Marine Biology

, Volume 161, Issue 4, pp 805–819 | Cite as

Does temporal and spatial segregation explain the complex population structure of humpback whales on the coast of West Africa?

  • Inês Carvalho
  • Jacqueline Loo
  • Timothy Collins
  • Jaco Barendse
  • Cristina Pomilla
  • Matthew S. Leslie
  • Solange Ngouessono
  • Peter B. Best
  • Howard C. Rosenbaum
Original Paper

Abstract

Humpback whales (Megaptera novaeangliae) in the Southeastern Atlantic Ocean (International Whaling Commission ‘Breeding Stock B’—BSB) are distributed from the Gulf of Guinea to Western South Africa. Genetic data suggest that this stock may be sub-structured, but it remains unknown if this is due to reproductive segregation. This paper evaluates the spatial and temporal population structure of BSB humpback whales using a combination of maternally and bi-parentally inherited markers. The genetic differentiation that we identify in this study could be due to a combination of (1) spatial and/or temporal segregation on breeding grounds in the greater Gulf of Guinea, (2) the possibility of maternally inherited site fidelity to specific feeding grounds and (3) the use of two generalized but exclusive migratory routes (coastal and offshore) between feeding and breeding areas. Further, photo-identification and genetic sampling efforts in other areas of the Sub-Saharan Western Africa winter range and targeted deployment of satellite tags would help to clarify some of the apparent complexity in the population structure of animals biopsied in this region.

Supplementary material

227_2013_2379_MOESM1_ESM.tif (417 kb)
Figure S1 (Supplementary material) - STRUCTURE clustering results for K = 2, 3 and 4. Group labels are B1 = TSA, combined samples from Gabon, São Tomé, and Angola; B2 = WSA, samples from the West coast of South Africa. Each individual is represented by a vertical column partitioned into colour segments that represents its estimated admixture fraction in each cluster. (TIFF 417 kb)
227_2013_2379_MOESM2_ESM.tif (222 kb)
Figure S2 (Supplementary material) - Median-joining network of control region mtDNA haplotypes of humpback whales, implemented in NETWORK 4.6. (Bandelt et al. 1999). Circle size is proportional to the number of individuals exhibiting the corresponding haplotype. Each location within each haplotype is coloured according to the legend: TSA region: green circle Gabon; blue circle São Tomé; yellow circle Angola – Cabinda; WSA region: red circle West South Africa. (TIFF 222 kb)

References

  1. Acevedo JA, Aguayo-Lobo A, Pastene LA (2006) Filopatría de la ballena jorobada (Megaptera novaeangliae Borowski, 1781), al área de alimentación del Estrecho de Magallanes. Rev Biol Mar Oceanog 41:11–19Google Scholar
  2. Aguilar A (1985) Aboriginal whaling off Pagalu (Equatorial Guinea). Paper SC/36/PS13 presented to the International Whaling Commission Scientific CommitteeGoogle Scholar
  3. Ainley DG, Jongsomjit D, Ballard G, Thiele D, Fraser WR, Tynan CT (2012) Modeling the relationship of Antarctic minke whales to major ocean boundaries. Polar Biol 35:281–290Google Scholar
  4. Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 10:697–709Google Scholar
  5. André C, Larsson LC, Laikre L, Bekkevold D, Brigham J, Carvalho GR, Dahlgren TG, Hutchinson WF, Mariani S, Mudde K, Ruzzante DE, Ryman N (2011) Detecting population structure in a high gene-flow species, Atlantic herring (Clupea harengus): direct, simultaneous evaluation of neutral vs putatively selected loci. Heredity 106:270–280Google Scholar
  6. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  7. Baker CS, Palumbi SR, Lambertson RH, Weinrich MT, Calambokidis J, O’Brien SJ (1990) Influence of seasonal migration on geographic distribution of mitochondrial DNA haplotypes in humpback whales. Nature 344:238–240Google Scholar
  8. Baker CS, Perry A, Bannister JL, Weinrich MT, Abernethy RB, Calambokidis J, Lien J, Lambertsen RH, Urbán J, Vásquez O, Clapham PJ, Alling A, O′Brien SJ, Palumbi SR (1993) Abundant mitochondrial DNA variation and world-wide population structure in humpback whales. Proc Natl Acad Sci 90:8239–8243Google Scholar
  9. Baker CS, Slade RW, Bannister JL, Abernethy RB, Weinrich MT, Lien J, Urbán Ramirez J, Corkeron P, Calambokidis J, Vasquez O, Palumbi SR (1994) Hierarchical structure of mitochondrial DNA gene flow among humpback whales Megaptera novaeangliae, worldwide. Mol Ecol 3:313–327Google Scholar
  10. Baker CS, Flórez-González L, Abernethy B, Rosenbaum HC, Slade RW, Capella J, Bannister JL (1998) Mitochondrial DNA variation and maternal gene flow among humpback whales of the southern hemisphere. Mar Mammal Sci 14:721–737Google Scholar
  11. Bamy I, Van Waerebeek K, Bah SS, Dia M, Kaba B, Keita N, Konate S (2010) Species occurrence of cetaceans in Guinea, including humpback whales with southern hemisphere seasonality. Mar Biodivers Rec 3:e48Google Scholar
  12. Barendse J, Best P, Thornton M, Pomilla C, Carvalho I, Rosenbaum HC (2010) Migration redefined? Seasonality, movements, and group composition of humpback whales Megaptera novaeangliae off the west coast of South Africa. Afr J Mar Sci 32:1–22Google Scholar
  13. Barendse J, Best PB, Thornton M, Elwen SH, Rosenbaum HC, Carvalho I, Pomilla C, Collins T, Meyer M (2011) Transit station or destination? Attendance patterns, regional movement, and population estimate of humpback whales Megaptera novaeangliae off west South Africa based on photographic and genotypic matching. Afr J Mar Sci 33:353–373Google Scholar
  14. Barendse J, Best PB, Carvalho I, Pomilla C (2013) Mother knows best: occurrence and associations of resighted humpback whales suggest maternally derived fidelity to a Southern Hemisphere coastal feeding ground. PLoS ONE 8:e81238Google Scholar
  15. Berubé M, Palsbøll P (1996) Identification of sex in Cetaceans by multiplexing with three ZFX and ZFY specific primers. Mol Ecol 5:283–287Google Scholar
  16. Best PB, Sekiguchi K, Findlay KP (1995) A suspended migration of humpback whales Megaptera novaeangliae on the west coast of South Africa. Mar Ecol Prog Ser 118:1–12Google Scholar
  17. Best PB, Reeb D, Morais M, Baird A (1999) A preliminary investigation of humpback whales off northern Angola. Paper SC/51/CAWS33 presented to the International Whaling Commission Scientific CommitteeGoogle Scholar
  18. Bowen BW, Karl SA (2007) Population genetics and phylogeography of sea turtles. Mol Ecol 16:4886–4907Google Scholar
  19. Brown M, Corkeron P, Hale P, Schultz K, Bryden M (1995) Evidence for a sex-segregated migration in the humpback whale (Megaptera novaeangliae). Proc R Soc Lond Ser B 259:229–234Google Scholar
  20. Budker P, Collignon J (1952) Trois campagnes balenieres au Gabon: 1949–1950–1951. Bulletin l’Institut d’etudes centrafricaines 3:75–100Google Scholar
  21. Carvalho I, Brito C, dos Santos M, Rosenbaum HC (2011) The waters of São Tomé: a calving ground for West African humpback whales? Afr J Mar Sci 33:91–97Google Scholar
  22. Cerchio S, Strindberg S, Collins T, Bennett C, Rosenbaum HC (accepted) Seismic surveys negatively affect humpback whale singing activity off northern Angola. PLoS ONEGoogle Scholar
  23. Chittleborough RG (1965) Dynamics of two populations of humpback whales, Megaptera novaeangliae (Borowski). Aust J Mar Fresh Res 16:33–128Google Scholar
  24. Chow S, Okamoto H, Miyabe N, Hiramatsu K, Barut N (2000) Genetic divergence between Atlantic and Indo-Pacific stocks of bigeye tuna (Thunnus obesus) and admixture around South Africa. Mol Ecol 9:221–227Google Scholar
  25. Clapham PJ, Baraff LS, Carlson CA, Christian MA, Mattila DK, Mayo CA, Murphy MA, Pittman S (1993) Seasonal occurrence and annual return of humpback whales, Megaptera novaeangliae, in the southern Gulf of Maine. Can J Zool 71: 440–443Google Scholar
  26. Cornuet JM, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000Google Scholar
  27. Davis RW, Ortega-Ortiz JG, Ribic CA, Evans WE, Biggs DC, Ressler PH, Cady RB, Leben RR, Mullin KD, Würsig B (2002) Cetacean habitat in the northern oceanic Gulf of Mexico. Deep-Sea Res (1 Oceanogra Res Pap) 49:121–142Google Scholar
  28. Dawbin W (1966) The seasonal migratory cycle of humpback whales. In: Norris KS (ed) Whales, dolphins, and porpoises. University of California Press, Berkeley and Los Angeles, pp 145–171Google Scholar
  29. Dawbin W (1997) Temporal segregation of humpback whales during migration in southern hemisphere waters. Mem Queensl Mus 42:105–138Google Scholar
  30. Earl D, vonHoldt B (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4(2):359–361Google Scholar
  31. Ersts PJ, Pomilla C, Kiszka J, Cerchio S, Rosenbaum HC, Vély M, Razafindrakoto Y, Loo JA, Leslie M, Avolio M (2011) Observations of individual humpback whales utilising multiple migratory destinations in the southwestern Indian Ocean. Afri J Mar Sci 33:333–338Google Scholar
  32. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620Google Scholar
  33. Excoffier L, Lischer H (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567Google Scholar
  34. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491Google Scholar
  35. Favre L, Balloux F, Goudet J, Perrin N (1997) Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellites patterns. Proc R Soc Lond Ser B 264:127–132Google Scholar
  36. Félix F, Haase B (2005) Distribution of humpback whales along the coast of Ecuador and management implications. J Cetacean Res Manag 7:21–31Google Scholar
  37. Findlay KP (2000) A review of humpback whale caches by modern whaling operations in the Southern Hemisphere. Mem Queensl Mus 47:411–420Google Scholar
  38. Flórez-González L (1991) Humpback whales Megaptera novaeangliae in the Gorgona Island, Colombian Pacific breeding waters: population and pod characteristics. Mem Queensl Mus 30:291–295Google Scholar
  39. Fontaine MC, Baird SJE, Piry S, Ray N, Tolley KA, Duke S, Birkun A, Ferreira M, Jauniaux T, Llavona A, ztúrk BO, ztúrk AAO, Ridoux V, Rogan E, Sequeira M, Siebert U, Vikingsson GA, Bouquegneau J, Michaux JR (2007) Rise of oceanographic barriers in continuous populations of a cetacean: the genetic structure of harbour porpoises in Old World waters. BMC Biol 5:30–46Google Scholar
  40. Gibbons J, Capella J, Valladares C (2003) Rediscovery of a humpback whale, Megaptera novaeangliae, summering ground in the Strait of Magellan, Chile. J Cetacean Res Manag 5:203–208Google Scholar
  41. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html. Accessed 26 June 2008
  42. Guo S, Thompson E (1992) Performing the Exact test of Hardy Weinberg proportion for multiple alleles. Biometrics 48:361–372Google Scholar
  43. Hendry AP, Day T (2005) Population structure attributable to reproductive time: isolation by time and adaptation by time. Mol Ecol 14:901–916Google Scholar
  44. Hendry AP, Morbey YE, Berg OK, Wenburg JK (2004) Adaptive variation in senescence: reproductive lifespan in a wild salmon population. Proc R Soc Lond Ser B 271:259–266Google Scholar
  45. Hoelzel AR (1998) Genetic structure of cetacean populations in sympatry, parapatry and mixed assemblages; implications for conservation policy. J Hered 89:451–458Google Scholar
  46. Hubisz M, Falush D, Stephens M, Pritchard J (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332Google Scholar
  47. Hudson RR, Boos DD, Kaplan NL (1992) A statistical test for detecting geographic subdivision. Mol Biol Evol 9:138–151Google Scholar
  48. IWC (1998) Report of the scientific committee—annex G. Report of the sub committee on the comprehensive assessment of southern hemisphere humpback whales. Rep Int Whaling Comm 48:170–182Google Scholar
  49. Jost L (2008) G ST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026Google Scholar
  50. Kalinowski ST (2005) HP-rare: a computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:187–189Google Scholar
  51. Knutsen H, Jorde PE, André C, Stenseth NC (2003) Fine-scaled geographic population structuring in a highly mobile marine species: the Atlantic cod. Mol Ecol 12:385–394Google Scholar
  52. Laidre KL, Heagerty PJ, Heide-Jørgensen MP, Witting L, Simon M (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 66:2253–2266Google Scholar
  53. Lambertsen RH (1987) A biopsy system for large whales and its use for cytogenetics. J Mammal 68:443–445Google Scholar
  54. Lee PL, Luschi P, Hays GC (2007) Detecting female precise natal philopatry in green turtles using assignment methods. Mol Ecol 16:61–74Google Scholar
  55. Loseto LL, Richard P, Stern GA, Orr J, Ferguson SH (2006) Sexual segregation of Beaufort beluga whales during the open-water season. Can J Zool 84:1743–1751Google Scholar
  56. Lyrholm T, Leimar O, Johanneson B, Gyllensten U (1999) Sex-biased dispersal in sperm whales: contrasting mitochondrial and nuclear genetic structure of global populations. Proc R Soc Lond Ser B 266:347–354Google Scholar
  57. Mackintosh NA (1942) The southern stocks of whalebone whales. Discov Rep 22:197–300Google Scholar
  58. Matthews LH (1938) The humpback whale, Megaptera nodosa. Discov Rep 17:7–92Google Scholar
  59. Mattila DK, Clapham PJ, Vasquez O, Bowman R (1994) Occurrence, population composition and habitat use of humpback whales in Samana Bay, Dominican Republic. Can J Zoolog 72:1898–1907Google Scholar
  60. McKelvey KS, Schwartz MK (2005) DROPOUT: a program to identify problem loci and samples for noninvasive genetic samples in a capture-mark-recapture framework. Mol Ecol Notes 5:716–718Google Scholar
  61. Medrano-González L, Aguayo-Lobo A, Urbán-Ramirez J, Baker S (1995) Diversity and distribution of mitochondrial DNA lineages among humpback whales, Megaptera novaeangliae, in the Mexican Pacific Ocean. Can J Zool 73:1735–1743Google Scholar
  62. Mendez M, Rosenbaum HC, Subramaniam A, Yackulic C, Bordino P (2010) Isolation by environmental distance in mobile marine species: molecular ecology of franciscana dolphins at their southern range. Mol Ecol 19:2212–2228Google Scholar
  63. Mendez M, Subramaniam A, Collins T, Minton G, Baldwin R, Berggren P, Sarnblad A, Amir OA, Peddermors VM, Karczmarski L, Guissamulo A, Rosenbaum HC (2011) Molecular ecology meets remote sensing: environmental drivers to population structure of humpback dolphins in the Western Indian Ocean. Heredity 107:349–361Google Scholar
  64. Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distance between alleles with special reference for microsatellite loci. Genetics 142:1061–1064Google Scholar
  65. Mossman CA, Waser PM (1999) Genetic detection of sex-biased dispersal. Mol Ecol 8:1063–1067Google Scholar
  66. Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genets 7:783–787Google Scholar
  67. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  68. Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov Chain Monte Carlo approach. Genetics 158:885–896Google Scholar
  69. Palsbøll PJ, Vader A, Bakke I, Raafat El-Gewely M (1992) Determination of gender in cetaceans by the polymerase chain reaction. Can J Zool 70:2166–2170Google Scholar
  70. Palsbøll PJ, Bérubé M, Larsen A, Jørgensen H (1997) Primers for the amplification of tri- and tetramer microsatellite loci in baleen whales. Mol Ecol 6:893–895Google Scholar
  71. Palsbøll PJ, Bérubé M, Aguilar A, Notarbartolo-Di-Sciara G, Nielsen R (2004) Discerning between recurrent gene flow and recent divergence under a finite-site mutation model applied to North Atlantic and Mediterranean Sea fin whale (Balaenoptera physalus) populations. Evolution 58:670–675Google Scholar
  72. Palsbøll PJ, Bérubé M, Allendorf FW (2007) Identification of management units using population genetic data. Trends Ecol Evol 22:11–16Google Scholar
  73. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572Google Scholar
  74. Palumbi SR (2004) Marine reserves and ocean neighborhoods: the spatial scale of marine populations and their management. Annu Rev Environm Resourc 29:31–68Google Scholar
  75. Palumbi SR, Baker CS (1994) Contrasting population structure from nuclear intron sequences and mtDNA of humpback whales. Mol Biol Evol 11:426–435Google Scholar
  76. Palumbi SR, Warner RR (2003) Why gobies are like hobbits. Science 299:51–52Google Scholar
  77. Pardini AT, Jones CS, Noble LR, Kreiser B, Malcolm H, Bruce BD, Stevens JD, Cliff G, Scholl MC, Francis M, Duffy CAJ, Martin AP (2001) Sex-biased dispersal of great white sharks—in some respects, these sharks behave more like whales and dolphins than other fish. Nature 412:139–140Google Scholar
  78. Park S (2001) The excel microsatellite toolkit: Trypanotolerance in west African cattle and the population genetic effects of selection. Ph.D. dissertation, University of Dublin. Available at http://oscar.gen.tcd.ie/~sdepark/ms-toolkit/
  79. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel—population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539Google Scholar
  80. Perneger TV (1998) What’s wrong with Bonferroni adjustments. BMJ 316:1236–1238Google Scholar
  81. Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first generation migrants detection. J Hered 95:536–539Google Scholar
  82. Pomilla C (2005) Genetic structure of humpback whale (Megaptera novaeangliae) populations on Southern Hemisphere wintering grounds. Ph.D. Dissertation, New York UniversityGoogle Scholar
  83. Pomilla C, Best PB, Findlay KP, Collins T, Engel M, Minton G, Ersts P, Barendse J, Kotze PGH, Razafindrakoto Y, Ngouessono S, Meyer M, Thornton M Rosenbaum H (2006) Population structure and sex-biased gene flow in humpback whales from Wintering Regions A, B, C, and X based on nuclear microsatellite variation. Paper SC/A06/HW38 presented to the International Whaling Commission Scientific CommitteeGoogle Scholar
  84. Pritchard JK, Stephens M, Donelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959Google Scholar
  85. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci 98:9197–9201Google Scholar
  86. Rasmussen K, Palacios DM, Calambokidis J, Saborío MT, Dalla Rosa L, 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 Lett 3:302–305Google Scholar
  87. Raymond M, Rousset F (1995) GENEPOP: population genetic software for Exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  88. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225Google Scholar
  89. Rice DW (1998) Marine mammals of the world: systematics and distribution. Special Publication Number 4, Society for Marine Mammalogy. Allen Press, USAGoogle Scholar
  90. Rosenbaum HC, Collins T (2006) The ecology, population characteristics and conservation efforts for humpback whales (Megaptera novaeangliae) on their wintering grounds in the coastal waters of Gabon. In: Alonso A, Campbell P (eds) Natural history of the gamba complex. Smithsonian Press, Washington DC, pp 425–433Google Scholar
  91. Rosenbaum HC, Ersts P, Razafindrakoto Y, Sounguet G, Pomilla C, Ngouessono S, Rasoamampianina V, White L (2002) Population characteristics, distribution, and relative abundance of humpback whales off the coasts of Madagascar and Gabon: an update on recent and planned research. Paper SC/54/H20 presented to the International Whaling Commission Scientific CommitteeGoogle Scholar
  92. Rosenbaum HC, Pomilla CC, Mendez MC, Leslie M, Best P, Findlay K, Minton G, Ersts P, Collins T, Engel M, Bonatto S, Kotze D, Meÿer M, Barendse J, Thornton M, Razafindrakoto Y, Ngouessono S, Vely M, Kiszka J (2009) Population structure of humpback whales from their breeding grounds in the South Atlantic and Indian Oceans. PLoS ONE 4:e7318Google Scholar
  93. Rosenbaum HC, Maxwell S, Kershaw F, Mate B (accepted) Quantifying long-range movements and potential overlap with anthropogenic activity for humpback whales in the South Atlantic Ocean. Conserv BiolGoogle Scholar
  94. Rozas J, Sánchez-DelBarrio JC, Messegyer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497Google Scholar
  95. Ruckstuhl KE, Neuhaus P (2005) Sexual segregation in vertebrates: ecology of the two sexes. Cambridge University Press, CambridgeGoogle Scholar
  96. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  97. Scheidat M, Castro C, Denkinger J, González J, Adelung D (2000) A breeding area for humpback whales (Megaptera novaeangliae) off Ecuador. J Cetacean Res Manag 2:165–172Google Scholar
  98. Schlötterer C, Amos B, Tautz D (1991) Conservation of polymorphic simple sequence loci in cetacean species. Nature 354:63–65Google Scholar
  99. Shaw PW, Pierce GJ, Boyle PR (1999) Subtle population structuring within a highly vagile marine invertebrate, the veined squid Loligo forbesi, demonstrated with microsatellite DNA markers. Mol Ecol 8:407–417Google Scholar
  100. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462Google Scholar
  101. Smultea M (1994) Segregation by humpback whale (Megaptera novaeangliae) cows with a calf in coastal habitat near the island of Hawaii. Can J Zool 72:805–811Google Scholar
  102. Stevick P, Aguayo A, Allen J, Avila IC, Capella J, Castro C, Chater K, Engel MH, Félix F, Flórez-González L, Freitas A, Haase 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
  103. Stone GS, Flórez-González L, Katona S (1990) Whale migration record. Nature 346:705Google Scholar
  104. Valsecchi E, Amos W (1996) Microsatellite markers for the study of cetacean populations. Mol Ecol 5:151–156Google Scholar
  105. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538Google Scholar
  106. Van Waerebeek K, Tchibozo S, Montcho J, Nobime G, Sohouhoue P, Dossou C (2001) The Bight of Benin, a North Atlantic breeding ground of the Southern Hemisphere humpback whale population, likely related to Gabon and Angola substocks. Paper SC/53/IA21 presented to the International Whaling Commission Scientific CommitteeGoogle Scholar
  107. Van Waerebeek K, Ofori-Danson PK, Debrah J (2009) The cetaceans of Ghana: a validated faunal checklist. West Afr J Appl Ecol 15:61–90Google Scholar
  108. Waits L, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256Google Scholar
  109. Walsh PD, Fay JM, Gulick S, Sounguet GP (2000) Humpback whale activity near Cap Lopez, Gabon. J Cetacean Res Manag 2:63–68Google Scholar
  110. Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89:438–450Google Scholar
  111. Ward RD, Woodwark M, Skibinski DOF (1994) A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. J Fish Biol 44:213–232Google Scholar
  112. Weir C (2011) Distribution and seasonality of cetaceans in tropical waters between Angola and the Gulf of Guinea. Afr J Mar Sci 33:1–15Google Scholar
  113. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370Google Scholar
  114. Whitehead H (2003) Sperm whales: social evolution in the oceans. University of Chicago Press, ChicagoGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Inês Carvalho
    • 1
    • 2
    • 3
  • Jacqueline Loo
    • 2
    • 3
    • 4
  • Timothy Collins
    • 3
    • 5
  • Jaco Barendse
    • 6
    • 7
  • Cristina Pomilla
    • 2
    • 8
  • Matthew S. Leslie
    • 2
    • 9
  • Solange Ngouessono
    • 3
    • 10
  • Peter B. Best
    • 6
  • Howard C. Rosenbaum
    • 2
    • 3
  1. 1.Faculdade de Ciências e TecnologiaUniversidade do AlgarveFaroPortugal
  2. 2.Sackler Institute for Comparative GenomicsAmerican Museum of Natural HistoryNew YorkUSA
  3. 3.Ocean Giants ProgramWildlife Conservation SocietyBronxUSA
  4. 4.Department of BiologyNew York UniversityNew YorkUSA
  5. 5.Environment Society of OmanRuwiSultanate of Oman
  6. 6.Mammal Research InstituteUniversity of PretoriaCape TownSouth Africa
  7. 7.Sustainability Research Unit/SANParksNelson Mandela Metropolitan UniversityGeorgeSouth Africa
  8. 8.Wellcome Trust Sanger InstituteCambridgeUK
  9. 9.Scripps Institution of OceanographyUniversity of California San DiegoLa JollaUSA
  10. 10.Agence Nationale des Parcs NationauxLibrevilleGabon

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