Abstract
Antarctic minke whales Balaenoptera bonaerensis are rorquals that migrate to Antarctic waters to forage during the austral summer. Because the species frequents the edges of ice packs in summer, the potential impact of long-term physical environmental changes poses serious conservation concerns. Condition along the ice edge vary regionally, sometimes forming small ice free areas (ice gaps), and little is known about whale movement patterns associated with these small-scale variations in the physical environment. In this study, six minke whales were tracked for an average of 31 days (range 4–77 days) from January to March of 2016 and 2017 between 60° E and 140° E above and off the continental shelf. The tracking data of five animals were fitted to a Bayesian hierarchical switching state-space model assembled from ARGOS data filters to estimate behavioral states. Results show that Antarctic minke whales are likely to search for ice gaps areas and remain there for extended periods until the surrounding ice melts, rather than stay at krill rich shelf breaks or areas with high chlorophyll-a concentration. When no ice gaps were nearby, the whales were likely to move eastward along highly concentrated ice packs to find a gap. Our study found a strong association between minke whale movements and ice dynamics during the summer foraging season in this region.
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References
Abe H, Goto M, Pastene LA et al (2001) Practical use of multiplex fluorescent PCR for cetacean sex identification. Mar Mammal Sci 17:657–664. https://doi.org/10.1111/j.1748-7692.2001.tb01011.x
Ainley DG, David Hyrenbach K (2010) Top-down and bottom-up factors affecting seabird population trends in the California current system (1985–2006). Prog Oceanogr 84:242–254. https://doi.org/10.1016/j.pocean.2009.10.001
Ainley DG, Dugger KM, Toniolo V, Gaffney I (2007) Cetacean occurrence patterns in the Amundsen and southern Bellingshausen sea sector, southern ocean. Mar Mammal Sci 23:287–305. https://doi.org/10.1111/j.1748-7692.2007.00109.x
Ainley DG, Jongsomjit D, Ballard G et al (2011) Modeling the relationship of Antarctic minke whales to major ocean boundaries. Polar Biol 35:281–290. https://doi.org/10.1007/s00300-011-1075-1
Amante C, Eakins B (2009) ETOPO1 1 Arc-Minute Global Relief Model: Procedures, Data Sources and Analysis. NOAA Tech Memo NESDIS NGDC-24 Natl Geophys Data Center, NOAA. doi: 10.7289/V5C8276M
Armstrong AJ, Siegfried WR (1991) Consumption of Antarctic krill by minke whales (Balaenoptera acutorostrata). Antarct Sci 3(1):13–18
Atkinson A, Siegel V, Pakhomov E, Rothery P (2004) Long-term decline in krill stock and increase in salps within the Southern Ocean. Nat Int Wkly J Sci 432:100–103. https://doi.org/10.1038/nature02950.1
Atkinson A, Siegel V, Pakhomov EA et al (2009) A re-appraisal of the total biomass and annual production of Antarctic krill. Deep Sea Res Part I Oceanogr Res Pap 56:727–740. https://doi.org/10.1016/j.dsr.2008.12.007
Bailey H, Mate BR, Palacios DM et al (2010) Behavioural estimation of blue whale movements in the Northeast Pacific from state-space model analysis of satellite tracks. Endanger Species Res 10:93–106. https://doi.org/10.3354/esr00239
Beekmans BWPM, Forcada J, Murphy E et al (2010) Generalised additive models to investigate environmental drivers of Antarctic minke whale (Balaenoptera bonaerensis) spatial density in austral summer. J Cetacean Res Manag 11:115–129
Bérubé M, Jørgensen H, McEwing R, Palsbøll P (2000) Polymorphic di-nucleotide microsatellite loci isolated from the humpback whale. Mol Ecol 9:2181–2183
Boyd JD, Brightsmith DJ (2013) Error properties of argos satellite telemetry locations using least squares and kalman filtering. PLoS ONE 8:1–10. https://doi.org/10.1371/journal.pone.0063051
Brandt A, Linse K, Schüller M (2009) Bathymetric distribution patterns of Southern Ocean macrofaunal taxa: bivalvia, gastropoda, isopoda and polychaeta. Deep Res Part I Oceanogr Res Pap 56:2013–2025. https://doi.org/10.1016/j.dsr.2009.06.007
Brierley AS, Fernandes PG, Brandon MA et al (2002) Antarctic krill under sea ice: elevated abundance in a narrow band just south of ice edge. Science 295:1890–1892. https://doi.org/10.1126/science.1068574
Cavalieri DJ, Parkinson CL, Gloersen P, Zwally HJ (1996) Boulder, Colorado USA. NASA DAAC National Snow and Ice Data Center
Clarke A, Murphy EJ, Meredith MP et al (2007) Climate change and the marine ecosystem of the western Antarctic Peninsula. Philos Trans R Soc B Biol Sci 362:149–166. https://doi.org/10.1098/rstb.2006.1958
Comiso JC, Kwok R, Martin S, Gordon AL (2011) Variability and trends in sea ice extent and ice production in the Ross Sea. J Geophys Res 116:1–19. https://doi.org/10.1029/2010JC006391
Comiso JC, Gersten RA, Stock LV et al (2017) Positive trend in the antarctic sea ice cover and associated changes in surface temperature. J Clim 30:2251–2267. https://doi.org/10.1175/JCLI-D-16-0408.1
Curtice C, Johnston DW, Ducklow H et al (2015) Modeling the spatial and temporal dynamics of foraging movements of humpback whales (Megaptera novaeangliae) in the Western Antarctic Peninsula. Mov Ecol 3:13. https://doi.org/10.1186/s40462-015-0041-x
Dinniman MS, Klinck JM, Smith WO (2003) Cross-shelf exchange in a model of the Ross Sea circulation and biogeochemistry. Deep Res Part II Top Stud Oceanogr 50:3103–3120. https://doi.org/10.1016/j.dsr2.2003.07.011
Donovan G (1991) A review of IWC stock boundaries. Rep Int Whal Commn Special Issue 13:39–68
Dulau V, Pinet P, Geyer Y et al (2017) Continuous movement behavior of humpback whales during the breeding season in the southwest Indian Ocean: on the road again! Mov Ecol 5:11. https://doi.org/10.1186/s40462-017-0101-5
Flores H, Atkinson A, Kawaguchi S et al (2012a) Impact of climate change on Antarctic krill. Mar Ecol Prog Ser 458:1–19. https://doi.org/10.3354/meps09831
Flores H, van Franeker JA, Siegel V et al (2012b) The association of Antarctic krill Euphausia superba with the under-ice habitat. PLoS ONE. https://doi.org/10.1371/journal.pone.0031775
Ford JKB, Ellis GM, Matkin DR et al (2005) Killer Whale attacks on Minke Whales: prey capture and antipredator tactics. Mar Mammal Sci 21:603–618. https://doi.org/10.1111/j.1748-7692.2005.tb01254.x
Friedlaender AS, Halpin PN, Qian SS et al (2006) Whale distribution in relation to prey abundance and oceanographic processes in shelf waters of the Western Antarctic Peninsula. Mar Ecol Prog Ser 317:297–310. https://doi.org/10.3354/meps317297
Friedlaender AS, Lawson GL, Halpin PN (2009) Evidence of resource partitioning between humpback and minke whales around the western Antarctic Peninsula. Mar Mammal Sci 25:402–415. https://doi.org/10.1111/j.1748-7692.2008.00263.x
Friedlaender A, Johnston D, Fraser W et al (2011) Ecological niche modeling of sympatric krill predators around Marguerite Bay, Western Antarctic Peninsula. Deep Sea Res Part II Top Stud Oceanogr 58:1729–1740. https://doi.org/10.1016/j.dsr2.2010.11.018
Friedlaender AS, Goldbogen JA, Nowacek DP et al (2014) Feeding rates and under-ice foraging strategies of the smallest lunge filter feeder, the Antarctic minke whale (Balaenoptera bonaerensis). J Exp Biol 217:2851–2854. https://doi.org/10.1242/jeb.106682
Garrigue C, Zerbini AN, Geyer Y, Clapham P (2010) Movements of satellite-monitored humpback whales from New Caledonia Movements of satellite-monitored humpback whales from New Caledonia. J Mammal 91:109–115. https://doi.org/10.1644/09-MAMM-A-033R.1.Key
Guisan A, Thuiller W (2005) Predicting species distribution: offering more than simple habitat models. Ecol Lett 8:993–1009. https://doi.org/10.1111/j.1461-0248.2005.00792.x
Hazen EL, Friedlaender ASA, Thompson MAM et al (2009) Fine-scale prey aggregations and foraging ecology of humpback whales Megaptera novaeangliae. Mar Ecol Prog Ser 395:75–89. https://doi.org/10.3354/meps08108
Heide-Jørgensen MP, Kleivane L, Øien N et al (2001) A new technique for deploying satellite transmitters on baleen whales: Tracking a blue whale (Balaenoptera musculus) in the North Atlantic. Mar Mammal Sci 17:949–954. https://doi.org/10.1111/j.1748-7692.2001.tb01309.x
Hill SL, Murphy EJ, Reid K et al (2006) Modelling Southern Ocean ecosystems: krill, the food-web, and the impacts of harvesting. Biol Rev Camb Philos Soc 81:581–608. https://doi.org/10.1017/S1464793106007123
Hill SL, Phillips T, Atkinson A (2013) Potential climate change effects on the habitat of Antarctic krill in the Weddell quadrant of the Southern Ocean. PLoS ONE 8:e72246. https://doi.org/10.1371/journal.pone.0072246
Ichii T (1990) Distribution of Antarctic krill concentrations exploited by Japanese krill trawlers and minke whales. In: Proceedings of the NIPR Symposium on Polar Biology. pp 36–56
Ichii T, Kato H (1991) Food and daily food consumption of southern minke whales in the Antarctic. Polar Biol 11:479–487. https://doi.org/10.1007/BF00233083
Ichii T, Shinohara N, Fujise Y et al (1998) Interannual changes in body fat condition index of minke whales in the Antarctic. Mar Ecol Prog Ser 175:1–12. https://doi.org/10.3354/meps175001
IWC (2013) Report of the Scientific Committee. J Cetacean Res Manag 14:1–468
IWC (2016) Report of the expert panel to review the proposal by Japan for NEWREP-A. J Cetacean Res Manag 17:509–553
Jarvis T, Kelly N, Kawaguchi S et al (2010) Acoustic characterisation of the broad-scale distribution and abundance of Antarctic krill (Euphausia superba) off East Antarctica (30–80°E) in January-March 2006. Deep Sea Res Part II Top Stud Oceanogr 57:916–933. https://doi.org/10.1016/j.dsr2.2008.06.013
Jefferson TA, Stacey PJ, Baird RW (1991) A review of Killer Whale interactions with other marine mammals: predation to co-existence. Mamm Rev 21:151–180. https://doi.org/10.1111/j.1365-2907.1991.tb00291.x
Jonsen ID (2016) Joint estimation over multiple individuals improves behavioural state inference from animal movement data. Sci Rep 6:1–9. https://doi.org/10.1038/srep20625
Jonsen ID, Flemming JM, Myers RA (2005) Robust state: space modeling of animal movement data. Ecology 86:2874–2880. https://doi.org/10.1890/04-1852
Jonsen ID, Myers RA, James MC (2007) Identifying leatherback turtle foraging behaviour from satellite telemetry using a switching state-space model. Mar Ecol Prog Ser 337:255–264. https://doi.org/10.3354/meps337255
Jonsen ID, Basson M, Bestley S et al (2013) State-space models for bio-loggers: a methodological road map. Deep Res Part II 88–89:34–46. https://doi.org/10.1016/j.dsr2.2012.07.008
Kasamatsu F, Matsuoka K, Hakamada T (2000) Interspecific relationships in density among the whale community in the Antarctic. Polar Biol 23:466–473. https://doi.org/10.1007/s003009900107
Kato H (1990) Some analyses on age composition and segregation of southern minke whales using samples obtained from the Japanese feasibility study in 1987/88. Rep Int Whal Commn 40:249–256
Kennedy AS, Zerbini AN, Rone BK, Clapham PJ (2014) Individual variation in movements of satellitetracked humpback whales Megaptera novaeangliae in the Eastern Aleutian Islands and Bering Sea. Endanger Species Res 23:187–195. https://doi.org/10.3354/esr00570
Konishi K, Walløe L (1990) Substantial decline in energy storage and stomach fullness in Antarctic minke whales (Balaenoptera bonaerensis) during the 1990s. J Cetacean Res Manag 15:77–92
Konishi K, Tamura T, Zenitani R et al (2008) Decline in energy storage in the Antarctic minke whale (Balaenoptera bonaerensis) in the Southern Ocean. Polar Biol 31:1509–1520. https://doi.org/10.1007/s00300-008-0491-3
Konishi K, Hakamada T, Kiwada H et al (2014) Decrease in stomach contents in the Antarctic minke whale (Balaenoptera bonaerensis) in the Southern Ocean. Polar Biol 37:205–215. https://doi.org/10.1007/s00300-013-1424-3
Krafft BA, Skaret G, Knutsen T (2015) An Antarctic krill (Euphausia superba) hotspot: population characteristics, abundance and vertical structure explored from a krill fishing vessel. Polar Biol 38:1687–1700. https://doi.org/10.1007/s00300-015-1735-7
Laidre KL, Heagerty PJ, Heide-Jørgensen MP et al (2009) Sexual segregation of common minke whales (Balaenoptera acutorostrata) in Greenland, and the influence of sea temperature on the sex ratio of catches. ICES J Mar Sci 66:2253–2266
Large S, Fay G, Friedland K, Link J (2014) Critical points in ecosystem responses to fishing and environmental pressures. Mar Ecol Prog Ser 521:1–17. https://doi.org/10.3354/meps11165
Larsen F (1998) Development of a biopsy system primarily for use on large cetaceans. Paper SC/50/O15 presented to the IWC Scientific Committee
Laws RM (1985) The ecology of the Southern Ocean. Am Sci 73:26–40
Lecomte O, Goosse H, Fichefet T et al (2017) Vertical ocean heat redistribution sustaining sea-ice concentration trends in the Ross Sea. Nat Commun. https://doi.org/10.1038/s41467-017-00347-4
Lee JF, Friedlaender AS, Oliver MJ, DeLiberty TL (2017) Behavior of satellite-tracked Antarctic minke whales (Balaenoptera bonaerensis) in relation to environmental factors around the western Antarctic Peninsula. Anim Biotelemetry 5:23. https://doi.org/10.1186/s40317-017-0138-7
Mate B, Mesecar R, Lagerquist B (2007) The evolution of satellite-monitored radio tags for large whales: one laboratory’s experience. Deep Res Part II Top Stud Oceanogr 54:224–247. https://doi.org/10.1016/j.dsr2.2006.11.021
Matsuoka K, Hakamada T, Kiwada H et al (2011) Abundance estimates and trends for humpback whales (Megaptera novaeangliae) in Antarctic Areas IV and V based on JARPA sighting data. J Cetacean Res Manag Special Issue 3:75–94
Meehl GA, Arblaster JM, Chung CTY et al (2018) Sustained ocean changes contributed to sudden Antarctic sea ice retreat in late 2016. Nat Commun 10:1–9. https://doi.org/10.1038/s41467-018-07865-9
Murase H, Matsuoka K, Ichii T, Nishiwaki S (2002) Relationship between the distribution of euphausiids and baleen whales in the Antarctic (35 E-145 W). Polar Biol 25:135–145. https://doi.org/10.1007/s003000100321
Murase H, Nagashima H, Yonezaki S et al (2009) Application of a generalized additive model (GAM) to reveal relationships between environmental factors and distributions of pelagic fish and krill: a case study in Sendai Bay, Japan. ICES J Mar Sci. https://doi.org/10.1093/icesjms/fsp105
Murase H, Kitakado T, Hakamada T et al (2013) Spatial distribution of Antarctic minke whales (Balaenoptera bonaerensis) in relation to spatial distributions of krill in the Ross Sea, Antarctica. Fish Oceanogr 22:154–173. https://doi.org/10.1111/fog.12011
Nicol S, Pauly T, Bindoff N, Strutton P (2000) “BROKE” a biological/oceanographic survey off the coast of East Antarctica (80–150°E) carried out in January-March 1996. Deep Sea Res Part II Top Stud Oceanogr 47:2281–2297
Ohsumi S (1979) Feeding habits of the minke whale in the Antarctic. Rep Int Whal Commn 29:473–476
Ohsumi S, Masaki Y, Kawamura A (1970) Stock of the Antarctic minke whale. Sci Rep Whales Res Inst, Tokyo 22:75–125
Olsen E, Budgell WP, Head E et al (2009) First satellite-tracked long-distance movement of a sei whale (Balaenoptera borealis) in the North Atlantic. Aquat Mamm 35:313–318. https://doi.org/10.1578/AM.35.3.2009.313
Palsbøll P, Bérubé M, Larsen A, Jørgensen H (1997) Primers for the amplification of tri- and tetramer microsatellite loci in baleen whales. Mol Ecol 6:893–895
Panigada S, Donovan GP, Druon JN et al (2017) Satellite tagging of Mediterranean fin whales: working towards the identification of critical habitats and the focusing of mitigation measures. Sci Rep 7:1–12. https://doi.org/10.1038/s41598-017-03560-9
Pastene L (2006) What do we know about the stock structure of the Antarctic minke whale? A summary of studies and hypotheses. Pap SC/D06/J12 Present to IWC Sci Comm. https://www.icrwhale.org/pdf/SC-D06-J
Pastene LA, Goto M (2016) Genetic characterization and population genetic structure of the Antarctic minke whale Balaenoptera bonaerensis in the Indo-Pacific region of the Southern Ocean. Fish Sci 82:873–886. https://doi.org/10.1007/s12562-016-1025-5
Pauly T, Nicol S, Higginbottom I et al (2000) Distribution and abundance of Antarctic krill (Euphausia superba) off East Antarctica (80–150° E) during the Austral summer of 1995/1996. Deep Sea Res Part II Top Stud Oceanogr 47:2465–2488
Piñones A, Hofmann EE, Daly KL et al (2013) Modeling the remote and local connectivity of Antarctic krill populations along the western Antarctic Peninsula. Mar Ecol Prog Ser 481:69–92. https://doi.org/10.3354/meps10256
Pitman RL, Ensor P (2003) Three forms of killer whales (Orcinus orca) in Antarctic waters. J Cetacean Res Manag 5:131–139. https://doi.org/10.1038/news050606-2
Prieto R, Silva M, Waring G, Gonçalves J (2014) Sei whale movements and behaviour in the North Atlantic inferred from satellite telemetry. Endanger Species Res 26:103–113. https://doi.org/10.3354/esr00630
R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Sala A, Azzali M, Russo AA (2002) Krill of the Ross Sea: distribution, abundance and demography of Euphausia superba and Euphausia crystallorophias during the Italian Antarctic Expedition (January-February 2000). Sci Mar 66:123–133
Sancho LG, Pintado A, Navarro F et al (2017) Recent warming and cooling in the Antarctic peninsula region has rapid and large effects on lichen vegetation. Sci Rep 7:1–8. https://doi.org/10.1038/s41598-017-05989-4
Santora J, Reiss C, Loeb V, Veit R (2010) Spatial association between hotspots of baleen whales and demographic patterns of Antarctic krill Euphausia superba suggests size-dependent predation. Mar Ecol Prog Ser 405:255–269. https://doi.org/10.3354/meps08513
Silva MA, Prieto R, Jonsen I et al (2013) North Atlantic Blue and Fin Whales suspend their spring migration to forage in middle latitudes: building up energy reserves for the journey? PLoS ONE 8:e76507. https://doi.org/10.1371/journal.pone.0076507
Silva MA, Jonsen I, Russell DJF et al (2014) Assessing performance of Bayesian state-space models fit to argos satellite telemetry locations processed with kalman filtering. PLoS ONE. https://doi.org/10.1371/journal.pone.0092277
Taki K, Yabuki T, Noiri Y et al (2008) Horizontal and vertical distribution and demography of euphausiids in the Ross Sea and its adjacent waters in 2004/2005. Polar Biol 31:1343–1356
Tamura T, Konishi K (2009) Feeding habits and prey consumption of Antarctic Minke Whale ( Balaenoptera bonaerensis ) in the Southern Ocean. J Northwest Atl Fish Sci 42:13–25. https://doi.org/10.2960/J.v42.m652
Tamura T, Ichii T, Fujise Y (1997) Consumption of krill by minke whales in Areas IV and V of the Antarctic. IWC Sci Comm Work Pap SC/M 17:1–9
Vaughan DG, Marshall GJ, Connolley WM et al (2003) Recent rapid regional climate warming on the Antarctic Peninsula. Clim Chang 60:243–274
Williams GD, Nicol S, Aoki S et al (2010) Surface oceanography of BROKE-West, along the Antarctic margin of the south-west Indian Ocean (30–80°E). Deep Res Part II Top Stud Oceanogr 57:738–757. https://doi.org/10.1016/j.dsr2.2009.04.020
Williams R, Kelly N, Boebel O et al (2014) Counting whales in a challenging, changing environment. Sci Rep 4:4170. https://doi.org/10.1038/srep04170
Wood SN (2017) Generalized additive models: an introduction with R (2nd edn). Chapman and Hall/CRC, Boca Raton
Xie S, Bao C, Xue Z et al (1994) Interaction between Antarctic sea ice and ENSO events. Proc NIPR Symp Polar Meteorol Glaciol 8:95–110
Zhang L, Delworth TL, Cooke W, Yang X (2019) Natural variability of Southern Ocean convection as a driver of observed climate trends. Nat Clim Chang 9:59–65. https://doi.org/10.1038/s41558-018-0350-3
Acknowledgements
Authors thank all crew and researchers of Yushin-maru, Yushin-maru No.2, Yushin-maru No.3 and Kaiyo-maru No.7 who were engaged in the tagging experiments as part of the NEWREP-A cruises. This study was supported by the Fisheries Agency of Japan. We also thank M. Taguchi for providing information on the sex of the minke whales by genetic analyses, and S. Ohsumi, Y. Fujise, T. Tamura, L. Pastene and D. Goodman for their helpful comments. Comments from five anonymous reviewers helped to refine the manuscript further. We are thankful for the helpful advice.
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The tagging experiments on the Antarctic minke whale were conducted under the non-lethal research component of the New Scientific Whale Research Program in the Antarctic Ocean (NEWREP-A). The necessity of the tagging on the Antarctic minke whales and its procedure on this program has been opened to International Whaling Commission Scientific Committee and reviewed by a review panel selected from IWC specialists (IWC 2016). This process was substituted for ethical and protocol standards. The NEWREP-A program was conducted under the permission from The Fishery Agency of Japan and funded by the Institute of Cetacean Research. We did not receive funding from a commercial source and declare that there are no conflicts of interest.
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ESM 1
Locations of deployment (star) and tracking locations of the Antarctic minke whale (#160299) at every 6 hours estimated by the hSSSM in January (a) and February (b) in 2017. For further explanation, see the caption for Fig. 2. Supplementary file1 (PDF 241 kb)
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Konishi, K., Isoda, T., Bando, T. et al. Antarctic minke whales find ice gaps along the ice edge in foraging grounds of the Indo-Pacific sector (60° E and 140° E) of the Southern Ocean. Polar Biol 43, 343–357 (2020). https://doi.org/10.1007/s00300-020-02638-x
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DOI: https://doi.org/10.1007/s00300-020-02638-x