothfish industrial fishery off southern Chile. Ccamlr Science 11: 127–140.
Janc, A., G. Richard, C. Guinet, J.P.Y. Arnould, M.C. Villanueva, G. Duhamel, N. Gasco, and P. Tixier. 2018. How do fishing practices influence sperm whale (Physeter macrocephalus) depredation on demersal longline fisheries? Fisheries Research 206: 14–26. https://doi.org/10.1016/j.fishres.2018.04.019.
Labadie, G., P. Tixier, C. Barbraud, R. Fay, N. Gasco, G. Duhamel, and C. Guinet. 2018. First demographic insights on historically harvested and poorly known male sperm whale populations off the Crozet and Kerguelen Islands (Southern Ocean). Marine Mammal Science. 34: 595–615. https://doi.org/10.1111/mms.12469.
Madsen, P.T., M. Wahlberg, and B. Møhl. 2002. Male sperm whale (Physeter macrocephalus) acoustics in a high-latitude habitat: Implications for echolocation and communication. Behavioral Ecology and Sociobiology 53: 31–41. https://doi.org/10.1007/s00265-002-0548-1.
Martin, A., and P. Pruvost. 2007. Pecheker, relational database for analysis and management of fisheries and related biological data from the French Southern Ocean fisheries monitoring scientific programs. Muséum National d’Histoire Naturelle.
Mathias, D., A. Thode, J. Straley, and K. Folkert. 2009. Relationship between sperm whale (Physeter macrocephalus) click structure and size derived from videocamera images of a depredating whale (sperm whale prey acquisition). The Journal of the Acoustical Society of America 125: 3444. https://doi.org/10.1121/1.3097758.
Mathias, D., A.M. Thode, J. Straley, J. Calambokidis, G.S. Schorr, and K. Folkert. 2012. Acoustic and diving behavior of sperm whales (Physeter macrocephalus) during natural and depredation foraging in the Gulf of Alaska. The Journal of the Acoustical Society of America 132: 518–532.
McGill, R., J.W. Tukey, and W.A. Larsen. 1978. Variations of box plots. The American Statistician 32: 12. https://doi.org/10.2307/2683468.
Miller, P.J.O., M.P. Johnson, and P.L. Tyack. 2004. Sperm whale behaviour indicates the use of echolocation click buzzes “creaks” in prey capture. Proceedings of the Royal Society B: Biological Sciences 271: 2239–2247. https://doi.org/10.1098/rspb.2004.2863.
Moreno, C.A., R. Castro, L.J. Mújica, and P. Reyes. 2008. Significant conservation benefits obtained from the use of a new fishing gear in the Chilean Patagonian toothfish fishery. Ccamlr Science 15: 79–91.
Morissette, L., V. Christensen, and D. Pauly. 2012. Marine mammal impacts in exploited ecosystems: Would large scale culling benefit fisheries? Edited by Steven J. Bograd. PLoS ONE 7: e43966. https://doi.org/10.1371/journal.pone.0043966.
Norris, K.S. 1968. The echolocation of marine mammals, 391–423. HT Andersen: In The Biology of Marine Mammals.
Northridge, S. 1991. An updated world review of interactions between marine mammals and fisheries.
Northridge, S. P., and R. J. Hofman. 1999. Marine mammal interactions with fisheries. Conservation and Management of Marine Mammals: 99–119.
Passadore, C., A. Domingo, and E.R. Secchi. 2015. Depredation by killer whale (Orcinus orca) and false killer whale (Pseudorca crassidens) on the catch of the Uruguayan pelagic longline fishery in Southwestern Atlantic Ocean. ICES Journal of Marine Science 72: 1653–1666. https://doi.org/10.1093/icesjms/fsu251.
Peterson, M.J., and C. Carothers. 2013. Whale interactions with Alaskan sablefish and Pacific halibut fisheries: Surveying fishermen perception, changing fishing practices and mitigation. Marine Policy 42: 315–324.
Peterson, M.J., and D. Hanselman. 2017. Sablefish mortality associated with whale depredation in Alaska. ICES Journal of Marine Science 74: 1382–1394. https://doi.org/10.1093/icesjms/fsw239.
Peterson, M.J., F. Mueter, K. Criddle, and A.C. Haynie. 2014. Killer whale depredation and associated costs to Alaskan Sablefish, Pacific Halibut and Greenland Turbot Longliners. Edited by Daniel E. Duplisea. PLoS ONE 9: e88906. https://doi.org/10.1371/journal.pone.0088906.
Poncelet, E., C. Barbraud, and C. Guinet. 2009. Population dynamics of killer whales (Orcinus orca) in Crozet Archipelago, southern Indian Ocean: A mark recapture study from 1977 to 2002. Journal of Cetacean Research and Management 11: 41–50.
Purves, M.G., D.J. Agnew, E. Balguerias, C.A. Moreno, and B. Watkins. 2004. Killer whale (Orcinus orca) and sperm whale (Physeter macrocephalus) interactions with longline vessels in the Patagonian toothfish fishery at South Georgia, 11. Ccamlr Science: South Atlantic.
R Development Core Team. 2015. R: A language and environment for statistical computing. (version R version 3.2.3).
Rabearisoa, N., P. Bach, P. Tixier, and C. Guinet. 2012. Pelagic longline fishing trials to shape a mitigation device of the depredation by toothed whales. Journal of Experimental Marine Biology and Ecology 432–433: 55–63. https://doi.org/10.1016/j.jembe.2012.07.004.
Read, A.J. 2008. The looming crisis: Interactions between marine mammals and fisheries. Journal of Mammalogy 89: 541–548. https://doi.org/10.1644/07-mamm-s-315r1.1.
Read, A.J., P. Drinker, and S. Northridge. 2006. Bycatch of marine mammals in U.S. and global fisheries: Bycatch of marine mammals. Conservation Biology 20: 163–169. https://doi.org/10.1111/j.1523-1739.2006.00338.x.
Reisinger, R.R., M. Keith, R.D. Andrews, and P.J.N. de Bruyn. 2015. Movement and diving of killer whales (Orcinus orca) at a Southern Ocean archipelago. Journal of Experimental Marine Biology and Ecology 473: 90–102. https://doi.org/10.1016/j.jembe.2015.08.008.
Roche, C., C. Guinet, N. Gasco, and G. Duhamel. 2007. Marine mammals and demersal longline fishery interactions in Crozet and Kerguelen Exclusive Economic Zones: An assessment of depredation levels. CCAMLR Science 14: 67–82.
Söffker, M., P. Trathan, J. Clark, M.A. Collins, M. Belchier, and R. Scott. 2015. The impact of predation by marine mammals on Patagonian toothfish longline fisheries. Edited by Grant Ballard. PLOS ONE 10: e0118113. https://doi.org/10.1371/journal.pone.0118113.
Straley, J., V. O’Connell, J. Liddle, A. Thode, L. Wild, L. Behnken, D. Falvey, and C. Lunsford. 2015. Southeast alaska sperm whale avoidance project (SEASWAP): A successful collaboration among scientists and industry to study depredation in Alaskan waters. ICES Journal of Marine Science: Journal du Conseil 72: 1598–1609. https://doi.org/10.1093/icesjms/fsv090.
Sullivan, S. 2015. North Pacific Fishery Management Council: 5.
Teloni, V., J.P. Mark, M.J.O. Patrick, and M.T. Peter. 2008. Shallow food for deep divers: Dynamic foraging behavior of male sperm whales in a high latitude habitat. Journal of Experimental Marine Biology and Ecology 354: 119–131. https://doi.org/10.1016/j.jembe.2007.10.010.
Thode, A., L. Wild, J. Straley, D. Barnes, A. Bayless, V. O’Connell, E. Oleson, J. Sarkar, et al. 2016. Using line acceleration to measure false killer whale (Pseudorca crassidens) click and whistle source levels during pelagic longline depredation. The Journal of the Acoustical Society of America 140: 3941–3951.
Thode, A.M., L. Wild, D. Mathias, J. Straley, and C. Lunsford. 2014. A comparison of acoustic and visual metrics of sperm whale longline depredation. The Journal of the Acoustical Society of America 135: 3086–3100.
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. Aix-Marseille.
Tixier, P., N. Gasco, G. Duhamel, M. Viviant, M. Authier, and C. Guinet. 2010. Interactions of Patagonian toothfish fisheries with killer and sperm whales in the Crozet islands Exclusive Economic Zone: An assessment of depredation levels and insights on possible mitigation strategies. CCAMLR Science 17: 179–195.
Tixier, P., N. Gasco, G. Duhamel, and C. Guinet. 2015a. Habituation to an acoustic harassment device (AHD) by killer whales depredating demersal longlines. ICES Journal of Marine Science 72: 1673–1681. https://doi.org/10.1093/icesjms/fsu166.
Tixier, P., M. Authier, N. Gasco, and C. Guinet. 2015b. Influence of artificial food provisioning from fisheries on killer whale reproductive output: Artificial food provisioning and killer whale reproduction. Animal Conservation 18: 207–218. https://doi.org/10.1111/acv.12161.
Tixier, P., J. Vacquie Garcia, N. Gasco, G. Duhamel, and C. Guinet. 2015c. Mitigating killer whale depredation on demersal longline fisheries by changing fishing practices. ICES Journal of Marine Science 72: 1610–1620. https://doi.org/10.1093/icesjms/fsu137.
Tixier, P., C. Barbraud, D. Pardo, N. Gasco, G. Duhamel, and C. Guinet. 2017. Demographic consequences of fisheries interaction within a killer whale (Orcinus orca) population. Marine Biology 164: 170. https://doi.org/10.1007/s00227-017-3195-9.
Tixier, P., P. Burch, G. Richard, K. Olsson, D. Welsford, M.-A. Lea, M.A. Hindell, C. Guinet, et al. 2019a. Commercial fishing patterns influence odontocete whale-longline interactions in the Southern Ocean. Scientific Reports 9: 1904. https://doi.org/10.1038/s41598-018-36389-x.
Tixier, P., J. Giménez, R. Reisinger, P. Méndez-Fernandez, J.P.-Y. Arnould, Y. Cherel, and C. Guinet. 2019b. Importance of toothfish in the diet of generalist subantarctic killer whales: Implications for fisheries interactions. Marine Ecology Progress Series 613: 197–210. https://doi.org/10.3354/meps12894.
Towers, J.R., P. Tixier, K.A. Ross, J. Bennett, J.P.Y. Arnould, R.L. Pitman, and J.W. Durban. 2019. Movements and dive behaviour of a toothfish-depredating killer and sperm whale. ICES Journal of Marine Science 76: 298–311. https://doi.org/10.1093/icesjms/fsy118.
Trites, A.W., V. Christensen, and D. Pauly. 1997. Competition between fisheries and marine mammals for prey and primary production in the Pacific Ocean. Journal of Northwest Atlantic Fishery Science. 22: 173–187.
Van den Hoff, J., R. Kilpatrick, and D. Welsford. 2017. Southern elephant seals (Mirounga leonina Linn.) depredate toothfish longlines in the midnight zone. PLOS ONE 12: e0172396. https://doi.org/10.1371/journal.pone.0172396.
Watwood, S.L., P.J.O. Miller, M. Johnson, P.T. Madsen, and P.L. Tyack. 2006. Deep-diving foraging behaviour of sperm whales (Physeter macrocephalus). Journal of Animal Ecology 75: 814–825. https://doi.org/10.1111/j.1365-2656.2006.01101.x.
Weimerskirch, H., D. Capdeville, and G. Duhamel. 2000. Factors affecting the number and mortality of seabirds attending trawlers and long-liners in the Kerguelen area. Polar Biology 23: 236–249. https://doi.org/10.1007/s003000050440.
Werner, T.B., S. Northridge, K.M. Press, and N. Young. 2015. Mitigating bycatch and depredation of marine mammals in longline fisheries. ICES Journal of Marine Science 72: 1576–1586. https://doi.org/10.1093/icesjms/fsv092.
Whitehead, H. 2009. Sperm Whale. In Encyclopedia of marine mammals, 1091–1097 pp. Elsevier. https://doi.org/10.1016/b978-0-12-373553-9.00248-0.
Zimmer, W.M.X. 2011. Passive acoustic monitoring of cetaceans. Cambridge: Cambridge University Press.
Acknowledgements
We are particularly grateful to the captains and their crew of the Mascareignes 3, the Ile de La Réunion and the Albius for their assistance in the field. We thank Dominique Filipi for providing the accelerometer and for his help with the devices. We are also grateful to fishery observers operating from the vessel and especially to Gabriel Devique for sharing his picture of the dead sperm whale. We thank also the Museum National d’Histoire Naturelle de Paris for providing access to the PechKer Database. This study was part of the OrcaDepred program supported by the ANR, the Fondation d’Entreprise des Mers australes, the Syndicat des Armements Réunionais des Palangriers Congélateurs, fishing companies, the Direction des Pêche Maritimes et de l’Aquaculture, Terres Australes et Antarctiques Françaises (the Natural Reserve and Fishery units) and the Australian Research Council grant. The first author was financially supported by a departmental and regional grant (Deux-Sèvres and Poitou–Charentes).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Richard, G., Bonnel, J., Tixier, P. et al. Evidence of deep-sea interactions between toothed whales and longlines. Ambio 49, 173–186 (2020). https://doi.org/10.1007/s13280-019-01182-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13280-019-01182-1