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Mobbing-like behavior by pilot whales towards killer whales: a response to resource competition or perceived predation risk?

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Abstract

Interspecific interactions can be based on positive or negative outcome. Within antagonist interactions, predation refers to a predator attacking and feeding on a prey while competition is an interaction where individuals compete for a common resource. Worldwide distributions of long-finned pilot whales and killer whales rarely overlap, and they are not known to feed on the same preys. However, in this study, we described the interactions between long-finned pilot whales and killer whales in the Strait of Gibraltar. The former was seen pursuing away the latter in all observations. The main hypotheses for the cause of these interactions are predation or competition. To test both hypotheses, movement patterns and isotopic niches of both species were investigated in the Strait of Gibraltar through satellite tagging and stable isotopes, respectively. Satellite tracks showed no overlap between one tagged pilot whale and one tagged killer whaler’s distributions during 21 days. Similarly, Euclidian distances between centroids of Bayesian standard ellipse areas of carbon and nitrogen stable isotopes were significantly different from zero, showing different isotopic niches for each species. This shows that no competition for the resources should exist between both species in the Strait of Gibraltar and that they do not feed on each other, suggesting that the interactions would not be related to predation. A possible historical presence of marine mammal-eating killer whales in the area, today disappeared, could explain the antipredator defense mobbing-like behavior of pilot whales observed in the Strait.

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References

  • Andrews RD, Pitman RL, Ballance LT (2008) Satellite tracking reveals distinct movement patterns for type B and type C killer whales in the southern Ross Sea, Antarctica. Polar Biol 31:1461–1468. doi:10.1007/s00300-008-0487-z

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Berger J (1999) Anthropogenic extinction of top carnivores and interspecific animal behaviour: implications of the rapid decoupling of a web involving wolves, bears, moose and ravens. Proc R Soc Lond B Biol Sci 266:2261–2267

    Article  CAS  Google Scholar 

  • Berger J, Swenson JE, Persson I-L (2001) Recolonizing carnivores and naive prey: conservation lessons from Pleistocene extinctions. Science 291:1036–1039

    Article  CAS  PubMed  Google Scholar 

  • Best P (1979) Social organization in sperm whales, Physeter macrocephalus. In: Winn HE A (ed) Behavior of marine animals. Current perspectives in research. Springer, New York

    Google Scholar 

  • Bize P, Diaz C, Lindström J (2012) Experimental evidence that adult antipredator behaviour is heritable and not influenced by behavioural copying in a wild bird. Proc R Soc B Biol Sci 279:1380–1388. doi:10.1098/rspb.2011.1789

    Article  Google Scholar 

  • Blumstein DT (2006) The multipredator hypothesis and the evolutionary persistence of antipredator behavior. Ethology 112:209–217. doi:10.1111/j.1439-0310.2006.01209.x

    Article  Google Scholar 

  • Blumstein DT, Daniel JC, Griffin AS, Evans CS (2000) Insular tammar wallabies (Macropus eugenii) respond to visual but not acoustic cues from predators. Behav Ecol 11:528–535

    Article  Google Scholar 

  • Borrell A, Abad-Oliva N, Gómez-Campos E et al (2012) Discrimination of stable isotopes in fin whale tissues and application to diet assessment in cetaceans. Rapid Commun Mass Spectrom 26:1596–1602. doi:10.1002/rcm.6267

    Article  CAS  PubMed  Google Scholar 

  • Brú F (1913) Notas de caza. Imprenta de José Guix, Valencia

    Google Scholar 

  • Burkholder PR (1952) Cooperation and conflict among primitive organisms. Am Sci 40:600–631

    Google Scholar 

  • Cañadas A, Sagarminaga R, García-Tiscar S (2002) Cetacean distribution related with depth and slope in the Mediterranean waters off southern Spain. Deep Sea Res Part Oceanogr Res Pap 49:2053–2073

    Article  Google Scholar 

  • Cañadas A, Sagarminaga R, De Stephanis R et al (2005) Habitat preference modelling as a conservation tool: proposals for marine protected areas for cetaceans in southern Spanish waters. Aquat Conserv Mar Freshw Ecosyst 15:495–521

    Article  Google Scholar 

  • Caut S, Laran S, Garcia-Hartmann E, Das K (2011) Stable isotopes of captive cetaceans (killer whales and bottlenose dolphins). J Exp Biol 214:538–545. doi:10.1242/jeb.045104

    Article  PubMed  Google Scholar 

  • Cheney S, Wragham R (1987) Predation. In: Smuts BB, Cheney RM, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, London, pp 227–239

    Google Scholar 

  • Coss RG (1999) Effects of relaxed natural selection on the evolution of behavior. Geogr Var Behav Perspect Evol Mech 180–208

  • Costa DP, Robinson PW, Arnould JPY et al (2010) Accuracy of ARGOS locations of pinnipeds at-sea estimated using Fastloc GPS. PLoS ONE 5:e8677. doi:10.1371/journal.pone.0008677

    Article  PubMed Central  PubMed  Google Scholar 

  • Curé C, Antunes R, Samarra F et al (2012) Pilot whales attracted to killer whale sounds: acoustically-mediated interspecific interactions in Cetaceans. PLoS ONE 7:e52201. doi:10.1371/journal.pone.0052201

    Article  PubMed Central  PubMed  Google Scholar 

  • Curio E, Ernst U, Vieth W (1978) The adaptive significance of avian mobbing. Z Tierpsychol 48:184–202

    Article  Google Scholar 

  • DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506. doi:10.1016/0016-7037(78)90199-0

    Article  CAS  Google Scholar 

  • De Stephanis R, Cornulier T, Verborgh P et al (2008a) 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 

  • De Stephanis R, García-Tíscar S, Verborgh P et al (2008b) Diet of the social groups of long-finned pilot whales (Globicephala melas) in the Strait of Gibraltar. Mar Biol 154:603–612. doi:10.1007/s00227-008-0953-8

    Article  Google Scholar 

  • De Stephanis R, Verborgh P, Pérez S et al (2008c) Long-term social structure of long-finned pilot whales (Globicephala melas) in the Strait of Gibraltar. Acta Ethol 11:81–94. doi:10.1007/s10211-008-0045-2

    Article  Google Scholar 

  • Diamond JM (1990) Biological effects of ghosts. Nature

  • Esteban R (2008) Abundancia, Estructura social y Parámetros demográficos de la orca (Orcinus orca) en el Estrecho de Gibraltar. Master Thesis. Universidad de Cádiz, Spain

  • 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 U K FirstView:1–9. doi: 10.1017/S002531541300091X

  • FitzGibbon CD (1994) The costs and benefits of predator inspection behaviour in Thomson’s gazelles. Behav Ecol Sociobiol 34:139–148

    Article  Google Scholar 

  • Foote AD, Vilstrup JT, De STEPHANISR et al (2011) Genetic differentiation among North Atlantic killer whale populations. Mol Ecol 20:629–641. doi:10.1111/j.1365-294X.2010.04957.x

    Article  PubMed  Google Scholar 

  • Ford JK, Ellis GM, Barrett-Lennard LG et al (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. doi:10.1139/z98-089

    Article  Google Scholar 

  • Forney KA, Wade P (2007) Worldwide distribution and abundance of killer whales. Whales Whal Ocean Ecosyst 145–162.

  • Freitas C, Lydersen C, Fedak MA, Kovacs KM (2008) A simple new algorithm to filter marine mammal Argos locations. Mar Mamm Sci 24:315–325. doi:10.1111/j.1748-7692.2007.00180.x

    Article  Google Scholar 

  • Garcia-Tiscar S (2009) Interacciones entre delfines mulares (Tursiops truncatus), orcas (Orcinus orca), y pesquerías en el mar de Alborán y Estrecho de Gibraltar, Tesis Doctoral, Universidad Autónoma de Madrid

  • Giménez J, Stephanis RD, Gauffier P et al (2011) Biopsy wound healing in long-finned pilot whales (Globicephala melas). Vet Rec 168:101–101. doi:10.1136/vr.c5284

    Article  Google Scholar 

  • Graham BS, Grubbs D, Holland K, Popp BN (2007) A rapid ontogenetic shift in the diet of juvenile yellowfin tuna from Hawaii. Mar Biol 150:647–658. doi:10.1007/s00227-006-0360-y

    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. Mar Ecol Prog Ser 347:111–119

    Article  Google Scholar 

  • Hodge S, Arthur W, Mitchell P (1996) Effects of temporal priority on interspecific interactions and community development. Oikos 76:350. doi:10.2307/3546207

    Article  Google Scholar 

  • Hutchinson G (1957) Concluding remarks. Cold Spring Harb Symp Quant Biol 22:415–427

    Article  Google Scholar 

  • Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER—stable isotope Bayesian ellipses in R. J Anim Ecol 80:595–602. doi:10.1111/j.1365-2656.2011.01806.x

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Johnson M, Tyack P (2003) A digital acoustic recording tag for measuring the response of wild marine mammals to sound. IEEE J Ocean Eng 28:3–12

    Article  Google Scholar 

  • Jonsen ID, Myers RA, Flemming JM (2003) Meta-analysis of animal movement using state-space models. Ecology 84:3055–3063

    Article  Google Scholar 

  • Jonsen ID, Flemming JM, Myers RA (2005) Robust state-space modeling of animal movement data. Ecology 86:2874–2880

    Article  Google Scholar 

  • Jonsen ID, Basson M, Bestley S et al (2013) State-space models for bio-loggers: a methodological road map. Deep Sea Res Part II Top Stud Oceanogr 88–89:34–46. doi:10.1016/j.dsr2.2012.07.008

    Article  Google Scholar 

  • Kuningas S, Kvadsheim PH, Lam F-PA, Miller PJO (2013) Killer whale presence in relation to naval sonar activity and prey abundance in northern Norway. ICES J Mar Sci J Conserv 70:1287–1293. doi:10.1093/icesjms/fst127

    Article  Google Scholar 

  • Layman CA, Arrington DA, Montaña CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88:42–48. doi:10.1890/0012-9658(2007)88[42:CSIRPF]2.0.CO;2

    Article  PubMed  Google Scholar 

  • Layman CA, Araujo MS, Boucek R et al (2012) Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biol Rev 87:545–562. doi:10.1111/j.1469-185X.2011.00208.x

    Article  PubMed  Google Scholar 

  • Leatherwood JS, Dalheim ME (1978) Worldwide distribution of pilot whales and killer whales. Defense Technical information Center, Ft. Belvoir

  • Magurran AE (1999) The causes and consequences of geographic variation in antipredator behaviour. Geogr Var Behav Perspect Evol Mech 139–163

  • Mossbridge JA, Thomas JA (1999) An “acoustic Niche” for Antarctic killer whale and leopard seal sounds1. Mar Mamm Sci 15:1351–1357. doi:10.1111/j.1748-7692.1999.tb00897.x

    Article  Google Scholar 

  • Notarbartolo Di Sciara G, Birkun A (2010) Conserving whales, dolphins and porpoises in the Mediterranean and Black Seas. ACCOBAMS Status Rep. 2010

  • Notarbartolo-di-Sciara G (1987) Killer Whale, Orcinus Orca, in the Mediterranean Sea. Mar Mamm Sci 3:356–360. doi:10.1111/j.1748-7692.1987.tb00324.x

    Article  Google Scholar 

  • Odum EP (1959) Fundamentals of ecology. Saunders, Philadelphia, 546 pp

    Google Scholar 

  • Olson P, Reilly S (2002) Pilot whales—Globicephala melas and G. macrorhynchus. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic, San Diego, pp 898–903

    Google Scholar 

  • Parnell A, Jackson A (2010) siar: stable isotope analysis in RR package version 4.0. 2

  • Pianka ER (2011) Evolutionary ecology. Harper & Row, New York

    Google Scholar 

  • Pitman RL, Ballance LT, Mesnick SI, Chivers SJ (2001) Killer whale predation on sperm whales: observations and implications. Mar Mamm Sci 17:494–507. doi:10.1111/j.1748-7692.2001.tb01000.x

    Article  Google Scholar 

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

  • Reilly S, Shane S (1986) Pilot whale. In: Haley D (ed) Marine mammals of the eastern North Pacific and Arctic waters. Pacific Search, Seattle, pp 132–139

    Google Scholar 

  • Saayman G, Tayler C (1979) The socioecology of humpback dolphins (Sousa sp.). In: Winn HE A (ed) Behavior of marine animals. Current perspectives in research. Plenum, New York, pp 165–226

    Chapter  Google Scholar 

  • Sanpera C, Aguilar A (1992) Modern whaling off the Iberian Peninsula during the 20th century. Rep Int Whal Commn 42:723–730

    Google Scholar 

  • Saulitis E, Matkin C, Barrett-Lennard L et al (2000) Foraging strategies of sympatric killer whale (Orcinus orca) populations in Prince William Sound, Alaska. Mar Mamm Sci 16:94–109. doi:10.1111/j.1748-7692.2000.tb00906.x

    Article  Google Scholar 

  • Schneider C, Hodges K, Fischer J, Hammerschmidt K (2008) Acoustic niches of Siberut primates. Int J Primatol 29:601–613. doi:10.1007/s10764-007-9181-1

    Article  Google Scholar 

  • Schoener TW (1983) Rate of species turnover decreases from lower to higher organisms: a review of the data. Oikos 41:372. doi:10.2307/3544095

    Article  Google Scholar 

  • Schorr GS, Baird RW, Hanson Mb et al (2009) Movements of satellite-tagged Blainville’s beaked whales off the island of Hawaii. DTIC Document

  • Senigaglia V, de Stephanis R, Verborgh P, Lusseau D (2012) The role of synchronized swimming as affiliative and anti-predatory behavior in long-finned pilot whales. Behav Process 91:8–14. doi:10.1016/j.beproc.2012.04.011

    Article  Google Scholar 

  • Sigurjónsson J, Leatherwood S (1988) The Icelandic live-capture fishery for killer whales, 1976–1988. J Mar Res Inst 11:317

    Google Scholar 

  • Stenersen J, Similä T (2004) Norwegian killer whales. Tringa Forlag, Henningsvær

    Google Scholar 

  • Stockley P, Bro-Jørgensen J (2011) Female competition and its evolutionary consequences in mammals. Biol Rev 86:341–366. doi:10.1111/j.1469-185X.2010.00149.x

    Article  PubMed  Google Scholar 

  • Turner TF, Collyer ML, Krabbenhoft TJ (2010) A general hypothesis-testing framework for stable isotope ratios in ecological studies. Ecology 91:2227–2233

    Article  PubMed  Google Scholar 

  • Verborgh P, De Stephanis R, Pérez S et al (2009) Survival rate, abundance, and residency of long-finned pilot whales in the Strait of Gibraltar. Mar Mamm Sci 25:523–536

    Article  Google Scholar 

  • Whitehead H (1998) Cultural selection and genetic diversity in matrilineal whales. Science 282:1708–1711

    Google Scholar 

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Acknowledgments

This study was sponsored by Loro Parque Foundation, Fundación Biodiversidad, CEPSA, EcoCet Project (CGL2011-25543, Plan Nacional de investigación del Ministerio de Economía y Competitividad). Renaud de Stephanis and Joan Giménez 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 by the “Subprograma Juan de la Cierva.” Thanks are given to Russ Andrews for all the assesment regarding the Satellite tag deployements and to the IFAW for providing the software Logger 2000. Great thanks are given to all the people who helped in the field (CIRCE’s volunteers) and the lab (both in the EBD-CSIC and the UAM), especially to Juan Manuel Salazar Sierra, Carolina Jiménez, David Alarcón, Susana Carrasco, and Ricardo Álvarez. Andy Foote, Tiu Similä, and Francisco Ramirez provided interesting comments on the manuscript. Further, on behalf of Mikkel-Holger Strander Sinding, we would like to give sincere thanks to the owners of HG 333 Isafold, as well as to Captain Karsten Mølgård and the crew aboard the ship allowing Mikkel-Holger to accompany them during their fisheries. Thanks to Sarah Young for the English review.

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Authors and Affiliations

  1. Grupo de Ecología Marina Aplicada (GEMA), Estación Biológica de Doñana (CSIC), C/Americo Vespucio, s/n, 41092, Isla de la Cartuja, Sevilla, Spain

    R. De Stephanis & J. Giménez

  2. CIRCE (Conservation, Information and Research on Cetaceans), Cabeza de Manzaneda 3, Pelayo, 11390, Algeciras, Cadiz, Spain

    R. Esteban, P. Gauffier & P. Verborgh

  3. Department of Ecology, Universidad Autónoma de Madrid, Madrid, Spain

    S. García-Tiscar

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

    M-H. S. Sinding

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  1. R. De Stephanis
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  2. J. Giménez
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  3. R. Esteban
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  4. P. Gauffier
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  5. S. García-Tiscar
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  6. M-H. S. Sinding
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Correspondence to R. De Stephanis.

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De Stephanis, R., Giménez, J., Esteban, R. et al. Mobbing-like behavior by pilot whales towards killer whales: a response to resource competition or perceived predation risk?. acta ethol 18, 69–78 (2015). https://doi.org/10.1007/s10211-014-0189-1

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