Skip to main content

Advertisement

Log in

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

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Acevedo-Gutiérrez A, Croll DA, Tershy BR (2002) High feeding costs limit dive time in the largest whales. J Exp Biol 205:1747–1753

    PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Armstrong AJ, Siegfried WR (1991) Consumption of Antarctic krill by Minke whales. Antarct Sci 3:13–18. doi:10.1017/S0954102091000044

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Baayen RH (2011) languageR: Data sets and functions with “Analyzing Linguistic Data: A practical introduction to statistics”. R package version 1.2. http://CRAN.R-project.org/package=language

  • 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

    Article  Google Scholar 

  • 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 215–230

    Google Scholar 

  • Bannister JL (1994) Continued increase in humpback whales off Western Australia. Rep Int Whal Comm 44:309–310

    Google Scholar 

  • Bates DM (2007) Linear mixed model implementation in lme4. Manuscript, university of Wisconsin—Madison, January 2007

  • Branch TA (2006) Humpback abundance south of 60°S from three completed sets of IDCR/SOWER circumpolar surveys. IWC Document SC/AO6/HW6, pp 14

  • Branch TA (2007) Abundance of Antarctic blue whales south of 60 S from three complete circumpolar sets of surveys. J Cetacean Res Manag 9:253–262

    Google Scholar 

  • 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 3:143–174

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Donovan GP (1991) A review of IWC stock boundaries (special issue). Rep Int Whal Comm 13:39–68

    Google Scholar 

  • Faraway JJ (2006) Extending the linear model with R. Chapman & Hall/CRC, Boca Raton, FL, p 331

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 99

  • 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 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 35–39

  • 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

    Article  Google Scholar 

  • 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 41:287–292

    Google Scholar 

  • 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 28:411–420

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 9:105–115

    Google Scholar 

  • 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 3:75–94

    Google Scholar 

  • 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 

  • 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 6:73–131

    Google Scholar 

  • Mori M, Butterworth DS (2006) A first step towards modelling the krill-predator dynamics of the Antarctic ecosystem. CCAMLR Sci 13:217–277

    Google Scholar 

  • 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 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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: http://iwcoffice.org

  • 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

    Article  Google Scholar 

  • 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 

  • 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 http://www.R-project.org

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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: http://iwcoffice.org

  • Stefansson G (1996) Analysis of groundfish survey abundance data: combining the GLM and delta approaches. ICES J Mar Sci 53:577–588

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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. http://CRAN.R-project.org/package=LMERConvenienceFunctions

  • 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

  • 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 9

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kenji Konishi.

Additional information

The research reported here involved lethal sampling of minke whales, which was based on a permit issued by the Japanese Government in terms of Article VIII of the International Convention for the Regulation of Whaling. Reasons for the scientific need for this sampling have been stated both by the Japanese Government and by the authors.

Electronic supplementary material

Below is the link to the electronic supplementary material.

300_2013_1424_MOESM1_ESM.pdf

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

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

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)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Konishi, K., Hakamada, T., Kiwada, H. et al. Decrease in stomach contents in the Antarctic minke whale (Balaenoptera bonaerensis) in the Southern Ocean. Polar Biol 37, 205–215 (2014). https://doi.org/10.1007/s00300-013-1424-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-013-1424-3

Keywords

Navigation