Abstract
Humpback whales (Megaptera novaeangliae) congregate to breed during the austral winter near tropical islands of the South Pacific (Oceania). It has long been assumed that humpback whales from Oceania migrate primarily to Antarctic feeding grounds directly south (International Whaling Commission Management Areas V and VI); however, there are few records of individual movement connecting these seasonal habitats. Based on genetic samples of living whales collected over nearly two decades, we demonstrate interchange between the breeding grounds of Oceania and Antarctic feeding Areas V, VI, and I (i.e., from 130°E to 60°W), as well as with the eastern Pacific (Colombia), and the migratory corridors of eastern Australia and New Zealand. We first compared genotype profiles (up to 16 microsatellite loci) of samples collected from Oceania breeding grounds to each other and to those from the eastern Pacific. The matching profiles documented 47 individuals that were present on more than one breeding ground, including the first record of movement between Oceania and Colombia. We then compared the 1179 genotypes from the breeding grounds to 777 from the migratory corridors of east Australia and New Zealand, confirming the connection of these corridors with New Caledonia. Finally, we compared genotypes from breeding grounds to 166 individuals from Antarctic feeding Areas I–VI. This comparison of genotypes revealed five matches: one between New Caledonia and Area V, one between Tonga and Area VI, two between Tonga and Area I (western edge), and one between Colombia and Area I (Antarctic Peninsula). Despite the relatively small number of samples from the Antarctic, our comparison has doubled the number of recorded connections with Oceania available from previous studies during the era of commercial whaling.
Similar content being viewed by others
References
Albertson GR, Friedlaender AS, Steel DJ, Aguayo-Lobo A, Bonatto SL, Caballero S, Constantine R, Cypriano-Souza AL, Engel MH, Garrigue C, Flórez-González L, Johnston DW, Nowacek DP, Olavarría C, Poole MM, Read AJ, Robbins J, Sremba AL, Baker CS (2017) Temporal stability and mixed-stock analyses of humpback whales (Megaptera novaeangliae) in the nearshore waters of the Western Antarctic Peninsula. Polar Biol. https://doi.org/10.1007/s00300-017-2193-1
Anderson M, Baverstock P, Steel D, Baker CS, Olavarría C (2003) Standardisation of genetic analysis protocols used in humpback whale research. In: Final report to the Department of the Environment and Heritage and the Natural Heritage Trust. Canberra, Australia
Anderson M, Steel D, Franklin W, Franklin T, Paton D, Burns D, Harrison P, Baverstock PR, Garrigue C, Olavarría C, Poole M, Hauser N, Constantine R, Thiele D, Clapham P, Donoghue M, Baker CS (2010) Microsatellite genotype matches of eastern Australian humpback whales to Area V feeding and breeding grounds. SC/62/SH7. Report to Scientific Committee of the International Whaling Commission. Agadir, Morocco
Baker CS, Clapham P (2004) Modelling the past and future of whales and whaling. Trends Ecol Evol 19:365–371
Baker CS, Slade R, Bannister JL, Abernethy R (1994) Hierarchical structure of mitochondrial DNA gene flow among humpback whales Megaptera novaeangliae, world-wide. Mol Ecol 3:313–327
Baker C, Steel D, Calambokidis J, Falcone E, Gonzalez-Peral U, Barlow J, Burdin A, Clapham PJ, Ford J, Gabriele CM, Mattila D, Rojas-Bracho L, Straley J, Taylor BL, Urban J, Wade PR, Weller D, Witteveen B, Yamaguchi M (2013) Strong maternal fidelity and natal philopatry shape genetic structure in North Pacific humpback whales. Mar Ecol Prog Ser 494:291–306
Bérubé M, Jørgensen H, McEwing R, Palsbøll PJ (2000) Polymorphic di-nucleotide microsatellite loci isolated from the humpback whale, Megaptera novaeangliae. Mol Ecol 9:2181–2183
Bérubé M, Rew MB, Cole T, Swartz SL, Zolman E, Øien N, Palsbøll PJ (2004) Genetic identification of an individual humpback whale between the eastern Caribbean and the Norwegian sea. Mar Mammal Sci 20:657–663
Brown MR, Corkeron PJ, Hale PT, Schultz KW, Bryden MM (1995) Evidence for a sex-segregated migration in the humpback whale (Megaptera novaeangliae). Proc R Soc Lond Ser B 259:229–234
Chittleborough RG (1965) Dynamics of two populations of humpback whales, Megaptera novaeangliae (Borowski). Aust J Mar Freshw Res 16:33–128
Clapham P, Baker CS (2009) Modern whaling. In: Perrin WF, Wursig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic Press, New York, pp 1328–1332
Clapham PJ, Aguilar A, Hatch LT (2008) Determining spatial and temporal scales for management: lessons from whaling. Mar Mammal Sci 24:183–201
Constantine R, Russell K, Gibbs N, Childerhouse S, Baker CS (2007) Photo-identification of humpback whales (Megaptera novaeangliae) in New Zealand waters and their migratory connections to breeding grounds of Oceania. Mar Mammal Sci 23:715–720
Constantine R, Jackson JA, Steel D, Baker CS, Brooks L, Burns D, Clapham P, Hauser N, Madon B, Mattila D, Oremus M, Poole M, Robbins J, Thompson K, Garrigue C (2012) Abundance of humpback whales in Oceania using photo-identification and microsatellite genotyping. Mar Ecol Prog Ser 453:249–261
Constantine R, Steel D, Allen J, Anderson M, Andrews O, Baker CS, Beeman P, Burns D, Charrassin J-B, Childerhouse S, Double M, Ensor P, Franklin T, Franklin W, Gales N, Garrigue C, Gibbs N, Harrison P, Hauser N, Hutsel A, Jenner C, Jenner M-N, Kaufman G, Macie A, Mattila D, Olavarría C, Oosterman A, Paton D, Poole M, Robbins J, Schmitt N, Stevick P, Tagarino A, Thompson K, Ward J (2014) Remote Antarctic feeding ground important for east Australian humpback whales. Mar Biol 161:1087–1093
Cypriano-Souza AL, Engel MH, Caballero S, Olavarría C, Flórez-González L, Capella J, Steel D, Sremba A, Aguayo A, Thiele D, Baker CS, Bonatto SL (2017) Genetic differentiation between humpback whales (Megaptera novaeangliae) from Atlantic and Pacific breeding grounds of South America. Mar Mammal Sci 33:457–479
Dawbin WH (1956) Whale marking in the South Pacific waters. Nor Hvalfangsttiid 45:485–508
Dawbin WH (1959) New Zealand and South Pacific whale marking and recoveries to the end of 1958. Nor Hvalfangsttiid 48:213–238
Dawbin WH (1964) Movements of humpback whales marked in the southwest Pacific Ocean 1952–1962. Nor Hvalfangsttiid 53:68–78
Dawbin WH (1966) The seasonal migratory cycle of humpback whales. In: Norris KS (ed) Whales, dolphins and porpoises. University of California Press, Berkley, pp 145–171
DeSalle R, Amato G (2004) The expansion of conservation genetics. Nature 5:702–712
Donovan G (1991) A review of stock boundaries. In: Hoelzel AR (ed) Genetic ecology of whales and dolphins, Special Issue 13. Report of the International Whaling Commission, Cambridge
Elphinstone MS, Hinten GN, Anderson MJ, Nock CJ (2003) An inexpensive and high-throughput procedure to extract and purify total genomic DNA for population studies. Mol Ecol Notes 3:317–320
Franklin W, Franklin T, Brooks L, Gibbs N, Childerhouse S, Smith F, Burns D, Paton D, Garrigue C, Constantine R, Poole MM, Hauser N, Donoghue M, Russell K, Mattila DK, Robbins J, Oosterman A, Leaper R, Baker CS, Clapham P (2008) Migratory movements of humpback whales (Megaptera novaeangliae) between eastern Australia and the Balleny Islands, Antarctica, confirmed by photo-identification. SC/60/SH2. Report to Scientific Committee of the International Whaling Commission. Santiago, Chile
Gannier A (2004) The large-scale distribution of humpback whales (Megaptera novaeangliae) wintering in French Polynesia during 1997–2002. Aquat Mammals 30:227–236
Garrigue C, Aguayo A, Amante-Helweg VLU, Baker CS, Caballero S, Clapham P, Constantine R, Denkinger J, Donoghue M, Flórez-González L, Greaves J, Hauser N, Olavarría C, Pairoa C, Peckham H, Poole M (2002) Movements of humpback whales in Oceania, South Pacific. J Cetacean Res Manag 4:255–260
Garrigue C, Zerbini AN, Geyer Y, Heide-Jørgensen M-P, Hanaoka W, Clapham P (2010) Movements of satellite-monitored humpback whales from New Caledonia. J Mammal 91:109–115
Garrigue C, Constantine R, Poole M, Hauser N, Clapham P, Donoghue M, Russell K, Paton D, Mattila D, Robbins J, Baker CS (2011a) Movement of individual humpback whales between wintering grounds of Oceania (South Pacfic), 1999–2004. J Cetacean Res Manag (Special Issue) 3:275–281
Garrigue C, Franklin T, Russell K, Burns D, Poole M, Paton D, Hauser N, Oremus M, Constantine R, Childerhouse S, Mattila D, Franklin W, Robbins J, Clapham P, Baker CS (2011b) First assessment of interchange of humpback whales between Oceania and the east coast of Australia. J Cetacean Res Manag (Special Issue) 3:269–274
Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162
Hauser N, Peckham H, Clapham P (2000) Humpback whales in the southern Cook Islands, South Pacific. J Cetacean Res Manag 2:159–164
Hauser N, Zerbini AN, Geyer Y, Heide-Jørgensen M-P, Clapham P (2010) Movements of satellite-monitored humpback whales, Megaptera novaeangliae, from the Cook Islands. Mar Mammal Sci 26:679–685
Hoffman JI, Amos W (2005) Microsatellite genotyping errors: detection approaches, common sources and consequences for paternal exclusion. Mol Ecol 14:599–612
IWC (1998) Report of the Sub-Committee on Comprehensive Assessment of Southern Hemisphere Humpback Whales. Report of the Scientific Committee, Annex G. Report of the International Whaling Commission, Cambridge, UK, pp 170–182
IWC (2015) Report of the Sub-Committee on Other Southern Hemisphere Whale Stocks. Report of the Scientific Committee, Annex H. Report of the International Whaling Commission, Cambridge, UK, pp 250–282
IWC (2016) Report of the Sub-Committee on Other Southern Hemisphere Whale Stocks. Report of the Scientific Committee, Annex H. Report of the International Whaling Commission, Cambridge, UK, pp 230–263
Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655
Mikhalev YA (1997) Additional information about the catches of Soviet whaling fleet Sovietskaya Ukraina. Rep Int Whal Comm 47:147–150
Mikhalev YA, Tormosov DD (1997) Corrected data about non-Soviet whale marks recovered by Soviet whaling fleets. SC/48/SH29. Report to Scientific Committee of the International Whaling Commission. Aberdeen, Scotland
Noad M, Dunlop RA, Bennett L, Kniest H (2016) Abundance estimate of the east Australian humpback whale population (BSE1): 2015 survey and update. SC/66b/SH21. Report to Scientific Committee of the International Whaling Commission. Bled, Slovenia
Olavarría C, Anderson M, Paton D, Burns D, Brasseur M, Garrigue C, Hauser N, Poole M, Caballero S, Flórez-González L, Baker CS (2006) Eastern Australia humpback whale genetic diversity and their relationship with Breeding Stocks D,E,F and G. SC/58/SH25. Report to Scientific Committee of the International Whaling Commission. St Kitts and Nevis
Olavarría C, Baker CS, Garrigue C, Poole M, Hauser N, Caballero S, Flórez-González L, Brasseur M, Bannister JL, Capella J, Clapham PJ, Dodemont R, Donoghue M, Jenner C, Jenner M-N, Moro D, Oremus M, Paton D, Rosenbaum H, Russell K (2007) Population structure of South Pacific humpback whales and the origin of the Eastern Polynesian breeding grounds. Mar Ecol Prog Ser 330:257–268
Paetkau D (2003) An empirical exploration of data quality in DNA-based population inventories. Mol Ecol 12:1375–1387
Palsbøll PJ, Bérubé M, Larsen AH, Jørgensen H (1997) Primers for the amplification of tri- and tetramer microsatellite loci in baleen whales. Mol Ecol 6:893–895
Paterson R, Paterson P (1984) A study of the past and present status of humpback whales in east Australian waters. Biol Cons 29:321–343
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539
Pomilla C, Rosenbaum HC (2005) Against the current: an inter-oceanic whale migration event. Biol Let 1:476–479
Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Genet 6:846–847
Poole M (2002) Occurence of humpback whales (Megaptera novaeangliae) in French Polynesia in 1988–2001. SC/54/H14. Report to Scientific Committee of the International Whaling Commission. Shimonoseki, Japan
Rasmussen K, Palacios NM, Calambokidis J, Saborío MT, Rosa LD, Secchi ER, Steiger GH, Allen JM, Stone GS (2007) Southern Hemisphere humpback whales wintering off Central America: insights from water temperature into the longest mammalian migration. Biol Let 3:302–305
Robbins J, Dalla Rosa L, Allen J, Mattila D, Secchi E, Friedlaender A, Stevick P, Nowacek D, Steel D (2011) Return movement of a humpback whale between the Antarctic Peninsula and American Samoa: a seasonal migration record. Endanger Species Res 13:117–121
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York
Schlötterer C, Amos W, Tautz D (1991) Conservation of polymorphic simple sequence loci in cetacean species. Nature 354:63–65
Stevick P, Aguayo A, Allen JM, Avila IC, Capella J, Castro C, Chater K, Engel MH, Félix F, Flórez-González L, Freitas L, Hasse B, Llano M, Lodi L, Muñoz E, Olavarría C, Secchi E, Scheidat M, Siciliano S (2004) A note on the migrations of individually identified humpback whales between the Antarctic Peninsula and South America. J Cetacean Res Manag 6:109–113
Stevick PT, Neves MC, Johansen F, Engel MH, Allen J, Marcondes MCC, Carlson C (2011) A quarter of a world away: female humpback whale moves 10,000 km between breeding areas. Biol Let 7:299–302
Stone GS, Flórez-González L, Katona S (1990) Whale migration record. Nature 346:705
Townsend CH (1935) The distribution of certain whales as shown by logbook records of American whaleships. Zoologica 19:1–50
Valsecchi E, Amos W (1996) Microsatellite markers for the study of cetacean populations. Mol Ecol 5:151–156
Valsecchi E, Corkeron PJ, Galli P, Sherwin W, Bertorelle G (2010) Genetic evidence of sex-specific migratory behaviour in western South Pacific humpback whales. Mar Ecol Prog Ser 398:275–286
Waits JL, Leberg PL (2000) Biases associated with population estimation using molecular tagging. Anim Conserv 3:191–199
Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256
Waldick RC, Brown MW, White BN (1999) Characterization and isolation of microsatellite loci from the endangered North Atlantic right whale. Mol Ecol 8:1763–1765
Acknowledgements
This survey was made possible through the generous collaboration of members and affiliates of the South Pacific Whale Research Consortium (SPWRC), with support of the International Fund for Animal Welfare (IFAW). Fieldwork in American Samoa was conducted with help from David Mattila, Alden Tagarino, the Department of Marine and Wildlife Resources, and the U.S. National Marine Sanctuary Program. We acknowledge the Universidad de los Andes, proyecto semilla, Facultad de Ciencias. Funding for laboratory analysis was provided by the Regional Natural Heritage Program, Department of Environment and Heritage, Government of Australia and the Endowment of the Marine Mammal Institute, Oregon State University. All biopsy samples were collected with appropriate permits using protocols similar to those approved by the Animal Ethics Committee of the University of Auckland and the Institutional Animal Care and Use Committee of Oregon State University. We thank the International Whaling Commission for permission to use samples collected by Paul Ensor and Hidehiro Kato under the IDCR/SOWER program and the Southwest Fisheries Science Center (NMFS) for archiving the samples. Samples from the Antarctic Peninsula were made available courtesy of Instituto Antártico Chileno (INACH). We thank the Associate Editor and three anonymous reviewers for constructive comments.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Steel, D., Anderson, M., Garrigue, C. et al. Migratory interchange of humpback whales (Megaptera novaeangliae) among breeding grounds of Oceania and connections to Antarctic feeding areas based on genotype matching. Polar Biol 41, 653–662 (2018). https://doi.org/10.1007/s00300-017-2226-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-017-2226-9