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Polar Biology

, Volume 41, Issue 4, pp 653–662 | Cite as

Migratory interchange of humpback whales (Megaptera novaeangliae) among breeding grounds of Oceania and connections to Antarctic feeding areas based on genotype matching

  • D. Steel
  • M. Anderson
  • C. Garrigue
  • C. Olavarría
  • S. Caballero
  • S. Childerhouse
  • P. Clapham
  • R. Constantine
  • S. Dawson
  • M. Donoghue
  • L. Flórez-González
  • N. Gibbs
  • N. Hauser
  • M. Oremus
  • D. Paton
  • M. M. Poole
  • J. Robbins
  • L. Slooten
  • D. Thiele
  • J. Ward
  • C. S. Baker
Original Paper

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.

Keywords

Humpback Megaptera novaeangliae Migration Genotyping 

Notes

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.

Supplementary material

300_2017_2226_MOESM1_ESM.pdf (131 kb)
Supplementary material 1 (PDF 131 kb)
300_2017_2226_MOESM2_ESM.xlsx (44 kb)
Supplementary material 2 (XLSX 44 kb)

References

  1. 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 Google Scholar
  2. 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, AustraliaGoogle Scholar
  3. 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, MoroccoGoogle Scholar
  4. Baker CS, Clapham P (2004) Modelling the past and future of whales and whaling. Trends Ecol Evol 19:365–371CrossRefGoogle Scholar
  5. 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 3:313–327CrossRefPubMedGoogle Scholar
  6. 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 494:291–306CrossRefGoogle Scholar
  7. Bérubé M, Jørgensen H, McEwing R, Palsbøll PJ (2000) Polymorphic di-nucleotide microsatellite loci isolated from the humpback whale, Megaptera novaeangliae. Mol Ecol 9:2181–2183CrossRefPubMedGoogle Scholar
  8. 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 20:657–663CrossRefGoogle Scholar
  9. 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 259:229–234CrossRefGoogle Scholar
  10. Chittleborough RG (1965) Dynamics of two populations of humpback whales, Megaptera novaeangliae (Borowski). Aust J Mar Freshw Res 16:33–128CrossRefGoogle Scholar
  11. Clapham P, Baker CS (2009) Modern whaling. In: Perrin WF, Wursig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic Press, New York, pp 1328–1332Google Scholar
  12. Clapham PJ, Aguilar A, Hatch LT (2008) Determining spatial and temporal scales for management: lessons from whaling. Mar Mammal Sci 24:183–201CrossRefGoogle Scholar
  13. 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 23:715–720CrossRefGoogle Scholar
  14. 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 453:249–261CrossRefGoogle Scholar
  15. 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 161:1087–1093CrossRefGoogle Scholar
  16. 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 33:457–479CrossRefGoogle Scholar
  17. Dawbin WH (1956) Whale marking in the South Pacific waters. Nor Hvalfangsttiid 45:485–508Google Scholar
  18. Dawbin WH (1959) New Zealand and South Pacific whale marking and recoveries to the end of 1958. Nor Hvalfangsttiid 48:213–238Google Scholar
  19. Dawbin WH (1964) Movements of humpback whales marked in the southwest Pacific Ocean 1952–1962. Nor Hvalfangsttiid 53:68–78Google Scholar
  20. Dawbin WH (1966) The seasonal migratory cycle of humpback whales. In: Norris KS (ed) Whales, dolphins and porpoises. University of California Press, Berkley, pp 145–171Google Scholar
  21. DeSalle R, Amato G (2004) The expansion of conservation genetics. Nature 5:702–712Google Scholar
  22. 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, CambridgeGoogle Scholar
  23. 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 3:317–320CrossRefGoogle Scholar
  24. 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, ChileGoogle Scholar
  25. Gannier A (2004) The large-scale distribution of humpback whales (Megaptera novaeangliae) wintering in French Polynesia during 1997–2002. Aquat Mammals 30:227–236CrossRefGoogle Scholar
  26. 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 4:255–260Google Scholar
  27. 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 91:109–115CrossRefGoogle Scholar
  28. 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) 3:275–281Google Scholar
  29. 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) 3:269–274Google Scholar
  30. Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162CrossRefGoogle Scholar
  31. Hauser N, Peckham H, Clapham P (2000) Humpback whales in the southern Cook Islands, South Pacific. J Cetacean Res Manag 2:159–164Google Scholar
  32. 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 26:679–685Google Scholar
  33. Hoffman JI, Amos W (2005) Microsatellite genotyping errors: detection approaches, common sources and consequences for paternal exclusion. Mol Ecol 14:599–612CrossRefPubMedGoogle Scholar
  34. 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 170–182Google Scholar
  35. 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 250–282Google Scholar
  36. 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 230–263Google Scholar
  37. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655CrossRefPubMedGoogle Scholar
  38. Mikhalev YA (1997) Additional information about the catches of Soviet whaling fleet Sovietskaya Ukraina. Rep Int Whal Comm 47:147–150Google Scholar
  39. 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, ScotlandGoogle Scholar
  40. 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, SloveniaGoogle Scholar
  41. 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 NevisGoogle Scholar
  42. 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 330:257–268CrossRefGoogle Scholar
  43. Paetkau D (2003) An empirical exploration of data quality in DNA-based population inventories. Mol Ecol 12:1375–1387CrossRefPubMedGoogle Scholar
  44. Palsbøll PJ, Bérubé M, Larsen AH, Jørgensen H (1997) Primers for the amplification of tri- and tetramer microsatellite loci in baleen whales. Mol Ecol 6:893–895CrossRefPubMedGoogle Scholar
  45. Paterson R, Paterson P (1984) A study of the past and present status of humpback whales in east Australian waters. Biol Cons 29:321–343CrossRefGoogle Scholar
  46. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539CrossRefPubMedPubMedCentralGoogle Scholar
  47. Pomilla C, Rosenbaum HC (2005) Against the current: an inter-oceanic whale migration event. Biol Let 1:476–479CrossRefGoogle Scholar
  48. Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Genet 6:846–847CrossRefGoogle Scholar
  49. 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, JapanGoogle Scholar
  50. 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 3:302–305CrossRefGoogle Scholar
  51. 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 13:117–121CrossRefGoogle Scholar
  52. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  53. Schlötterer C, Amos W, Tautz D (1991) Conservation of polymorphic simple sequence loci in cetacean species. Nature 354:63–65CrossRefPubMedGoogle Scholar
  54. 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 6:109–113Google Scholar
  55. 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 7:299–302CrossRefGoogle Scholar
  56. Stone GS, Flórez-González L, Katona S (1990) Whale migration record. Nature 346:705CrossRefGoogle Scholar
  57. Townsend CH (1935) The distribution of certain whales as shown by logbook records of American whaleships. Zoologica 19:1–50Google Scholar
  58. Valsecchi E, Amos W (1996) Microsatellite markers for the study of cetacean populations. Mol Ecol 5:151–156CrossRefPubMedGoogle Scholar
  59. 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 398:275–286CrossRefGoogle Scholar
  60. Waits JL, Leberg PL (2000) Biases associated with population estimation using molecular tagging. Anim Conserv 3:191–199CrossRefGoogle Scholar
  61. Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256CrossRefPubMedGoogle Scholar
  62. Waldick RC, Brown MW, White BN (1999) Characterization and isolation of microsatellite loci from the endangered North Atlantic right whale. Mol Ecol 8:1763–1765CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • D. Steel
    • 1
    • 18
  • M. Anderson
    • 18
  • C. Garrigue
    • 2
    • 3
    • 18
  • C. Olavarría
    • 4
    • 18
  • S. Caballero
    • 5
    • 18
  • S. Childerhouse
    • 6
    • 18
  • P. Clapham
    • 7
    • 18
  • R. Constantine
    • 8
    • 18
  • S. Dawson
    • 9
  • M. Donoghue
    • 10
    • 18
  • L. Flórez-González
    • 11
    • 18
  • N. Gibbs
    • 12
    • 18
  • N. Hauser
    • 13
    • 18
  • M. Oremus
    • 14
    • 18
  • D. Paton
    • 6
    • 18
  • M. M. Poole
    • 15
    • 18
  • J. Robbins
    • 16
    • 18
  • L. Slooten
    • 9
  • D. Thiele
    • 17
  • J. Ward
    • 10
    • 18
  • C. S. Baker
    • 1
    • 8
    • 18
  1. 1.Marine Mammal Institute and Department of Fisheries and WildlifeOregon State UniversityNewportUSA
  2. 2.Opération CétacésNouméaNew Caledonia
  3. 3.IRD UMR ENTROPIENouméaNew Caledonia
  4. 4.Centro de Estudios Avanzados en Zonas Aridas – CEAZALa SerenaChile
  5. 5.Laboratorio de Ecología Molecular de Vertebrados Acuáticos-LEMVA, Biological Sciences DepartmentUniversidad de los AndesBogotáColombia
  6. 6.Blue Planet MarineKingstonAustralia
  7. 7.AFSC/Marine Mammal LaboratorySeattleUSA
  8. 8.School of Biological SciencesUniversity of AucklandAucklandNew Zealand
  9. 9.University of OtagoDunedinNew Zealand
  10. 10.Secretariat of the Pacific Regional Environment Programme (SPREP)ApiaSamoa
  11. 11.Fundación YubartaCaliColombia
  12. 12.Cook Strait Whale SurveyWellingtonNew Zealand
  13. 13.Cook Islands Whale ResearchAvarua, RarotongaCook Islands
  14. 14.WWF-FranceNouméa CédexNew Caledonia
  15. 15.Marine Mammal Research ProgramMaharepa, MooréaFrench Polynesia
  16. 16.Center for Coastal StudiesProvincetownUSA
  17. 17.MarequusCapelAustralia
  18. 18.South Pacific Whale Research ConsortiumAvarua, RarotongaCook Islands

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