Skip to main content

Hierarchical metapopulation structure in a highly mobile marine predator: the southern Australian coastal bottlenose dolphin (Tursiops cf. australis)

Conservation Genetics volume 19, pages 637–654 (2018)Cite this article

Abstract

Little is known about the population ecology of the recently described bottlenose dolphin species Tursiops australis. The classification of this species is still under debate, but this putative species is thought to be comprised of small and genetically distinct populations (including sub-populations under increasing anthropogenic threats) and is likely endemic to coastal southern Australia. Mitochondrial DNA (mtDNA) control region sequences and microsatellite loci were used to assess genetic variation and hierarchical population structure of coastal T. cf. australis across a range of spatial scales and environmental discontinuities between southern Western Australia (WA) and central South Australia (SA). Overall, genetic diversity was similar to that typically found for bottlenose dolphins, although very low mtDNA diversity was found in Gulf St. Vincent (GSV) dolphins. We found historical genetic subdivision and likely differences in colonisation between GSV and Spencer Gulf, outer- and inner-gulf locations, and SA/WA and previously identified Victorian/Tasmanian populations. A hierarchical metapopulation structure was revealed along southern Australia, with at least six genetic populations occurring between Esperance, WA and southern Tasmania. In addition, fine-scale genetic subdivision was observed within each SA/WA population. In general, contemporary migration was limited throughout southern Australia, but an important gene flow pathway was identified eastward along the Great Australian Bight. Management strategies that promote gene flow among populations should be implemented to assist with the maintenance of the inferred metapopulation structure. Further research into the population ecology of this species is needed to facilitate well-informed management decisions.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Amaral AR, Beheregaray LB, Bilgmann K, Boutov D, Freitas L, Robertson KM, Sequeira M, Stockin KA, Coelho MM, Möller LM (2012) Seascape genetics of a globally distributed, highly mobile marine mammal: the short-beaked common dolphin (genus Delphinus). PLoS ONE 7:e31482

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ansmann IC, Parra GJ, Lanyon JM, Seddon JM (2012) Fine-scale genetic population structure in a mobile marine mammal: inshore bottlenose dolphins in Moreton Bay, Australia. Mol Ecol 21:4472–4485. https://doi.org/10.1111/j.1365-294X.2012.05722.x

    Article  PubMed  Google Scholar 

  • Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  PubMed  CAS  Google Scholar 

  • Beerli P (2004) Effect of unsampled populations on the estimation of population sizes and migration rates between sampled populations. Mol Ecol 13:827–836

    Article  PubMed  Google Scholar 

  • Belperio A, Harvey N, Bourman R (2002) Spatial and temporal variability in the Holocene sea-level record of the South Australian coastline. Sediment Geol 150:153–169

    Article  Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188

    Article  Google Scholar 

  • Bilgmann K, Möller L, Harcourt R, Gibbs S, Beheregaray L (2007a) Genetic differentiation in bottlenose dolphins from South Australia: association with local oceanography and coastal geography. Mar Ecol Prog Ser 341:265–276

    Article  CAS  Google Scholar 

  • Bilgmann K, Griffiths O, Allen S, Möller L (2007b) A biopsy pole system for bow-riding dolphins: sampling success, behavioral responses, and test for sampling bias. Mar Mam Sci 23:218–225. https://doi.org/10.1111/j.1748-7692.2006.00099.x

    Article  Google Scholar 

  • Bilgmann K, Möller LM, Harcourt RG, Gales R, Beheregaray LB (2008) Common dolphins subject to fisheries impacts in southern Australia are genetically differentiated: implications for conservation. Anim Conserv 11:518–528. https://doi.org/10.1111/j.1469-1795.2008.00213.x

    Article  Google Scholar 

  • Bilgmann K, Parra G, Zanardo N, Beheregaray L, Möller L (2014) Multiple management units of short-beaked common dolphins subject to fisheries bycatch off southern and southeastern Australia. Mar Ecol Prog Ser 500:265–279

    Article  Google Scholar 

  • Bird C, Karl S, Smouse P, Toonen R (2011) Detecting and measuring genetic differentiation. CrustIssues 19(3):31–55

    Google Scholar 

  • Boyd IL (2004) Migration of marine mammals. Springer, Berlin

    Book  Google Scholar 

  • Caballero S, Santos MCD, Sanches A, Mignucci-Giannoni AA (2013) Initial description of the phylogeography, population structure and genetic diversity of Atlantic spotted dolphins from Brazil and the Caribbean, inferred from analyses of mitochondrial and nuclear DNA. Biochem Syst Ecol 48:263–270. https://doi.org/10.1016/j.bse.2012.12.016

    Article  CAS  Google Scholar 

  • Cann JH, Belperio AP, Gostin VA, Murraywallace CV (1988) Sea-level history, 45,000 to 30,000 year BP, inferred from benthic foraminifera, Gulf St. Vincent, South Australia. Quat Res 29:153–175. https://doi.org/10.1016/0033-5894(88)90058-0

    Article  Google Scholar 

  • Charlton K, Taylor A, McKechnie SW (2006) A note on divergent mtDNA lineages of bottlenose dolphins from coastal waters of southern Australia. J Cetacean Res Manag 8:173

    Google Scholar 

  • Charlton-Robb K, Gershwin L, Thompson R, Austin J, Owen K, McKechnie S (2011) A new dolphin species, the Burrunan dolphin Tursiops australis sp. nov., endemic to southern Australian coastal waters. PLoS ONE 6:e24047. https://doi.org/10.1371/journal.pone.0024047

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Charlton-Robb K, Taylor A, McKechnie S (2015) Population genetic structure of the Burrunan dolphin (Tursiops australis) in coastal waters of south-eastern Australia: conservation implications. Conserv Genet 16:195–207. https://doi.org/10.1007/s10592-014-0652-6

    Article  Google Scholar 

  • Chevron Australia (2016) Great Australian bight—Chevron’s exploration activities (Online). https://www.chevronaustralia.com/our-businesses/exploration/great-australian-bight. Accessed 23rd Nov 2016

  • Cirano M, Middleton JF (2004) Aspects of the mean wintertime circulation along Australia’s southern shelves: Numerical studies. J Phys Oceanogr 34:668–684. https://doi.org/10.1175/2509.1

    Article  Google Scholar 

  • DEH (Department of Environment and Heritage) (2006) ‘Map 2 IMCRA 4.0: Meso-scale Bioregions’, Australian Government Data Sources

  • DEWNR (Department of Environment Water and Natural Resources) (2014) Recreational fishing in SA marine parks. Government of South Australia, Adelaide

    Google Scholar 

  • DEWNR (Department of Environment, Water and Natural Resources) (2012) Upper Gulf St. Vincent Marine Park Management Plan. Government of South Australia, Adelaide

    Google Scholar 

  • DeWoody JA, Bickham JW, Michler CH, Nichols KM, Rhodes GE, Woeste KE (2010) Molecular approaches in natural resource conservation and management. Cambridge University Press, New York

    Book  Google Scholar 

  • Dowling TE, Brown WM (1993) Population structure of the bottlenose dolphin (Tursiops truncatus) as determined by restriction endonuclease analysis of mitochondrial DNA. Mar Mam Sci 9:138–155. https://doi.org/10.1111/j.1748-7692.1993.tb00439.x

    Article  Google Scholar 

  • Earl D, vonHoldt B (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7

    Article  Google Scholar 

  • ELWP (Department of Environment, Land, Water and Planning) (2016a) Marine National Parks (Online). Victoria State government. http://www.depi.vic.gov.au/forestry-and-land-use/coasts/marine/marine-national-parks/marine-national-parks. Accessed 19 Jan 2017

  • ELWP (Department of Environment, Land, Water and Planning) (2016b) Marine sanctuaries (Online). Victoria State government. http://www.depi.vic.gov.au/forestry-and-land-use/coasts/marine/marine-national-parks/marine-sanctuaries. Accessed 19 Jan 2017

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Lischer H (2010) Arlequin suite ver3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

  • Filby N, Stockin K, Scarpaci C (2014) Long-term responses of Burrunan dolphins (Tursiops australis) to swim-with dolphin tourism in Port Phillip Bay, Victoria, Australia: a population at risk. Global Ecol Conserv 2:62–71

    Article  Google Scholar 

  • Frankham R (1995) Conservation genetics. Annu Rev Genet 29:305–327. https://doi.org/10.1146/annurev.ge.29.120195.001513

    Article  PubMed  CAS  Google Scholar 

  • Fruet PF, Secchi ER, Daura-Jorge F, Vermeulen E, Flores PA, Simoes-Lopes PC, Genoves RC, Laporta P, Di Tullio JC, Freitas TRO (2014) Remarkably low genetic diversity and strong population structure in common bottlenose dolphins (Tursiops truncatus) from coastal waters of the Southwestern Atlantic Ocean. Conserv Genet 15:879–895

    Google Scholar 

  • Gaggiotti O, Lange O, Rassmann K, Gliddon C (1999) A comparison of two indirect methods for estimating average levels of gene flow using microsatellite data. Mol Ecol 8(9):1513–1520

    Article  PubMed  CAS  Google Scholar 

  • Gibbs S, Harcourt R, Kemper C (2011) Niche differentiation of bottlenose dolphin species in South Australia revealed by stable isotopes and stomach contents. Wildl Res 38:261–270

    Article  CAS  Google Scholar 

  • Gilson A, Syvanen M, Levine K, Banks J (1998) Deer gender determination by polymerase chain reaction: validation study and application to tissues, bloodstains, and hair forensic samples from California. Calif Fish Game 84(4):159–169

    Google Scholar 

  • Google Earth 6.2.1.6014 (2012) Southern Australia coastline. Places data layer. http://www.google.com/earth/index.html. Accessed 02 Nov 2015

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices, Ver 2.9.3. http://www.unil.ch/popgen/softwares/fstat.html

  • Hanski I (1998) Metapopulation dynamics. Nature 396:41–49

    Article  CAS  Google Scholar 

  • Hanski I, Gilpin M (1991) Metapopulation dynamics: brief histroy and conceptual domain. Biol J Linnean Soc 42:3–16

    Article  Google Scholar 

  • Harvey N (2006) Holocene coastal evolution: barriers, beach ridges, and tidal flats of South Australia. J Coast Res 22:90–99. https://doi.org/10.2112/05a-0008.1

    Article  Google Scholar 

  • Hedrick PW (2001) Conservation genetics: where are we now? Trends Ecol Evol 16:629–636. https://doi.org/10.1016/s0169-5347(01)02282-0

    Article  Google Scholar 

  • Hoelzel A, Potter C, Best P (1998) Genetic differentiation between parapatric ‘nearshore’ and ‘offshore’ populations of the bottlenose dolphins. J R Soc 265:1177–1183

    CAS  Google Scholar 

  • Holmes L (2011) Relative abundance of the southern Australian bottlenose dolphin Tursiops australis within the South Australian Gulfs. Honours thesis, Flinders University, Adelaide

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332. https://doi.org/10.1111/j.1755-0998.2009.02591.x

    Article  PubMed  PubMed Central  Google Scholar 

  • Jensen J, Bohonak A, Kelley S (2005) Isolation by distance, web service v.3.23. BMC Genet 6:13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jombart T, Ahmed I (2011) Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94

    Article  PubMed  PubMed Central  Google Scholar 

  • Jost L (2008) G(ST) and its relatives do not measure differentiation. Mol Ecol 17:4015–4026. https://doi.org/10.1111/j.1365-294X.2008.03887.x

    Article  PubMed  Google Scholar 

  • Kämpf J, Payne N, Malthouse P (2010) Marine connectivity in a large inverse estuary. J Coast Res 26:1047–1056. https://doi.org/10.2112/jcoastres-d-10-00043.1

    Article  Google Scholar 

  • Keenan K, McGinnity P, Cross TF, Crozier WW, Prodöhl PA (2013) Diversity: an R package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol Evol 4:782–788. https://doi.org/10.1111/2041-210X.12067

    Article  Google Scholar 

  • Kemper C, Tomo I, Bingham J, Bastianello S, Wang J, Gibbs S, Woolford L, Dickason C, Kelly D (2016) Morbillivirus-associated unusual mortality event in South Australian bottlenose dolphins is largest reported for the Southern Hemisphere. R Soc Open Sci 3:160838

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kompelman N, Mayzel J, Jakobsson M, Rosenberg N, Maryrose I (2015) CLUMPAK: a program for identifying clustering models and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191. https://doi.org/10.1111/1755-0998.12387

    Article  CAS  Google Scholar 

  • Krützen M, Barre L, Möller L, Heithaus M, Simms C, Sherwin W (2002) A biopsy system for small cetaceans: darting success and wound healing in Tursiops spp. Mar Mam Sci 18:863–878

    Article  Google Scholar 

  • Krützen M, Sherwin W, Berggren P, Gales N (2004) Population structure in an inshore cetacean revealed by microsatellite and mtDNA analysis: bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia. Mar Mam Sci 20:28–47. https://doi.org/10.1016/j.quascirev.2012.09.006

    Article  Google Scholar 

  • Louis M, Viricel A, Lucas T, Peltier H, Alfonsi E, Berrow S, Brownlow A, Covelo P, Dabin W, Deaville R (2014) Habitat-driven population structure of bottlenose dolphins, Tursiops truncatus, in the North-East Atlantic. Mol Ecol 23(4):857–874

    Article  PubMed  Google Scholar 

  • Lowther-Thieleking J, Archer F, Lang A, Weller D (2015) Genetic differentiation among coastal and offshore common bottlenose dolphins, Tursiops truncatus, in the eastern North Pacific Ocean. Mar Mam Sci 31:1–20

    Article  Google Scholar 

  • Magera AM, Flemming JEM, Kaschner K, Christensen LB, Lotze HK (2013) Recovery trends in marine mammal populations. PLoS ONE 8:12. https://doi.org/10.1371/journal.pone.0077908

    Article  CAS  Google Scholar 

  • Mead J, Potter C (1995) Recognizing two populations of the bottlenose dolphin (Tursiops truncatus) off the coast of North America: morphologic and ecological considerations. IBI Rep 5:3144

    Google Scholar 

  • Meirmans P (2012) The trouble with isolation by distance. 21:2839–2846

  • Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794. https://doi.org/10.1111/j.1471-8286.2004.00770.x

    Article  Google Scholar 

  • 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 19:2212–2228

    Article  PubMed  CAS  Google Scholar 

  • Middleton JF, Bye JAT (2007) A review of the shelf-slope circulation along Australia’s southern shelves: Cape Leeuwin to Portland. Prog Oceanogr 75:1–41. https://doi.org/10.1016/j.pocean.2007.07.001

    Article  Google Scholar 

  • Möller L (2011) Sociogenetic structure, kin associations and bonding in delphinids. Mol Ecol 21:745–764. https://doi.org/10.1111/j.1365-294X.2011.05405.x

    Article  PubMed  Google Scholar 

  • Möller LM, Beheregaray LB (2004) Genetic evidence for sex-biased dispersal in resident bottlenose dolphins (Tursiops aduncus). Mol Ecol 13:1607–1612. https://doi.org/10.1111/j.1365-294X.2004.02137.x

    Article  PubMed  CAS  Google Scholar 

  • Möller L, Beheregaray L, Harcourt R, Krützen M (2001) Alliance membership and kinship in wild male bottlenose dolphins (Tursiops aduncus) southeastern Australia. J R Soc 268:1941–1947

    Google Scholar 

  • Möller L, Wiszniewski J, Allen S, Beheregaray L (2007) Habitat type promotes rapid and extremely localised genetic differentiation in dolphins. Mar Freshw Res 58:640–648

    Article  Google Scholar 

  • Möller L, Bilgmann K, Charlton-Robb K, Beheregaray L (2008) Multi-gene evidence for a new bottlenose dolphin species in southern Australia. Mol Phylogenet Evol 49:674–681

    Article  PubMed  CAS  Google Scholar 

  • Möller L, Valdez F, Allen S, Bilgmann K, Corrigan S, Beheregaray L (2011) Fine-scale genetic structure in short-beaked common dolphins (Delphinus delphis) along the East Australian Current. Mar Biol 158:113–126

    Article  Google Scholar 

  • Monk A, Charlton-Robb K, Buddhadasa S, Thompson RM (2014) Comparison of mercury contamination in live and dead dolphins from a newly described species, Tursiops australis. PLoS ONE 9:6. https://doi.org/10.1371/journal.pone.0104887

    Article  CAS  Google Scholar 

  • Moura AE, Natoli A, Rogan E, Hoelzel AR (2013) Atypical panmixia in a European dolphin species (Delphinus delphis): implications for the evolution of diversity across oceanic boundaries. J Evol Biol 26:63–75. https://doi.org/10.1111/jeb.12032

    Article  PubMed  CAS  Google Scholar 

  • Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787

    Article  CAS  Google Scholar 

  • Natoli A, Birkun A, Lopez A, Hoelzel A (2005) Habitat structure and the dispersal of male and female bottlenose dolphins (Tursiops truncatus). J R Soc 272:1217–1226

    CAS  Google Scholar 

  • Palsbøll PJ, Berube M, Allendorf FW (2007) Identification of management units using population genetic data. Trends Ecol Evol 22:11–16

    Article  PubMed  Google Scholar 

  • Parks and Wildlife (2017) Marine parks and reserves (Online). Government of Western Australia. https://www.dpaw.wa.gov.au/management/marine/marine-parks-and-reserves. Accessed 19 Jan 2017

  • Passadore C, Möller L, Diaz-Aguirre F, Parra GJ (2017) Demography of southern Australian bottlenose dolphins living in a protected inverse estuary. Aquat Conserv 1:1–12

    Google Scholar 

  • Payne NL, Snelling EP, Semmens JM, Gillanders BM (2013) Mechanisms of population structuring in giant Australian cuttlefish Sepia apama. PLoS ONE 8:7. https://doi.org/10.1371/journal.pone.0058694

    Article  CAS  Google Scholar 

  • Peakall R, Smouse P (2006) GENALEX 6: gentic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peakall R, Smouse P (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Perez-Alvarez MJ, Olavarria C, Moraga R, Baker CS, Hamner RM, Poulin E (2015) Microsatellite markers reveal strong genetic structure in the endemic Chilean dolphin. PLoS ONE 10:e0123956. https://doi.org/10.1371/journal.pone.0123956

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    Article  PubMed  Google Scholar 

  • Querouil S, Silva MA, Freitas L, Prieto R, Magalhaes S, Dinis A, Alves F, Matos JA, Mendonca D, Hammond PS, Santos RS (2007) High gene flow in oceanic bottlenose dolphins (Tursiops truncatus) of the North Atlantic. Conserv Genet 8:1405–1419. https://doi.org/10.1007/s10592-007-9291-5

    Article  CAS  Google Scholar 

  • Querouil S, Freitas L, Cascao I, Alves F, Dinis A, Almeida JR, Prieto R, Borras S, Matos JA, Mendonca D, Santos RS (2010) Molecular insight into the population structure of common and spotted dolphins inhabiting the pelagic waters of the Northeast Atlantic. Mar Biol 157:2567–2580. https://doi.org/10.1007/s00227-010-1519-0

    Article  Google Scholar 

  • Rannala B (2007) BayesAss esition 3.0 user’s manual. University of California, Davis

    Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism1. J Hered 86:248–249

    Article  Google Scholar 

  • Roberts S, Dixon C, Andreacchio L (2012) Temperature dependent larval duration and survival of the western king prawn, Penaeus (Melicertus) latisulcatus Kishinouye, from Spencer Gulf, South Australia. J Exp Mar Biol Ecol 411:14–22. https://doi.org/10.1016/j.jembe.2011.10.022

    Article  Google Scholar 

  • Rosel PE, Hansen L, Hohn AA (2009) Restricted dispersal in a continuously distributed marine species: common bottlenose dolphins Tursiops truncatus in coastal waters of the western North Atlantic. Mol Ecol 18(24):5030–5045

    Article  PubMed  CAS  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Schipper J, Chanson JS, Chiozza F, Cox NA, Hoffmann M, Katariya V, Lamoreux J, Rodrigues ASL, Stuart SN, Temple HJ, Baillie J, Boitani L, Lacher TE, Mittermeier RA, Smith AT, Absolon D, Aguiar JM, Amori G, Bakkour N, Baldi R, Berridge RJ, Bielby J, Black PA, Blanc JJ, Brooks TM, Burton JA, Butynski TM, Catullo G, Chapman R, Cokeliss Z, Collen B, Conroy J, Cooke JG, da Fonseca GAB, Derocher AE, Dublin HT, Duckworth JW, Emmons L, Emslie RH, Festa-Bianchet M, Foster M, Foster S, Garshelis DL, Gates C, Gimenez-Dixon M, Gonzalez S, Gonzalez-Maya JF, Good TC, Hammerson G, Hammond PS, Happold D, Happold M, Hare J, Harris RB, Hawkins CE, Haywood M, Heaney LR, Hedges S, Helgen KM, Hilton-Taylor C, Hussain SA, Ishii N, Jefferson TA, Jenkins RKB, Johnston CH, Keith M, Kingdon J, Knox DH, Kovacs KM, Langhammer P, Leus K, Lewison R, Lichtenstein G, Lowry LF, Macavoy Z, Mace GM, Mallon DP, Masi M, McKnight MW, Medellin RA, Medici P, Mills G, Moehlman PD, Molur S, Mora A, Nowell K, Oates JF, Olech W, Oliver WRL, Oprea M, Patterson BD, Perrin WF, Polidoro BA, Pollock C, Powel A, Protas Y, Racey P, Ragle J, Ramani P, Rathbun G, Reeves RR, Reilly SB, Reynolds JE, Rondinini C, Rosell-Ambal RG, Rulli M, Rylands AB, Savini S, Schank CJ, Sechrest W, Self-Sullivan C, Shoemaker A, Sillero-Zubiri C, De Silva N, Smith DE, Srinivasulu C, Stephenson PJ, van Strien N, Talukdar BK, Taylor BL, Timmins R, Tirira DG, Tognelli MF, Tsytsulina K, Veiga LM, Vie JC, Williamson EA, Wyatt SA, Xie Y, Young BE (2008) The status of the world’s land and marine mammals: diversity, threat, and knowledge. Science 322:225–230. https://doi.org/10.1126/science.1165115

    Article  PubMed  CAS  Google Scholar 

  • Scientific Working Group (2011) The vulnerability of coastal and marine habitats in South Australia. Marine Parks: Department of Environment, Water and Natural Resources, Government of South Australia, Adelaide

    Google Scholar 

  • Sellas AB, Wells RS, Rosel PE (2005) Mitochondrial and nuclear DNA analyses reveal fine scale geographic structure in bottlenose dolphins (Tursiops truncatus) in the Gulf of Mexico. Conserv Genet 6:715–728. https://doi.org/10.1007/s10592-005-9031-7

    Article  CAS  Google Scholar 

  • Seuront L, Cribb N (2011) Fractal analysis reveals pernicious stress levels related to boat presence and type in the Indo-Pacific bottlenose dolphin, Tursiops aduncus. Phys A 390:2333–2339. https://doi.org/10.1016/j.physa.2011.02.015

    Article  CAS  Google Scholar 

  • Silva MA, Prieto R, Magalhaes S, Seabra M, Santos R, Hammond P (2008) Ranging patterns of bottlenose dolphins living in oceanic waters: implications for population structure. Mar Biol 156:179–192. https://doi.org/10.1007/s00227-008-1075-z

    Article  Google Scholar 

  • Slatkin M (2005) Seeing ghosts: the effect of unsampled populations on migration rates estimated for sampled populations. Mol Ecol 14:67–73

    Article  PubMed  Google Scholar 

  • Sunnucks P, Hales DF (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol Biol Evol 13:510–524

    Article  PubMed  CAS  Google Scholar 

  • Svane I (2005) Occurrence of dolphins and seabirds and their consumption of by-catch during prawn trawling in Spencer Gulf, South Australia. Fish Res 76:317–327. https://doi.org/10.1016/j.fishres.2005.07.012

    Article  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial-DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    PubMed  CAS  Google Scholar 

  • Tsai Y, Mann J (2012) Dispersal, philopatry, and the role of fission-fusion dynamics in bottlenose dolphins. Mar Mam Sci. https://doi.org/10.1111/j.1748-7692.2011.00559.x

    Article  Google Scholar 

  • Van Oosterhout C, Hutchinson W, Wills D, Shipley P (2004) MICROCHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  CAS  Google Scholar 

  • Viricel A, Rosel PE (2014) Hierarchical population structure and habitat differences in a highly mobile marine species: the Atlantic spotted dolphin. Mol Ecol 23:5018–5035. https://doi.org/10.1111/mec.12923

    Article  PubMed  Google Scholar 

  • Waters JM, Roy MS (2003) Marine biogeography of southern Australia: phylogeographical structure in a temperate sea-star. J Biogeogr 30:1787–1796

    Article  Google Scholar 

  • Wilson G, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

    PubMed  PubMed Central  Google Scholar 

  • Wiszniewski J, Beheregaray L, Allen S, Möller L (2010) Environmental and social influences on the genetic structure of bottlenose dolphins (Tursiops aduncus) in southeastern Australia. Conserv Genet 11:1405–1419

    Article  Google Scholar 

  • Zanardo N, Parra GJ, Möller LM (2016) Site fidelity, residency, and abundance of bottlenose dolphins (Tursiops sp.) in Adelaide’s coastal waters, South Australia. Mar Mam Sci 32(4):1381–1401

    Article  Google Scholar 

Download references

Acknowledgements

Flinders University, the Department of Environment, Water and Natural Resources (DEWNR), ANZ, Equity Trustees (Holsworth Wildlife Research Endowment), the Nature Foundation of South Australia, the Field Naturalists Society of South Australia, and the Biological Society of South Australia provided monetary contributions to this project, and those of PhD students, Nikki Zanardo (Adelaide metropolitan coast) and Fernando Diaz-Aguirre (Coffin Bay). This study was also partially funded by the Australian Research Council (DP110101275 to Luciano Beheregaray, Luciana Möller and Jonathan Waters, and FT130101068 to Luciano Beheregaray). Fieldwork was conducted with Ministerial Exemption from Primary Industries Resources South Australia (PIRSA), exemptions #9902648, #9902714 and #9902601, with permits #K25761-6 and #E26171 from the Department of Environment, Water and Natural Resources (DEWNR), South Australia, and with permit from the Department of Environment and Conservation, WA (#SF008961). Animal ethics approvals were acquired from the Flinders University Animal Welfare Committee, projects #E310, #E375 and #E326. The present article is publication #65 of the Molecular Ecology Group for Marine Research (MEGMAR).

Author information

Authors and Affiliations

  1. Molecular Ecology Laboratory, College of Science and Engineering, Flinders University, Bedford Park, SA, 5042, Australia

    Eleanor A. L. Pratt, Luciano B. Beheregaray, Kerstin Bilgmann, Nikki Zanardo, Fernando Diaz-Aguirre & Luciana M. Möller

  2. Cetacean Ecology, Behaviour and Evolution Laboratory, College of Science and Engineering, Flinders University, Bedford Park, SA, 5042, Australia

    Eleanor A. L. Pratt, Kerstin Bilgmann, Nikki Zanardo, Fernando Diaz-Aguirre & Luciana M. Möller

  3. Department of Biological Sciences, Faculty of Science and Engineering, Macquarie University, Sydney, NSW, 2109, Australia

    Kerstin Bilgmann

Authors
  1. Eleanor A. L. Pratt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luciano B. Beheregaray
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kerstin Bilgmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nikki Zanardo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fernando Diaz-Aguirre
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Luciana M. Möller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luciana M. Möller.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 2262 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Pratt, E.A.L., Beheregaray, L.B., Bilgmann, K. et al. Hierarchical metapopulation structure in a highly mobile marine predator: the southern Australian coastal bottlenose dolphin (Tursiops cf. australis). Conserv Genet 19, 637–654 (2018). https://doi.org/10.1007/s10592-017-1043-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-017-1043-6

Keywords

  • Tursiops australis
  • Conservation genetics
  • Phylogeography
  • Management units
  • Gene flow
  • Cetacean