Polar Biology

, Volume 37, Issue 2, pp 205–215 | Cite as

Decrease in stomach contents in the Antarctic minke whale (Balaenoptera bonaerensis) in the Southern Ocean

  • Kenji Konishi
  • Takashi Hakamada
  • Hiroshi Kiwada
  • Toshihide Kitakado
  • Lars Walløe
Original Paper


The Antarctic minke whale (Balaenoptera bonaerensis) is one of the major krill predators in Antarctic waters. A reported decline in energy storage over almost two decades indicates that food availability for the whales may also have declined recently. To test this hypothesis, catch data from 20 survey years in the Japanese Whale Research Program in the Antarctic (JARPA) and its second phase (JARPA II) (1990/91–2009/10), which covered the longitudinal sector between 35°E and 145°W south of 58°S, were used to investigate whether there was any annual trend in the stomach contents weight of Antarctic minke whales. A linear mixed-effects analysis showed a 31 % (95 % CI 12.6–45.3 %) decrease in the weight of stomach contents over the 20 years since 1990/1991. A similar pattern of decrease was found in both males and females, except in the case of females sampled at higher latitude in the Ross Sea. These results suggest a decrease in the availability of krill for Antarctic minke whales in the lower latitudinal range of the research area. The results are consistent with the decline in energy storage reported previously. The decrease in krill availability could be due to environmental changes or to an increase in the abundance of other krill-feeding predators. The latter appears somewhat more likely, given the recent rapid recovery of humpback whale. Furthermore, humpback whales are not found in the Ross Sea, where both Antarctic krill and ice krill (Euphausia crystallorophias) are available, and where no change in prey availability for Antarctic minke whales is indicated.


Minke whale Feeding ecology Balaenoptera Ross Sea Antarctic krill 



We would like to thank all the captains, crews, especially Hajime Shirasaki (Kyodo Senpaku Co. Ltd.) and the scientists who were involved in the JARPA and JARPA II surveys. Thanks are also due to T. Tamura, S. Kumagai, L.A. Pastene, H. Skaug and D. Butterworth for their useful comments on the manuscript, and to Alison Coulthard for correcting the English. The JARPA program was conducted with permission from the Japanese Fisheries Agency, Government of Japan.

Supplementary material

300_2013_1424_MOESM1_ESM.pdf (396 kb)
Online Resource 1 Efforts of sighting and sampling vessels and position of the Antarctic minke whales with stomach contents caught in JARPA and JARPA II periods (1990/91-2009/10). Grey lines represent search lines and black circles represent sampling positions where whales were sampled. (PDF 396 kb)
300_2013_1424_MOESM2_ESM.pdf (95 kb)
Online Resource 2 List of linear mixed-effects models used in the main analyses with log-transformed stomach content weight (log-SCW) as the dependent variable. The covariates in models were selected by an inclusion and exclusion process depending on whether the AIC value was smaller than in a previous model (Online Resource 3). (PDF 94 kb)
300_2013_1424_MOESM3_ESM.pdf (125 kb)
Online Resource 3 Results of linear mixed-effects models with log-transformed stomach content weight (log-SCW) as the dependent variable. Results are shown for both sexes combined and for males and females separately. The female dataset was divided into two, for lower (<70°S) and higher (>70°S) latitude areas. The Markov chain Monte Carlo (MCMC) method was applied for each model to evaluate and estimate p-values. Delta-AIC = 0 for the minimum AIC in each group of results. (PDF 124 kb)


  1. Acevedo-Gutiérrez A, Croll DA, Tershy BR (2002) High feeding costs limit dive time in the largest whales. J Exp Biol 205:1747–1753PubMedGoogle Scholar
  2. Ainley D, Ballard G, Ackley S, Blight LK, Eastman JT, Emslie SD, Lescroël A, Olmastroni S, Townsend SE, Tynan CT, Wilson P, Woehler E (2007) Paradigm lost, or is top-down forcing no longer significant in the Antarctic marine ecosystem? Antarct Sci 19:283–290. doi: 10.1017/S095410200700051X CrossRefGoogle Scholar
  3. Ainley D, Russell J, Jenouvrier S, Woehler E, Lyver P, Fraser WR, Kooyman GL (2010) Antarctic penguin response to habitat change as Earth’s troposphere reaches 28 °C above preindustrial levels. Ecol Monogr 801:49–66. doi: 10.1890/08-2289.1 CrossRefGoogle Scholar
  4. Armstrong AJ, Siegfried WR (1991) Consumption of Antarctic krill by Minke whales. Antarct Sci 3:13–18. doi: 10.1017/S0954102091000044 CrossRefGoogle Scholar
  5. Atkinson A, Siegel V, Pakhomov E, Rothery P (2004) Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature 432:100–103. doi: 10.1038/nature02996 PubMedCrossRefGoogle Scholar
  6. Baayen RH (2011) languageR: Data sets and functions with “Analyzing Linguistic Data: A practical introduction to statistics”. R package version 1.2.
  7. Baayen RH, Davidson DJ, Bates DM (2008) Mixed-effects modeling with crossed random effects for subjects and items. J Mem Lang 59:390–412. doi: 10.1016/j.jml.2007.12.005 CrossRefGoogle Scholar
  8. Ballance LT, Pitman RL, Hewitt RP, Siniff DB, Trivelpiece WZ, Clapham PJ, Brownell LB (2006) In: Estes A et al (eds) Whales, whaling and ocean ecosystems. University of California Press, Berkeley, CA, pp 215–230Google Scholar
  9. Bannister JL (1994) Continued increase in humpback whales off Western Australia. Rep Int Whal Comm 44:309–310Google Scholar
  10. Bates DM (2007) Linear mixed model implementation in lme4. Manuscript, university of Wisconsin—Madison, January 2007Google Scholar
  11. Branch TA (2006) Humpback abundance south of 60°S from three completed sets of IDCR/SOWER circumpolar surveys. IWC Document SC/AO6/HW6, pp 14Google Scholar
  12. Branch TA (2007) Abundance of Antarctic blue whales south of 60 S from three complete circumpolar sets of surveys. J Cetacean Res Manag 9:253–262Google Scholar
  13. Branch TA, Butterworth DS (2001) Southern Hemisphere minke whales: standardised abundance estimates from the 1978/79 to 1997/98 IDCR-SOWER surveys. J Cetacean Res Manag 3:143–174Google Scholar
  14. 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. doi: 10.1029/2010JC006391 CrossRefGoogle Scholar
  15. Donovan GP (1991) A review of IWC stock boundaries (special issue). Rep Int Whal Comm 13:39–68Google Scholar
  16. Faraway JJ (2006) Extending the linear model with R. Chapman & Hall/CRC, Boca Raton, FL, p 331Google Scholar
  17. Fletcher D, MacKenzie D, Villouta E (2005) Modelling skewed data with many zeros: a simple approach combining ordinary and logistic regression. Environ Ecol Stat 12:45–54. doi: 10.1007/s10651-005-6817-1 CrossRefGoogle Scholar
  18. Friedlaender AS, Lawson GL, Halpin PN (2009) Evidence of resource partitioning between humpback and minke whales around the western Antarctic Peninsula. Mar Mamm Sci 25:402–415. doi: 10.1111/j.1748-7692.2008.00263.x CrossRefGoogle Scholar
  19. Goldbogen JA, Calambokidis J, Shadwick RE, Oleson EM, McDonald MA, Hildebrand JA (2006) Kinematics of foraging dives and lunge-feeding in fin whales. J Exp Biol 209:1231–1244. doi: 10.1242/jeb.02135 PubMedCrossRefGoogle Scholar
  20. Goldbogen JA, Calambokidis J, Croll DA, Harvey JT, Newton KM, Oleson EM, Schorr G, Shadwick RE (2008) Foraging behavior of humpback whales: kinematic and respiratory patterns suggest a high cost for a lunge. J Exp Biol 211:3712–3719. doi: 10.1242/jeb.023366 PubMedCrossRefGoogle Scholar
  21. Government of Japan (2005) Plan for the Second Phase of the Japanese Whale Research Program under Special Permit in the Antarctic (JARPA II) -Monitoring of the Antarctic Ecosystem and Development of New Management Objectives for Whale Resources. Paper SC/57/O1 presented to the IWC Scientific Committee, Jun 2005, pp 99Google Scholar
  22. Hosokawa H, Kamiya T (1971) Some observations on the cetacean stomachs, with special considerations on the feeding habits of whales. Sci Rep Whales Res Inst 23:91–101 Google Scholar
  23. Hunt B, Hosie G (2006) The seasonal succession of zooplankton in the Southern Ocean south of Australia, part I: the seasonal ice zone. Deep Sea Res I 53:1182–1202. doi: 10.1016/j.dsr.2006.05.001 CrossRefGoogle Scholar
  24. Ichii T, Shinohara N, Fujise Y, Nishiwaki S, Matsuoka K (1998) Interannual changes in body fat condition index of minke whales in the Antarctic. Mar Ecol Prog Ser 175:1–12. doi: 10.3354/meps175001 CrossRefGoogle Scholar
  25. International Whaling Commission (2012) Report of the Sub-Committee on Abundance estimate on the Antarctic minke whale. Rep Int Whal Comm (available on IWC web page), pp 35–39Google Scholar
  26. Kasamatsu F, Matsuoka K, Hakamada T (2000) Interspecific relationships in density among the whale community in the Antarctic. Polar Biol 23:466–473. doi: 10.1007/s003009900107 CrossRefGoogle Scholar
  27. Kato H, Fujise Y, Kishino H (1991) Age structure and segregation of southern minke whales by the data obtained during Japanese research take in 1988/89. Rep Int Whal Comm 41:287–292Google Scholar
  28. Kawamura A (1978) An interim consideration on a possible interspecific relation in southern baleen whales from the viewpoint of their food habits. Rep Int Whal Comm 28:411–420Google Scholar
  29. Konishi K, Tamura T, Zenitani R, Bando T, Kato H, Walløe L (2008) Decline in energy storage in the Antarctic minke whale (Balaenoptera bonaerensis) in the Southern Ocean. Polar Biol 31:1509–1520. doi: 10.1007/s00300-008-0491-3 CrossRefGoogle Scholar
  30. Laws RM (1977) Seals and whales of the Southern Ocean. Philos Trans R Soc Lond B 279:81–96. doi: 10.1098/rstb.1977.0073 CrossRefGoogle Scholar
  31. Loeb V, Siegel V, Holm-Hansen O, Hewitt R, Fraser W, Trivelpiece W, Trivelpiece S (1997) Effects of sea-ice extent and krill or salp dominance on the Antarctic food web. Nature 387:897–900. doi: 10.1038/43174 CrossRefGoogle Scholar
  32. Martin T, Wintle B, Rhodes J, Kuhnert P, Field S, Low-Choy S, Tyre A, Possingham H (2005) Zero tolerance ecology: improving ecological inference by modelling the source of zero observations. Ecol Lett 8:1235–1246. doi: 10.1111/j.1461-0248.2005.00826.x PubMedCrossRefGoogle Scholar
  33. Matsuoka K, Hakamada T, Kiwada H, Murase H, Nishiwaki S (2005) Abundance increases of large baleen whales in the Antarctic based on the sighting survey during Japanese Whale Research Program (JARPA). Glob Environ Res 9:105–115Google Scholar
  34. Matsuoka K, Hakamada T, Kiwada H, Murase H, Nishiwaki S (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 3:75–94Google Scholar
  35. Meredith MP (2005) Rapid climate change in the ocean west of the Antarctic Peninsula during the second half of the 20th century. Geophys Res Lett 32:1–5. doi: 10.1029/2005GL024042 Google Scholar
  36. Mizue K, Murata T (1951) Biological investigation on the whales caught by the Japanese Antarctic whaling fleets season 1949–50. Sci Rep Whales Res Inst Tokyo 6:73–131Google Scholar
  37. Mori M, Butterworth DS (2006) A first step towards modelling the krill-predator dynamics of the Antarctic ecosystem. CCAMLR Sci 13:217–277Google Scholar
  38. 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. doi: 10.1007/s003000100321 Google Scholar
  39. Nicol S (2006) Krill, currents, and sea ice: Euphausia superba and its changing environment. BioScience 56:111–120. doi: 10.1641/0006-3568(2006)056 CrossRefGoogle Scholar
  40. Nicol S, Croxall J, Trathan P, Gales N, Murphy E (2007) Paradigm misplaced? Antarctic marine ecosystems are affected by climate change as well as biological processes and harvesting. Antarct Sci 19:291. doi: 10.1017/S0954102007000491 CrossRefGoogle Scholar
  41. Noad MJ, Dunlop RA, Paton D, Kniest H (2011) Abundance estimates of the east Australian humpback whale population: 2010 survey and update. Paper IWC/SC/63/SH22. Available at IWC web page:
  42. Olsen MA, Nordøy ES, Blix AS, Mathiesen SD (1994) Function anatomy of the gastrointestinal system of Northeastern Atlantic minke whales (Balaenoptera acutorostrata). J Zool Lond 234:55–74. doi: 10.1111/j.1469-7998.1994.tb06056.x CrossRefGoogle Scholar
  43. Plagányi EE, Butterworth DS (2012) The Scotia Sea krill fishery and its possible impacts on dependent predators—modeling localized depletion of prey. Ecol Monogr 22:748–761. doi: 10.1890/11-0441.1 Google Scholar
  44. R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL
  45. Reid K, Croxall JP (2001) Environmental response of upper trophic-level predators reveals a system change in an Antarctic marine ecosystem. Proc R Soc Lond B 268:377–384. doi: 10.1098/rspb.2000.1371 CrossRefGoogle Scholar
  46. Sala A, Azzali M, Russo A (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. doi: 10.3989/scimar.2002.66n2123 CrossRefGoogle Scholar
  47. 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. doi: 10.3354/meps08513 CrossRefGoogle Scholar
  48. Siegel V (2005) Distribution and population dynamics of Euphausia superba: summary of recent findings. Polar Biol 29:1–22. doi: 10.1007/s00300-005-0058-5 CrossRefGoogle Scholar
  49. Siegel V, Loeb V (1995) Recruitment of Antarctic krill Euphausia superba and possible causes for its variability. Mar Ecol Prog Ser 123:45–56. doi: 10.3354/meps123045 CrossRefGoogle Scholar
  50. Skaug (2011) Results of mixed-effects regression analyses of blubber thickness in Antarctic minke whale from data collected under JARPA. Appendix 2 in IWC/63/Rep 1 Report of the Scientific Committee Annex K1: Working Group to Address Multi-species and Ecosystem Modelling Approaches, Tromsø, Norway, 30 May to 11 June 2011. Available at IWC web page:
  51. Stefansson G (1996) Analysis of groundfish survey abundance data: combining the GLM and delta approaches. ICES J Mar Sci 53:577–588CrossRefGoogle Scholar
  52. Stone GS, Hamner WM (1988) Humpback whales Megaptera novaeangliae and southern right whales Eubalaena australis in Gerlache Strait, Antarctica. Polar Rec 24:15–20. doi: 10.1017/S0032247400022300 CrossRefGoogle Scholar
  53. Taki K, Yabuki T, Noiri Y, Hayashi T, Naganobu M (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. doi: 10.1007/s00300-008-0472-6 CrossRefGoogle Scholar
  54. Tamura T, Konishi K (2009) Feeding habits and prey consumption of Antarctic minke whale (Balaenoptera bonaerensis) in the Southern Ocean. J Northwest Alt Fish Sci 42:13–25. doi: 10.2960/J.v42.m652 CrossRefGoogle Scholar
  55. Trathan PN, Brierley AS, Brandon MA, Bone DG, Goss C, Grant SA, Murphy EJ, Watkins JL (2003) Oceanographic variability and changes in Antarctic krill (Euphausia superba) abundance at South Georgia. Fish Oceanogr 12:569–583. doi: 10.1046/j.1365-2419.2003.00268.x CrossRefGoogle Scholar
  56. Tremblay A (2011) LMERConvenienceFunctions: a suite of functions to back-fit fixed effects and forward-fit random effects, as well as other miscellaneous functions. R package version 1.6.3.
  57. Trivelpiece WZ, Hinke JT, Miller AK, Reiss CS, Trivelpiece SG, Watters GM (2011) Variability in krill biomass links harvesting and climate warming to penguin population changes in Antarctica. Proc Natl Acad Sci. Available on the PNAS web page, pp 1–4. doi: 10.1073/pnas.1016560108
  58. Zenitani R, Kato H (2006) Temporal trend of age at sexual maturity of Antarctic minke whales based on transition phase in earplugs obtained under JARPA surveys from 1987/88-2004/05. Paper AC/D05/J15 presented to the JARPA Review Meeting called by IWC, December 2006, pp 9Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Kenji Konishi
    • 1
  • Takashi Hakamada
    • 1
  • Hiroshi Kiwada
    • 2
  • Toshihide Kitakado
    • 3
  • Lars Walløe
    • 4
  1. 1.Institute of Cetacean ResearchTokyoJapan
  2. 2.Ocean Engineering & Development Co., Ltd.TokyoJapan
  3. 3.Tokyo University of Marine Science and TechnologyTokyoJapan
  4. 4.Department of Physiology, Institute of Basic Medical SciencesUniversity of OsloBlindern, OsloNorway

Personalised recommendations