Conservation Genetics

, Volume 19, Issue 1, pp 27–41 | Cite as

Genetic divergence between colonies of Flesh-footed Shearwater Ardenna carneipes exhibiting different foraging strategies

  • Anicee J. LombalEmail author
  • Theodore J. Wenner
  • Jennifer L. Lavers
  • Jeremy J. Austin
  • Eric J. Woehler
  • Ian Hutton
  • Christopher P. Burridge
Research Article


Increasing evidence suggests foraging segregation as a key mechanism promoting genetic divergence within seabird species. However, testing for a relationship between population genetic structure and foraging movements among seabird colonies can be challenging. Telemetry studies suggest that Flesh-footed Shearwater Ardenna carneipes that breed at Lord Howe Island or New Zealand, versus southwestern Australia or Saint-Paul Island in the Indian Ocean, migrate to different regions (North Pacific Ocean and northern Indian Ocean, respectively) during the non-breeding season, which may inhibit gene flow among colonies. In this study, we sequenced a 858-base pair mitochondrial region and seven nuclear DNA fragments (352–654 bp) for 148 individuals to test genetic differentiation among colonies of Flesh-footed Shearwaters. Strong genetic divergence was detected between Pacific colonies relative to those further West. Molecular analysis of fisheries’ bycatch individuals sampled in the Sea of Japan indicated that individuals from both western and eastern colonies were migrating through this area, and hence the apparent segregation of the non-breeding distribution based on telemetry is invalid and cannot contribute to the population genetic structure among colonies. The genetic divergence among colonies is better explained by philopatry and evidence of differences in foraging strategies during the breeding season, as supported by the observed genetic divergence between Lord Howe Island and New Zealand colonies. We suggest molecular analysis of fisheries’ bycatch individuals as a rigorous method to identify foraging segregation, and we recommend the eastern and western A. carneipes colonies be regarded as different Management Units.


Oceanic seabirds Ardenna carneipes Gene flow Genetic divergence Foraging segregation Genetic assignment Conservation management 



South Australia Nature Foundation, Trading Consultants (V. Wellington), Pennicott Wilderness Journeys and the Winifred Violet Scott Charitable Trust provided funding for the field and laboratory components of this research. Special thanks go to C. & G. Biddulph, P. Collins, A. Fidler, S. Goldsworthy, M. Stadler, the South Australian Department of Environment, Water & Natural Resources (DEWNR), and Western Australian Department of Parks and Wildlife (DPaW) for generously providing data and logistical support. This research was undertaken with animal ethic permissions from DPaW (SF009585), the University of Tasmania Animal Ethics committee (A13598 and A13836), DEWNR Resources permits (AEC 021028/02), and Lord Howe Island Board permits (LHIB 07/12 & LHIB 02/14). We thank the anonymous reviewers for their careful reading of our paper.

Author contributions

AL, JL and IH performed the sample collection. AL and TW collected the molecular data. AL performed the statistical and Bayesian analyses. CB and JL designed the study. AL, CB, JL, IH, JA and EW contributed to the manuscript.

Supplementary material

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Supplementary Information SI Additional information relative to the study entitled: ‘Genetic divergence between colonies of Flesh-footed Shearwater Ardenna carneipes exhibiting different foraging strategies 1) Identification numbers of A. carneipes samples. 2) Number of A. carneipes individuals sequenced for Cytochrome b and seven nuclear DNA fragments. 3) Description of primers for seven nuclear DNA fragments. 4) Variable sites in Cytochrome b. 5) Characterization of genetic diversity for Cytochrome b and seven nuclear DNA fragments. 6) Deviation from neutral expectations. 7) Haplotype networks for seven nuclear DNA fragments based on the TCS algorithm. 8) AMOVA Φ-statistics for Cytochrome b. 9-10) Marginal posterior distribution of the genetic parameters as implemented with IMa/IMa2. 11) Extended Bayesian Skyline Plot (EBSP) for Cytochrome b and four nuclear DNA fragments. (DOCX 534 KB)


  1. Abbott CL, Double MC (2003) Genetic structure, conservation genetics and evidence of speciation by range expansion in shy and white-capped albatrosses. Mol Ecol 12:2953–2962PubMedCrossRefGoogle Scholar
  2. Ashmole NP (1971) Seabird ecology and the marine environment. Avian Biol 1:223–286Google Scholar
  3. Austin JJ, White RW, Ovenden JR (1994) Population-genetic structure of a philopatric, colonially nesting seabird, the Short-tailed Shearwater (Puffinus tenuirostris). Auk 111:70–79CrossRefGoogle Scholar
  4. Avise JC (1989) A role for molecular genetics in the recognition and conservation of endangered species. Trends Ecol Evol 4:279–281PubMedCrossRefGoogle Scholar
  5. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  6. Avise JC, Hamrick JL (1996) Conservation genetics: case histories from nature. Chapman & Hall, UKCrossRefGoogle Scholar
  7. Avise JC, Alisauskas RT, Nelson WS, Ankney CD (1992) Matriarchal population genetic structure in an avian species with female natal philopatry. Evol Int J Org Evol 46:1084–1096CrossRefGoogle Scholar
  8. Axelsson E, Smith NG, Sundström H, Berlin S, Ellegren H (2004) Male-biased mutation rate and divergence in autosomal, Z-linked and W-linked introns of chicken and turkey. Mol Biol Evol 21:1538–1547PubMedCrossRefGoogle Scholar
  9. Backström N, Fagerberg S, Ellegren H (2008) Genomics of natural bird populations: a gene-based set of reference markers evenly spread across the avian genome. Mol Ecol 17:964–980PubMedCrossRefGoogle Scholar
  10. Baker GB, Wise BS (2005) The impact of pelagic longline fishing on the flesh-footed shearwater Puffinus carneipes in Eastern Australia. Biol Conserv 126:306–316CrossRefGoogle Scholar
  11. Bond AL, Lavers JL (2014) Climate change alters the trophic niche of a declining apex marine predator. Glob Change Biol 20:2100–2107CrossRefGoogle Scholar
  12. Bouckaert R et al (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537PubMedPubMedCentralCrossRefGoogle Scholar
  13. Brooke M (2004) Albatrosses and petrels across the world. Oxford University Press, EnglandGoogle Scholar
  14. Buckley TR, Marske K, Attanayake D (2010) Phylogeography and ecological niche modelling of the New Zealand stick insect Clitarchus hookeri (White) support survival in multiple coastal refugia. J Biogeogr 37:682–695CrossRefGoogle Scholar
  15. Burg T, Croxall J (2001) Global relationships amongst black-browed and grey-headed albatrosses: analysis of population structure using mitochondrial DNA and microsatellites. Mol Ecol 10:2647–2660PubMedCrossRefGoogle Scholar
  16. Burridge CP (2000) Biogeographic history of geminate cirrhitoids (Perciformes: Cirrhitoidea) with east–west allopatric distributions across southern Australia, based on molecular data. Global Ecol Biogeogr 9:517–525CrossRefGoogle Scholar
  17. Byrne M (2008) Evidence for multiple refugia at different time scales during Pleistocene climatic oscillations in southern Australia inferred from phylogeography. Quaternary Sci Rev 27:2576–2585CrossRefGoogle Scholar
  18. Catard A, Weimerskirch H, Cherel Y (2000) Exploitation of distant Antarctic waters and close shelf-break waters by white-chinned petrels rearing chicks. Mar Ecol-Prog Ser 194:249–261CrossRefGoogle Scholar
  19. Charlesworth B, Morgan M, Charlesworth D (1993) The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289–1303PubMedPubMedCentralGoogle Scholar
  20. Chepko-Sade BD, Halpin ZT (1987) Mammalian dispersal patterns: the effects of social structure on population genetics. University of Chicago Press, USAGoogle Scholar
  21. Cheung WW et al (2012) Climate-change induced tropicalisation of marine communities in Western Australia. Mar Freshwater Res 63:415–427CrossRefGoogle Scholar
  22. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659PubMedCrossRefGoogle Scholar
  23. Congdon BC, Piatt JF, Martin K, Friesen VL (2000) Mechanisms of population differentiation in marbled murrelets: historical versus contemporary processes. Evol Int J org Evol 54:974–986CrossRefGoogle Scholar
  24. Coulson JC (2001) Biology of marine birds. CRC Press, USAGoogle Scholar
  25. Dartnall MA (1974) Littoral biogeography. In: Biogeography and ecology in Tasmania. Springer, Netherlands, pp 171–194CrossRefGoogle Scholar
  26. Dawson MN, Hays CG, Grosberg RK, Raimondi PT (2014) Dispersal potential and population genetic structure in the marine intertidal of the eastern North Pacific. Ecol Monogr 84:435–456CrossRefGoogle Scholar
  27. Dellicour S, Mardulyn P (2014) SPADS 1.0: a toolbox to perform spatial analyses on DNA sequence data sets. Mol. Ecol Res 14:647–651CrossRefGoogle Scholar
  28. DeSalle R, Amato G (2004) The expansion of conservation genetics. Nature Rev Genet 5:702–712PubMedCrossRefGoogle Scholar
  29. Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192PubMedCrossRefGoogle Scholar
  30. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797PubMedPubMedCentralCrossRefGoogle Scholar
  31. Edwards SV, Silva MC, Burg T, Friesen V, Warheit KI Molecular genetic markers in the analysis of seabird bycatch populations. In: Proceedings of the Symposium Seabird Bycatch: Trends, Roadblocks and Solutions, 2001. pp 115–140Google Scholar
  32. 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 131:479–491PubMedPubMedCentralGoogle Scholar
  33. Flot JF (2010) SeqPHASE: a web tool for interconverting PHASE input/output files and FASTA sequence alignments. Mol Ecol Res 10:162–166CrossRefGoogle Scholar
  34. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140CrossRefGoogle Scholar
  35. Frankham R (2010) Where are we in conservation genetics and where do we need to go? Conserv Genet 11:661–663CrossRefGoogle Scholar
  36. Fraser CI, Spencer HG, Waters JM (2009) Glacial oceanographic contrasts explain phylogeography of Australian bull kelp. Mol Ecol 18:2287–2296PubMedCrossRefGoogle Scholar
  37. Friesen VL (2015) Speciation in seabirds: why are there so many species… and why aren’t there more? J Ornithol 156:27–39CrossRefGoogle Scholar
  38. Friesen V, Burg T, McCoy K (2007) Mechanisms of population differentiation in seabirds. Mol Ecol 16:1765–1785PubMedCrossRefGoogle Scholar
  39. Fu Y-X, Li W-H (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709PubMedPubMedCentralGoogle Scholar
  40. Genovart M, Oro D, Juste J, Bertorelle G (2007) What genetics tell us about the conservation of the critically endangered Balearic Shearwater? Biol Conserv 137:283–293CrossRefGoogle Scholar
  41. Grant WS (2015) Problems and cautions with sequence mismatch analysis and Bayesian skyline plots to infer historical demography. J Hered 106:333–346PubMedCrossRefGoogle Scholar
  42. Greenwood PJ, Harvey PH, PERRINS CM (1978) Inbreeding and dispersal in the great tit. Nature 271:52–54CrossRefGoogle Scholar
  43. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  44. Hamrick JL, Godt MJW, Sherman-Broyles SL (1992) Factors influencing levels of genetic diversity in woody plant species. New For 6:95–124CrossRefGoogle Scholar
  45. Hardesty B, Metcalfe S, Wilcox C (2013) Genetic variability and population diversity as revealed by microsatellites for Flesh-footed Shearwaters (Puffinus carneipes) in the Southern Hemisphere. Conserv Genet Resour 5:27–29CrossRefGoogle Scholar
  46. Harrison RG (1998) Linking evolutionary pattern and process. Endless Forms 19–31Google Scholar
  47. Hasegawa M, Kishino H, Yano T-a (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174PubMedCrossRefGoogle Scholar
  48. Helbig AJ, Knox AG, Parkin DT, Sangster G, Collinson M (2002) Guidelines for assigning species rank. Ibis 144:518–525CrossRefGoogle Scholar
  49. Heller R, Chikhi L, Siegismund HR (2013) The confounding effect of population structure on Bayesian skyline plot inferences of demographic history. PloS ONE 8:e62992PubMedPubMedCentralCrossRefGoogle Scholar
  50. Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913PubMedCrossRefGoogle Scholar
  51. Hey J (2010) Isolation with migration models for more than two populations. Mol Biol Evol 27:905–920PubMedCrossRefGoogle Scholar
  52. Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760PubMedPubMedCentralCrossRefGoogle Scholar
  53. Hey J, Nielsen R (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc Natl Acad Sci USA 104:2785–2790PubMedPubMedCentralCrossRefGoogle Scholar
  54. Hindwood K (1945) The Fleshy-footed Shearwater (Puffinus carneipes). Emu 44:241–248CrossRefGoogle Scholar
  55. Hudson RR (1990) Gene genealogies and the coalescent process. Oxford Surv Evol Biol 7:44Google Scholar
  56. Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147–164PubMedPubMedCentralGoogle Scholar
  57. Ibrahim KM, Nichols RA, Hewitt GM (1996) Spatial patterns of genetic variation generated by different forms of dispersal. Heredity 77:282–291CrossRefGoogle Scholar
  58. Kidd MG, Friesen VL (1998) Sequence variation in the Guillemot (Alcidae: Cepphus) mitochondrial control region and its nuclear homolog. Mol Biol Evol 15:61–70PubMedCrossRefGoogle Scholar
  59. Kimura M (1969) The number of heterozygous nucleotide sites maintained in a finite population due to steady flux of mutations. Genetics 61:893PubMedPubMedCentralGoogle Scholar
  60. Kinsky F (1957) 7th annual report of the Ornithological Society of New Zealand Ringing Committee for the year ending 31 March 1957. Notornis 7:123–135Google Scholar
  61. Kocher TD, Thomas WK, Meyer A, Edwards SV, Pääbo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86:6196–6200PubMedPubMedCentralCrossRefGoogle Scholar
  62. Kyle C, Boulding E (2000) Comparative population genetic structure of marine gastropods (Littorina spp.) with and without pelagic larval dispersal. Mar Biol 137:835–845CrossRefGoogle Scholar
  63. Lambeck K, Yokoyama Y, Purcell T (2002) Into and out of the Last Glacial Maximum: sea-level change during Oxygen Isotope Stages 3 and 2. Quaternary Sci Rev 21:343–360CrossRefGoogle Scholar
  64. Lavers JL (2014) Population status and threats to Flesh-footed Shearwaters (Puffinus carneipes) in South and Western Australia. ICES J Mar Sci 72(2):316–327CrossRefGoogle Scholar
  65. Lavers JL, Bond AL, Van Wilgenburg SL, Hobson KA (2013) Linking at-sea mortality of a pelagic shearwater to breeding colonies of origin using biogeochemical markers. Mar Ecol-Prog Ser 491:265–275CrossRefGoogle Scholar
  66. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452PubMedCrossRefGoogle Scholar
  67. Lindsey T (1986) The seabirds of Australia. Angus & Robertson, National Photographic Index of Australian Wildlife, AustraliaGoogle Scholar
  68. Lombal AJ, Wenner TJ, Carlile N, Austin JJ, Woehler E, Priddel D, Burridge CP (2016) Population genetic and behavioural variation of the two remaining colonies of Providence petrel (Pterodroma solandri). Conserv Genet 1–13Google Scholar
  69. Marchant S, Higgins P (1990) Handbook of Australian, New Zealand and Antarctic birds. vol 1: Ratites to Ducks, Part A-Ratites to Petrels, Part B-Australian Pelican to Ducks. Oxford University Press, AustraliaGoogle Scholar
  70. Mardulyn P, Mikhailov YE, Pasteels JM (2009) Testing phylogeographic hypotheses in a Euro-Siberian cold-adapted leaf beetle with coalescent simulations. Evol Int J Org Evol 63:2717–2729CrossRefGoogle Scholar
  71. Mayr E (1942) Systematics and the origin of species, from the viewpoint of a zoologist. Harvard University Press, USAGoogle Scholar
  72. Mayr E (1963) Animal species and evolution, vol 797. Belknap Press of Harvard University Press Cambridge, USACrossRefGoogle Scholar
  73. Mayr E (1970) Populations, species, and evolution: an abridgment of animal species and evolution. Harvard University Press, USAGoogle Scholar
  74. Mayr E, Short LL (1970) Species taxa of North American birds: a contribution to comparative systematics. Harvard University Press, USAGoogle Scholar
  75. McKitrick MC, Zink RM (1988) Species concepts in ornithology. Condor 90:1–14CrossRefGoogle Scholar
  76. Mills LS, Allendorf FW (1996) The one-migrant-per-generation rule in conservation and management. Conserv Biol 10:1509–1518CrossRefGoogle Scholar
  77. Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9:373–375PubMedCrossRefGoogle Scholar
  78. Moritz C (1999) Conservation units and translocations: strategies for conserving evolutionary processes. Hereditas 130:217–228CrossRefGoogle Scholar
  79. Nei M (1987) Molecular evolutionary genetics. Columbia university Press, USAGoogle Scholar
  80. Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158:885–896PubMedPubMedCentralGoogle Scholar
  81. Nistelberger H, Gibson N, Macdonald B, Tapper S, Byrne M (2014) Phylogeographic evidence for two mesic refugia in a biodiversity hotspot. Heredity 113:454–463PubMedPubMedCentralCrossRefGoogle Scholar
  82. Nunn GB, Stanley SE (1998) Body size effects and rates of cytochrome b evolution in tube-nosed seabirds. Mol Biol Evol 15:1360–1371PubMedCrossRefGoogle Scholar
  83. Orians GH, Pearson NE (1979) On the theory of central place foraging. Analysis of Ecological Systems Ohio State University Press, Columbus, pp 155–177Google Scholar
  84. Patterson S, Morris-Pocock J, Friesen V (2011) A multilocus phylogeny of the Sulidae (Aves: Pelecaniformes). Mol Phylogenet Evol 58:181–191PubMedCrossRefGoogle Scholar
  85. Pearce JM, Talbot SL, Pierson BJ, Petersen MR, Scribner KT, Dickson DL, Mosbech A (2004) Lack of spatial genetic structure among nesting and wintering King Eiders. Condor 106:229–240CrossRefGoogle Scholar
  86. Peck DR, Congdon BC (2004) Reconciling historical processes and population structure in the sooty tern Sterna fuscata. J Avian Biol 35:327–335CrossRefGoogle Scholar
  87. Peck DR, Congdon BC (2005) Colony-specific foraging behaviour and co-ordinated divergence of chick development in the wedge-tailed shearwater Puffinus pacificus. Mar Ecol-Prog Ser 299:289–296CrossRefGoogle Scholar
  88. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808PubMedCrossRefGoogle Scholar
  89. Powell CD (2009) Foraging movements and the migration trajectory of Flesh-footed Shearwaters Puffinus carneipes from the south coast of Western Australia. Mar Ornithol 37:115–120Google Scholar
  90. Rambaut A, Suchard MA, Xie D, Drummond AJ (2015) Tracer v1. 6. 2014, Available from
  91. Rayner MJ et al (2011a) Contemporary and historical separation of transequatorial migration between genetically distinct seabird populations. Nat Commun 2:332PubMedCrossRefGoogle Scholar
  92. Rayner MJ, Taylor GA, Thompson DR, Torres LG, Sagar PM, Shaffer SA (2011b) Migration and diving activity in three non-breeding flesh-footed shearwaters Puffinus carneipes. J Avian Biol 42:266–270CrossRefGoogle Scholar
  93. Reid TA (2011) Modelling the foraging ecology of the Flesh-footed Shearwater Puffinus carneipes in relation to fisheries and oceanography. Ph.D. Thesis, University of TasmaniaGoogle Scholar
  94. Reid TA, Hindell MA, Wilcox C (2012) Environmental determinants of the at-sea distribution of encounters between Flesh-footed Shearwaters Puffinus carneipes and fishing vessels. Mar Ecol-Prog Ser 447:231–242CrossRefGoogle Scholar
  95. Reid T, Hindell M, Lavers JL, Wilcox C (2013a) Re-examining mortality sources and population trends in a declining seabird: using Bayesian methods to incorporate existing information and new data. PloS ONE 8:e58230PubMedPubMedCentralCrossRefGoogle Scholar
  96. Reid TA, Tuck GN, Hindell MA, Thalmann S, Phillips RA, Wilcox C (2013b) Nonbreeding distribution of Flesh-footed Shearwaters and the potential for overlap with north Pacific fisheries. Biol Conserv 166:3–10CrossRefGoogle Scholar
  97. Ridgway K, Dunn J (2003) Mesoscale structure of the mean East Australian Current System and its relationship with topography. Progr Oceanogr 56:189–222CrossRefGoogle Scholar
  98. Roeder AD et al (2001) Gene flow on the ice: genetic differentiation among Adélie penguin colonies around Antarctica. Mol Ecol 10:1645–1656PubMedCrossRefGoogle Scholar
  99. Roux J (1985) Status of Puffinus carneipes in Saint Paul Island (38843′S, 77830′E). L’oiseau et la Revue Francaise D’Ornithologie 55:155–157Google Scholar
  100. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90CrossRefGoogle Scholar
  101. Shaffer SA et al (2006) Migratory shearwaters integrate oceanic resources across the Pacific Ocean in an endless summer. Proc Natl Acad Sci USA 103:12799–12802PubMedPubMedCentralCrossRefGoogle Scholar
  102. Silva MC, Duarte MA, Coelho MM (2011) Anonymous nuclear loci in the White-faced Storm-Petrel Pelagodroma marina and their applicability to other Procellariiform seabirds. J Hered 102:362–365PubMedCrossRefGoogle Scholar
  103. Sites JW, Marshall JC (2004) Operational criteria for delimiting species. Annu Rev Ecol Evol Syst 35:199–227CrossRefGoogle Scholar
  104. Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–793PubMedCrossRefGoogle Scholar
  105. Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989PubMedPubMedCentralCrossRefGoogle Scholar
  106. Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460PubMedPubMedCentralGoogle Scholar
  107. Taylor GA, Unit BR (2000) Action plan for seabird conservation in New Zealand. Biodiversity Recovery Unit, Department of Conservation, New ZealandGoogle Scholar
  108. Techow N et al (2010) Speciation and phylogeography of giant petrels Macronectes. Mol Phylogenet Evol 54:472–487PubMedCrossRefGoogle Scholar
  109. Thalmann SJ, Baker GB, Hindell M, Tuck GN (2009) Longline fisheries and foraging distribution of Flesh-footed Shearwaters in Eastern Australia. J Wildl Manage 73:399–406CrossRefGoogle Scholar
  110. Tuck GN, Wilcox C (2010) Assessing the potential impacts of fishing on the Lord Howe Island population of Flesh-footed Shearwaters. CSIRO Marine and Atmospheric Research, TasmaniaGoogle Scholar
  111. Warham J (1990) The petrels: their ecology and breeding systems. A&C Black, United KingdomGoogle Scholar
  112. Waugh SM, Tennyson A, Taylor GA, Wilson K-J (2013) Population sizes of shearwaters (Puffinus spp.) breeding in New Zealand, with recommendations for monitoring. Tuhinga 24:159–204Google Scholar
  113. Waugh SM, Patrick SC, Filippi DP, Taylor GA, Arnould JP (2016) Overlap between Flesh-footed Shearwater Puffinus carneipes foraging areas and commercial fisheries in New Zealand waters. Mar Ecol-Prog Ser 551:249–260CrossRefGoogle Scholar
  114. Weir J, Schluter D (2008) Calibrating the avian molecular clock. Mol Ecol 17:2321–2328PubMedCrossRefGoogle Scholar
  115. Wiley AE et al (2012) Foraging segregation and genetic divergence between geographically proximate colonies of a highly mobile seabird. Oecologia 168:119–130PubMedCrossRefGoogle Scholar
  116. Wright S (1931) Evolution in Mendelian populations. Genetics 16:97PubMedPubMedCentralGoogle Scholar

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© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of TasmaniaHobartAustralia
  2. 2.Institute for Marine and Antarctic StudiesUniversity of TasmaniaHobartAustralia
  3. 3.Australian Centre for Ancient DNA, School of Biological SciencesUniversity of AdelaideAdelaideAustralia
  4. 4.Lord Howe Island MuseumLord Howe IslandAustralia

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