Abstract
Predators specialising on migratory prey that frequently change migration route face the challenge of finding prey with an unpredictable distribution. Here, we used photo-identification data to investigate whether killer whales observed in herring overwintering and spawning grounds off Iceland follow herring year-round, as previously proposed, and have the ability to adapt to long-term changes in herring distribution. Of 327 identified whales seen more than once, 45% were seen in both grounds, and were thus presumed herring-specialists, likely following herring year-round, while others were only seen on one of the grounds, possibly following herring to unsampled grounds or moving to other locations and exploiting different prey. High seasonal site fidelity to herring grounds, long-term site fidelity to herring spawning grounds, and matches of individual whales between past and recently occupied herring overwintering grounds showed an ability to adapt to long-term changes in prey distribution as well as diversity of movement patterns which are maintained over time, likely as socially-learnt traditions. Such population structuring shows that the movement patterns and foraging ecology of herring-eating killer whales are more complex than previously assumed and must be taken into account in future population assessments. Identifying the factors driving these differences in movements and resource use will be relevant towards our understanding of how prey predictability may drive specialization in this and other top predator species.
Similar content being viewed by others
References
Andrews RD, Pitman RL, Balance 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
Bigg M (1982) An assessment of killer whale (Orcinus orca) stocks off Vancouver Island, British Columbia. Rep Int Whal Comm 32:655–666
Bloch D, Lockyer C (1988) Killer whales (Orcinus orca) in Faroese waters. Rit Fisk 11:55–64
Calambokidis J, Steiger GH, Straley JM, Herman LM, Cerchio S, Salden DR, Urbán JR, Jacobsen JK, von Ziegesar O, Balcomb KC, Gabriele CM, Dahlheim ME, Uchida S, Ellis G, Miyamura Y, de Guevara PLP, Yamaguchi M, Sato F, Mizroch SA, Schlender L, Rasmussen K, Barlow J, Quinn TJ II (2001) Movements and population structure of humpback whales in the North Pacific. Mar Mamm Sci 17:769–794
Corten A (2001) Northern distribution of North Sea herring as a response to high water temperatures and/or low food abundance. Fish Res 50:189–204
Corten A (2002) The role of “conservatism” in herring migrations. Rev Fish Biol Fish 11:339–361
Dahlheim ME, Schulman-Janiger A, Black N, Ternullo R, Ellifrit D, Balcomb KC (2008) Eastern temperate North Pacific offshore killer whales (Orcinus orca): occurrence, movements, and insights into feeding ecology. Mar Mamm Sci 24:719–729
Deecke VB, Nykänen M, Foote AD, Janik VM (2011) Vocal behaviour and feeding ecology of killer whales Orcinus orca around Shetland, UK. Aquat Biol 13:79–88
Dommasnes A, Rey F, Røttingen I (1994) Reduced oxygen concentrations in herring wintering areas. ICES J Mar Sci 51:63–69
Dragesund O, Johannessen A, Ulltang Ø (1997) Variation in migration and abundance of Norwegian spring-spawning herring (Clupea harengus L.). Sarsia 82:97–105
Dufault S, Whitehead H, Dillon M (1999) An examination of the current knowledge on the stock structure of sperm whales (Physeter macrocephalus) worldwide. J Cetacean Res Manage 1:1–10
Durban JW, Pitman RL (2012) Antarctic killer whales make rapid, round-trip movements to subtropical waters: evidence for physiological maintenance migrations? Biol Lett 8:274–277
Eisert R, Ovsyanikova E, Visser I, Ensor P, Currey R, Sharp B (2015) Seasonal site fidelity and movement of type-C killer whales between Antarctica and New Zealand. Rep Int Whal Comm [SC/66a/SM/9]
Esteban R, Verborgh P, Gauffier P, Giménez J, Foote AD, de Stephanis R (2016a) Maternal kinship and fisheries interaction influence killer whale social structure. Behav Ecol Sociobiol 70:111–122
Esteban R, Verborgh P, Gauffier P, Giménez J, Martín V, Pérez-Gil M, Tejedor M, Almunia J, Jepson PD, García-Tiscar S, Barrett-Lennard LG, Guinet C, Foote AD, de Stephanis R (2016b) Using a multi-disciplinary approach to identify a critically endangered killer whale management unit. Ecol Ind 66:291–300
Fearnbach H, Durban JW, Ellifrit DK, Waite JM, Matkin CO, Lunsford CR, Peterson MJ, Barlow J, Wade PR (2014) Spatial and social connectivity of fish-eating “Resident” killer whales (Orcinus orca) in the northern North Pacific. Mar Biol 161:459–472
Fernö A, Pitcher TJ, Melle W, Nøttestad L, Mackinson S, Hollingworth C, Misund OA (1998) The challenge of the herring in the Norwegian Sea: making optimal collective spatial decisions. Sarsia 83:149–167
Foote AD, Similä T, Víkingsson GA, Stevick PT (2010) Movement, site fidelity and connectivity in a top marine predator, the killer whale. Evol Ecol 24:803–814
Ford JKB, Ellis GM, Olesiuk PF, Balcomb KC (2010) Linking killer whale survival and prey abundance: food limitation in the oceans’ apex predator? Biol Lett 6:139–142
Forney KA, Wade P (2006) Worldwide distribution and abundance of killer whales. In: Estes JA, Brownell RL, DeMaster DP, Doak DF, Williams TM (eds) Whales, whaling, and ecosystems. University of California Press, Berkeley, pp 145–162
Friday N, Smith TD, Stevick PT, Allen J (2000) Measurement of photographic quality and individual distinctiveness for the photographic identification of humpback whales, Megaptera novaeangliae. Mar Mamm Sci 16:355–374
Goley PD, Straley JM (1994) Attack on gray whales (Eschrichtius robustus) in Monterey Bay, California, by killer whales (Orcinus orca) previously identified in Glacier Bay, Alaska. Can J Zool 72:1528–1530
Gunnlaugsson T, Sigurjónsson J (1990) NASS-87: estimation of abundance of large cetaceans from observations made onboard Icelandic and Faroese survey vessels. Rep Int Whal Comm 40:571–580
Hauser DDW, Logsdon MG, Holmes EE, VanBlaricom GR, Osborne RW (2007) Summer distribution patterns of southern resident killer whales Orcinus orca: core areas and spatial segregation of social groups. Mar Ecol Prog Ser 351:301–310
Heimlich-Boran JR (1986) Photogrammetric analysis of growth in Puget Sound Orcinus orca. In: Kirkevold BC, Lockard JS (eds) Behavioral biology of killer whales. Alan R Liss, New York, pp 97–111
Holst JC, Røttingen I, Melle W (2004) The herring. In: Skjoldal HR (ed) The Norwegian sea ecosystem. Tapir Academic Press, Trondheim, pp 203–226
Huse G, Fernö A, Holst JC (2010) Establishment of new wintering areas in herring co-occurs with peaks in the ‘first time/repeat spawner’ ratio. Mar Ecol Prog Ser 409:189–198
ICES (International Council for the Exploration of the Sea) (2014) Report of the North-Western Working Group (NWWG), 24 April–1 May 2014. ICES CM 2014/ACOM: 07. ICES Headquarters, Copenhagen
ICES (International Council for the Exploration of the Sea) (2015) Report of the Working Group on Widely Distributed Species (WGWIDE), 25 August–31 August 2015. ICES CM2015/ACOM: 15, Pasaia, Spain
ICES (International Council for the Exploration of the Sea) (2016) Report of the North-Western Working Group (NWWG), 27 April–4 May 2016. ICES CM 2016/ACOM: 08, ICES Headquarters, Copenhagen
Jakobsson J, Stefánsson G (1999) Management of summer-spawning herring off Iceland. ICES J Mar Sci 56:827–833
Jakobsson J, Vilhjálmsson H, Schopka SA (1969) On the biology of the Icelandic herring stocks. Rit Fisk 4:1–16
Jaquet N, Whitehead H (1999) Movements, distribution and feeding success of sperm whales in the Pacific Ocean, over scales of days and tens of kilometers. Aquat Mamm 25:1–13
Kacelnik A, Krebs JR, Bernstein C (1992) The ideal free distribution and predator prey populations. Trends Ecol Evol 7:50–55
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 70:1287–1293
Kuningas S, Similä T, Hammond PS (2014) Population size, survival and reproductive rates of northern Norwegian killer whales (Orcinus orca) in 1986–2003. J Mar Biol Assoc UK 94:1277–1291
Luque PL, Davis CG, Reid DG, Wang J, Pierce GJ (2006) Opportunistic sightings of killer whales from Scottish pelagic trawlers fishing for mackerel and herring off North Scotland (UK) between 2000 and 2006. Aquat Living Resour 19:403–410
Lusseau D, Wilson B, Hammond PS, Grellier K, Durban JW, Parsons KM, Barton TR, Thompson PM (2006) Quantifying the influence of sociality on population structure in bottlenose dolphins. J Anim Ecol 75:14–24
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
Matkin CO, Durban JW, Saulitis EL, Andrews RD, Straley JM, Matkin DR, Ellis GM (2012) Contrasting abundance and residency patterns of two sympatric populations of transient killer whales (Orcinus orca) in the northern Gulf of Alaska. Fish Bull 110:143–155
Matthews CJD, Luque SP, Petersen SD, Andrews RD, Ferguson SH (2011) Satellite tracking of a killer whale (Orcinus orca) in the eastern Canadian Arctic documents ice avoidance and rapid, long-distance movement into the North Atlantic. Polar Biol 34:1091–1096
Musiani M, Leonard JA, Cluff HD, Gates CC, Mariani S, Paquet PC, Vilà C, Wayne RK (2007) Differentiation of tundra/taiga and boreal coniferous forest wolves: genetics, coat colour and association with migratory caribou. Mol Ecol 16:4149–4170
Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315:1846–1850
Nichol LM, Shackleton DM (1996) Seasonal movements and foraging behaviour of northern resident killer whales (Orcinus orca) in relation to the inshore distribution of salmon (Oncorhynchus spp.) in British Columbia. Can J Zool 74:983–991
Óskarsson GJ, Gudmundsdottir A, Sigurdsson T (2009) Variation in spatial distribution and migration of Icelandic summer-spawning herring. ICES J Mar Sci 66:1762–1767
Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915
Sæmundsson B (1939) Mammalia. The Zoology of Iceland, vol IV: 1–37
Samarra FIP, Foote AD (2015) Seasonal movements of killer whales between Iceland and Scotland. Aquat Biol 24:75–79
Samarra FIP, Miller PJO (2015) Prey-induced behavioural plasticity of herring-eating killer whales. Mar Biol 162:809–821
Samarra FIP, Tavares S, Miller PJO, Víkingsson GA (2017a) Killer whales of Iceland 2006–2015. Report of the Marine and Freshwater Research Institute HV 2017-005 (ISSN 2298-9137)
Samarra FIP, Vighi M, Aguilar A, Víkingsson G (2017b) Intra-population variation in isotopic niche in herring-eating killer whales. Mar Ecol Prog Ser 564:199–210
Sigurjónsson J (1984) Killer whale census off Iceland during October 1982. Rep Int Whal Comm 34:609–612
Sigurjónsson J, Gunnlaugsson T (1989) NASS-87: shipboard sightings surveys in Icelandic and adjacent waters June-July 1987. Rep Int Whal Comm 39:392–409
Sigurjónsson J, Lyrholm T, Leatherwood S, Jónsson E, Víkingsson G (1988) Photo-identification of killer whales, Orcinus orca, off Iceland, 1981 through 1986. Rit Fisk 11:99–114
Similä T, Holst JC, Christensen I (1996) Occurrence and diet of killer whales in northern Norway: seasonal patterns relative to the distribution and abundance of Norwegian spring-spawning herring. Can J Fish Aquat Sci 53:769–779
Stenersen J, Similä T (2004) Norwegian killer whales. Tringa forlag, Henningsvær
Stevick PT, Allen J, Clapham PJ, Katona SK, Larsen F, Lien J, Mattila DK, Palsbøll PJ, Sears R, Sigurjónsson J, Smith TD, Víkingsson G, Øien N, Hammond PS (2006) Population spatial structuring on the feeding grounds in North Atlantic humpback whales (Megaptera novaeangliae). J Zool 270:244–255
Sveegaard S, Andreasen H, Mouritsen KN, Jeppesen JP, Teilmann J, Kinze CC (2012) Correlation between the seasonal distribution of harbour porpoises and their prey in the Sound, Baltic Sea. Mar Biol 159:1029–1037
Tavares SB, Samarra FIP, Miller PJO (2017) A multilevel society of herring-eating killer whales indicates adaptation to prey characteristics. Behav Ecol 28:500–514
Toresen R, Østvedt OJ (2000) Variation in abundance of Norwegian spring-spawning herring (Clupea harengus, Clupeidae) throughout the 20th century and the influence of climatic fluctuations. Fish Fish 1:231–256
Valenzuela LO, Sironi M, Rowntree VJ, Seger J (2009) Isotopic and genetic evidence for culturally inherited site fidelity to feeding grounds in southern right whales (Eubalaena australis). Mol Ecol 18:782–791
Víkingsson GA (2004) Háhyrningur. In: Hersteinsson P (ed) Íslensk spendýr. Vaka-Helgafell, Reykjavík, pp 166–171
Vongraven D, Anna B (2014) Prey switching by killer whales in the north-east Atlantic: observational evidence and experimental insights. J Mar Biol Assoc UK 94(6):1357–1365
Ward EJ, Holmes EE, Balcomb KC (2009) Quantifying the effects of prey abundance on killer whale reproduction. J Appl Ecol 46:632–640
Weinrich M, Martin M, Griffiths R, Bove J, Schilling M (1997) A shift in distribution of humpback whales, Megaptera novaeangliae, in response to prey in the southern Gulf of Maine. Fish Bull 95:826–836
Whitehead H (2001) Analysis of animal movement using opportunistic individual identifications: application to sperm whales. Ecology 82:1417–1432
Whitehead H (2003) Sperm whales: social evolution in the ocean. University of Chicago Press, Chicago, p 431
Whitehead H (2007) Selection of models of lagged identification rates and lagged association rates using AIC and QAIC. Commun Stat B Simul 36:1233–1246
Whitehead H (2009) SOCPROG programs: analysing animal social structures. Behav Ecol Sociobiol 63:765–778
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
Acknowledgements
We thank all volunteers, colleagues and students who helped with data collection throughout the many field seasons, Annika Firmenich for help processing the photographic data from 2008, and the Vestmannaeyjar Research Centre, particularly Páll M. Jónsson, for logistical support. We are grateful to Láki Tours, particularly Gísli Ólafsson, for allowing research assistants to join whale-watch trips to collect photo-identification data and sharing sightings information in Grundarfjörður and Kolgrafafjörður. Thanks are also due to Viking Tours and RibSafari for sharing sightings information and allowing us to go onboard to collect data in Vestmannaeyjar. We are grateful to Cathy Harlow and Alexa Kershaw from Discover the World, as well Rob Lott, Baldur Thorvaldsson, Róbert Stefánsson, Stefán Á. Ragnarsson, Vassili Papastavrou, Mike Hatcher, Dave Gibson, Kevin Tappenden, Neil Woodward and other members of the public for kindly providing additional photographs, Malene Simon for providing pictures collected in Vestmannaeyjar during earlier efforts as well as Eyþór Þórðarson, Birgir Stefánsson and Tiu Similä. We thank Dr. Andrew Foote for very helpful guidance on the previously collected data in Iceland, as well as providing useful comments on a previous version of this manuscript. The manuscript furthermore benefited from helpful comments by 3 reviewers. Funding was provided by a Fundação para a Ciência e a Tecnologia doctoral scholarship (Grant No. SFRH/BD/30303/2006), an Icelandic Research Fund (i. Rannsóknasjóður) START Postdoctoral Fellowship (Grant No. 120248042), the National Geographic Society Science and Exploration Europe (Grant No. GEFNE65-12) and a Russell Trust Award (University of St. Andrews) to FIPS, the Office of Naval Research (Grant No. N00014-08-10984) to PJOM, a Fundação para a Ciência e a Tecnologia doctoral scholarship (Grant No. SFRH/BD/84714/2012) to SBT and support from the BBC Natural History Unit and funding from a Full Doctorate Fellowship from CNPq/Capes through the Science Without Borders Program, Marie-Curie Intra-European Fellowship and Research and Scholarship Development Fund (University of Cumbria) to VBD. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible Editor: T. L. Rogers.
Reviewed by J. Towers, B. Hanson and an undisclosed expert.
Rights and permissions
About this article
Cite this article
Samarra, F.I.P., Tavares, S.B., Béesau, J. et al. Movements and site fidelity of killer whales (Orcinus orca) relative to seasonal and long-term shifts in herring (Clupea harengus) distribution. Mar Biol 164, 159 (2017). https://doi.org/10.1007/s00227-017-3187-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-017-3187-9