Skip to main content
Springer Nature Link
Log in

Morphological and genetic evidence for two evolutionarily significant units (ESUs) in the South American fur seal, Arctocephalus gazella

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

The South American fur seal (Arctocephalus australis) is widely distributed, occurring along both the Atlantic and the Pacific coasts of South America. Previous work suggests there may be more than one subspecies, highlighting the need for further study. Here, we combine traditional and geometric morphometric analysis of skull shape and size with genetic data to compare two populations of South American fur seals, one from Uruguay and one from Peru. As a control group we used material from the closely related species Arctocephalus gazella. Both techniques of morphometric analysis reveal pronounced geographic variation in size and shape of the skull, with Peruvian specimens (n = 102) being larger than Uruguayan skulls (n = 133) and significant shape differences concentrated in the rostral region. Similarly, seven highly polymorphic microsatellite loci reveal highly significant differences in allele frequency. Moreover, Bayesian analysis implemented using the program structure reveals two separate clusters corresponding perfectly to the two populations, with an assignment test correctly placing over 98% of specimens in their population of origin. This degree of differentiation for both genetic and morphological traits suggests complete and possibly prolonged isolation to the extent that we believe these populations should be considered distinct evolutionarily significant units.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Allen PJ, Amos W, Pomery PP, Twiss SD (1995) Microsatellite variation in grey seals (Halichoerus grypus) shows evidence of genetic differentiation between two British breeding colonies. Mol Ecol 4:653–662

    Article  PubMed  CAS  Google Scholar 

  • Amos W, Hoelzel AR (1991) Long-term preservation of whale skin for DNA analysis, In: Hoelzel AR (ed) Genetic ecology of whales and dolphins. IWC, special issue 13, Cambridge, pp 99–103

  • Arias-Schreiber M, Rivas C (1998) Distribución, tamaño y estructura de las poblaciones de lobos marinos Arctocephalus australis y Otaria byronia en el litoral Peruano, en Noviembre 1996 y Marzo 1997. Informe Progresivo del Instituto del Mar del Perú 73:17–32. Callao, Peru

  • Avise JC (1989) A role for molecular geneticists in the recognition and conservation of endangered species. TREE 4:279–281

    Google Scholar 

  • Avise JC, Ball RM Jr (1990) Principles of genealogical concordance in species concepts and biological taxonomy. Oxford Surveys Evol Biol 7:45–67

    Google Scholar 

  • Bottin L, Tassin J, Nasi R, Bouvet J (2007) Molecular, quantitative and abiotic variables for the delineation of evolutionary significant units: case of sandalwood (Santalum austrocaledonicum Vieillard) in New Caledonia. Cons Gen 8:99–109

    Article  Google Scholar 

  • Bookstein FL (1984) A statistical method for biological shape comparisons. J Theor Biol 107:475–520

    Article  PubMed  CAS  Google Scholar 

  • Bookstei FL (1989) Size and shape: a comment on semantics. Syst Zool 38:173–180

    Article  Google Scholar 

  • Bookstein FL (1991) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, New York

    Google Scholar 

  • Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5:453–455

    Article  PubMed  CAS  Google Scholar 

  • Brunner S (2000) Cranial Morphometrics of fur seals and sea lions (Family: Otariidae) – systematics, geographic variation and growth. PhD thesis, University of Sydney

  • Brunner S (2004) Fur seals and sea lions (Otariidae): identification of species and taxonomic review. Syst Biod 1:339–439

    Article  Google Scholar 

  • Cane MA (1983) Oceanographic events during El Niño. Science 22:1189–1195

    Article  Google Scholar 

  • Cappozzo HL, Perez F, Batalles LM (1996) Reproductive behavior of South American fur seals in Uruguay. Paper presented at the International Symposium and workshop on Otariid reproductive strategies and conservation, Smithsonian Institution, Washington, 12–16 April 1996, p 37

  • Carvalho CT (1975) Ocorrência de mamíferos marinhos no Brasil. Boletim Técnico do Instituto Florestal 16:13–32

    Google Scholar 

  • Chan C, Ballantyne KN, Aikman H, Fastier D, Daugherty CH, Chambers GK (2006) Genetic analysis of interspecific hybridisation in the world’s only Forbes’ parakeet (Cyanoramphus forbesi) natural population. Cons Gen 7(4):493–506

    Article  CAS  Google Scholar 

  • Coltman DW, Bowen WD, Wright JM (1996) PCR primers for harbour seal (Phoca vitulina concolor) microsatellites amplify polymorphic loci in other species. Mol Ecol 5:161–163

    Article  PubMed  CAS  Google Scholar 

  • Cracraft J (1983) Species concepts and speciation analysis. In: Johnson RF (ed) Current ornithology. Plenum Press, New York, pp 159–187

  • Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. TREE 15:290–295

    PubMed  Google Scholar 

  • Daneri GA, Garcia Esponda CM, De Santis LJM (1997) A record of Arctocephalus australis (Zimmermann, 1783) (Carnivora, Otariidae) south of the Antarctic Convergence. Mammalia 61(3):451–454

    Google Scholar 

  • Demére TA, Berta A, Peter JA (2003) Pinnipedimorph evolutionary biogeography. Bull Am Mus Nat His 279:32–76

    Article  Google Scholar 

  • Drehmer CJ, Ferigolo J (1997) Osteologia cranianacomparada entre Arctocephalus australis e A. tropicalis (Pinnipedia, Otariidae). Iheringia. Série Zoologia 83:137–149

    Google Scholar 

  • Ellner S, Hairston NG Jr (1994) Role of overlapping generations in maintaining genetic variation in a fluctuating environment. The Am Nat 143:403–417

    Article  Google Scholar 

  • Encalada SE, Lahanas PH, Bjorndal KA, Bolten AB, Miyamoto MM, Bowen BW (1996) Phylogeography and population structure of the green turtle (Chelonia mydas) in the Atlantic Ocean and Mediterranean Sea: a mitochondrial DNA control region sequence assessment. Mol Ecol 5:473–484

    Article  PubMed  CAS  Google Scholar 

  • Fabiani A, Hoelzel AR, Galimberti F, Muelbert MMC (2003) Long-range paternal gene flow in the Southern Elephant Seal. Science 299:676

    Article  PubMed  Google Scholar 

  • Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752

    PubMed  CAS  Google Scholar 

  • Gaggiotti OE, Vetter RD (1999) Effect of life history strategy, environmental variability, and overexploitation on the genetic. Can J Fish Aquat Sci 56:1376–1388

    Article  Google Scholar 

  • Glantz MH (1996) Currents of change—El Niño’s impact on climate and society. Cambridge University Press, Cambridge

    Google Scholar 

  • Goldsworthy SD, Boness DJ, Fleischer RC (1999) Mate choice among sympatric fur seals: female preference for conphenotypic males. Behav Ecol Sociobiol 45:253–267

    Article  Google Scholar 

  • Goodman SJ (1998) Patterns of extensive genetic differentiation and variation among European harbour seals (Phoca vitulina vitulina) revealed using microsatellite DNA polymorphisms. Mol Biol Evol 15:104–118

    PubMed  CAS  Google Scholar 

  • Guerra CC, Torres DN (1987) Presence of South American fur seal, Arctcephalus australis, in northern Chile. In: Croxall JP, Gentry RL (eds) Status, biology and ecology of fur seals. Proceedings of an international symposium and workshop, United Kingdom, 23–27 April 1984, pp 169–176

  • Guo SW, Thompson EA (1992) Performing the exact test for Hardy–Weimberg proportion for multiple alleles. Biometrics 48:361–372

    Article  PubMed  CAS  Google Scholar 

  • Hedrick PW, Lee RN, Hurt CR (2006) The endangered Sonoran topminnow: examination of species and ESUs using three mtDNA genes. Cons Gen 7(4):483–492

    Article  CAS  Google Scholar 

  • Hingst-Zaher E, Marcus LF, Cerqueira R (2000) Application of geometric morphometrics to the study of postnatal size and shape changes in the skull of Callomys expulsus. Hystrix 11:99–114

    Google Scholar 

  • Hochberg Y (1988) A sharper Bonferroni procedure for multiple tests of sign. Biometrika 75:800–802

    Article  Google Scholar 

  • Hoelzel AR, LeBouef BJ, Campagna C, Reiter J (1999) Alpha male paternity in elephant seals. Behav Ecol Sociobiol 46:298–306

    Article  Google Scholar 

  • Hoelzel AR, Campagna C, Arnbom T (2000) Genetic and morphometric differentiation between island and mainland southern elephant seal populations. Proc Royal Soc Lond Ser B 268:325–332

    Article  Google Scholar 

  • Hoffman JI, Boyd IL, Amos W (2003) Male reproductive strategy and the importance of maternal status in the Antarctic fur seal Arctocephalus gazella. Evolution 57:1917–1930

    PubMed  Google Scholar 

  • Hoffman JI, Amos W (2005) Microsatellite genotyping errors: detection approaches, common sources and consequences for paternal exclusion. Mol Ecol 14:599–612

    Article  PubMed  CAS  Google Scholar 

  • Hoffman JI, Matson CW, Amos W, Loughlin TR, Bickham JW (2006) Deep genetic subdivision within a continuously distributed and highly vagile marine mammal, the Steller’s sea lion (Eumetopias jubatus). Mol Ecol 15:2821–2832

    Article  PubMed  CAS  Google Scholar 

  • Karl SA, Bowen BW (1999) Evolutionary significant units versus geopolitical taxonomy: molecular systematics of an endangered species. Cons Biol 13:990–999

    Article  Google Scholar 

  • Kerley GIH, Robinson TJ (1987) Skull morphometrics of male Antarctic and Subantarctic fur seals, Arctocephalus gazella and A. tropicalis, and their interspecific hybrids, In: Croxall JP, Gentry RL (eds) Status, biology and ecology of fur seals. Proceedings of an international symposium and workshop, Cambridge, United Kingdom, 23–27 April 1984, pp 121–131

  • King JE (1954) The otariid seals of the Pacific Coast of America. Bull Brit Mus (Natural History) 2:309–337

    Google Scholar 

  • Lancaster ML, Gemmell NJ, Negro S, Goldsworthy S, Sunnucks P (2006) Ménage à trois on Macquarie Island: hybridization among three species of fur seal (Arctocephalus spp.) following historical population extinction. Mol Ecol 15:3681–3692

    Article  PubMed  CAS  Google Scholar 

  • Lima M, Páez E (1995) Growth and reproductive patterns in the South American fur seal. J Mamm 76:1249–1255

    Article  Google Scholar 

  • Limberger D, Trillmich F, Kooyman GL, Majluf P (1983) Reproductive failure of fur seals in Galapagos and Peru in 1982–1983. Tropical Ocean-Atmosphere Newsletter 21:16–17

    Google Scholar 

  • Majluf P (1987) South American fur seal, Arctocephalus australis, in Peru. In: Croxall, JP, Gentry RL (eds) Status, biology and ecology of fur seals. Proceedings of an international symposium and workshop, Cambridge, United Kingdom, 23–27 April 1984, pp 23–27

  • Majluf P (1991) El Niño Effects on Pinnipeds in Peru. In: Trillmich F, Ono KA (eds) Pinniped and El Niño, Responses to Environmental stress. Springer-Verlag Press, pp 55–65

  • Majluf P (1992) Timing of births and juvenile mortality in the South American fur seal in Peru. J Zool Lond 227:367–383

    Article  Google Scholar 

  • Majluf P (1998) Effects of the 1997/1998 El Niño on pinnipeds in Peru. Paper presented at the 8a Reunião de Trabalho de Especialistas em Mamíferos Aquáticos da América do Sul e 2° Congresso da Sociedade Latinoamericana de Especialistas em Mamíferos Aquáticos de América do Sul, Olinda, 25–29 October 1998, p 120

  • Majluf P, Trillmich F (1981) Distribution and abundance of sea lions (Otaria byronia) and fur seal (Arctocephalus australis) in Peru. Z.f.Säugetierkunde 46:384–393

    Google Scholar 

  • Majluf P, Goebel ME (1992) The capture and handling of female South American fur seals and their pups. Mar Mamm Sci 8:187–190

    Article  Google Scholar 

  • Majluf P, Riveros JC, Parlane S (1996) Cool spots as “hot spots”: The evolution of lekking in the South American fur seal. In: Croxall JP, Gentry RL (eds) International symposium and workshop on Otariid reproductive strategies and conservation, Washington, p 26

  • Majluf P, Boness D, Insley S, Paredes R (2000) Determinantes de la estructura del sistema social en el lobo fino sudamericano Arctocephalus australis – resultados de un experimento natural. Paper presented at the 9ª Reunión de Trabajo de Especialistas en Mamíferos Acuáticos de América del Sur y 3° Congresso de la Sociedad Latinoamericana de Especialistas en Mamíferos Acuáticos de América del Sur, Buenos Aires, 30 October–03 November 2000, p 81

  • Marcus LF (1990) Traditional morphometrics. In: Rohlf FJ, Bookstein FL (eds) Proceedings of the Michigan morphometrics workshop. The University of Michigan, Michigan, pp 77–122

    Google Scholar 

  • Marcus L, Bello E, García-Valdecasas A (1993) Contributions to morphometrics. Monografias del Museu Nacional de Ciencias Naturales 8, Madrid, Spain, p 240

  • Martin AR, Katona SK, Matilla D, Hembree D, Waters TD (1984) Migration of Humpback Whales between the Caribbean and Iceland. J Mamm 65:330–333

    Article  Google Scholar 

  • Mate BR, Lagerquist BA, Calambokidis J (1999) Movements of North Pacific Blue whales during the feeding season off Southern California and their Southern fall migration. Mar Mamm Sci 15:1246–1257

    Article  Google Scholar 

  • Matthiopoulos J, Mcconnell B, Duck C, Fedak M (2004) Using satellite telemetry and aerial counts to estimate space use by grey seals around the British Isles. J Appl Ecol 41:476–491

    Article  Google Scholar 

  • McMillen-Jackson AL, Bert TM, Cruz-Lopez H, Seyoum S, Orsoy T, Crabtree RE (2005) Molecular genetic variation in tarpon (Megalops atlanticus Valenciennes) in the northern Atlantic Ocean. Mar Biol 146:253–261

    Article  CAS  Google Scholar 

  • Monteiro-Filho ELA, Monteiro LR, Reis SF (2002) Skull shape and size divergence in dolphins of the genus Sotalia: a tridimensional morphometric analysis. J Mamm 83:125–134

    Article  Google Scholar 

  • Moritz C (1994a) Defining evolutionary significant units for conservation. TREE 9:373–375

    Google Scholar 

  • Moritz C (1994b) Applications of mitochondrial DNA analysis in conservation: critical review. Mol Ecol 3:401–411

    Article  CAS  Google Scholar 

  • Moritz C, Lavery S, Slade R (1995) Using allele frequency and phylogeny to define units for conservation and management. In: Nielsen JL, Powers GA (eds) Evolution and the aquatic ecosystem: defining unique units in population conservation, symposium 17. American Fisheries Society, Bethesda, Maryland, pp 249–262

    Google Scholar 

  • Neff NA, Marcus LF (1980) A survey of multivariate methods for systematics. American Society of Mammalogy, p 243

  • Nielsen JL, Powers GA (1995) Evolution and the aquatic ecosystem: defining unique units in population conservation. American Fisheries Society, Bethesda, Maryland

    Google Scholar 

  • Oliveira LR (2004) Variação geográfica do lobo-marinho sulamericano, Arctocephalus australis (Zimmermann, 1783) com base em dados morfológicos e moleculares. PhD thesis, Universidade de São Paulo

  • Oliveira LR, Malabarba LR, Majluf P (1999) Variação geográfica em crânios do lobo-marinho sul-americano Arctocephalus australis (Zimmermann, 1783) das populações do Brasil e Peru. Comunicações do Museu de Ciências e Tecnologia da PUCRS 12:179–192

    Google Scholar 

  • Oliveira LR, Danilewicz D, Martins MB, Ott P, Moreno IB, Caon G (2001) New records of the Antarctic fur seal, Arctocephalus gazella (Peters, 1875) to the Brazilian coast. Comunicações do Museu de Ciências e Tecnologia da PUCRS 14:201–207

    Google Scholar 

  • Oliveira LR, Hingst-Zaher E, Morgante JS (2005) Size and shape sexual dimorphism in the skull of the South American fur seal, Arctocephalus australis (Zimmermann, 1783) (Carnivora: Otariidae). LAJAM 4:27–40

    Google Scholar 

  • Oliveira LR, Arias-Schreiber M, Meyer D, Morgante JS (2006) Effective population size in a bottlenecked fur seal population. Biol Cons 131:505–509

    Article  Google Scholar 

  • Ovenden JR, Salini J, O’connor S, Street R (2004) Pronounced genetic population structure in a potentially vagile fish species (Pristipomoides multidens, Teleostei: Perciformes: Lutjanidae) from the East Indies triangle. Mol Ecol 13:1991–1999

    Article  PubMed  CAS  Google Scholar 

  • Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354

    Article  PubMed  CAS  Google Scholar 

  • Parsons KM, Durban JW, Claridge DE, Herzing DL, Balcomb KC, Noble LR (2006) Population genetic structure of coastal bottlenose dolphins (Tursiops truncatus) in the Northern Bahamas. Mar Mamm Sci 22:276–298

    Article  Google Scholar 

  • Peters RH (1983) The ecological implications of body size. Cambridge studies in ecology. Cambridge Academic Press, Cambridge

    Google Scholar 

  • Pinedo MC (1990) Ocorrência de Pinípedes na costa brasileira. Garcia de Orta, Serie Zoologia 15:37–48

    Google Scholar 

  • Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first generation migrants detection. J Her 95:536–539

    Article  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) genepop (version 1.2): Population genetics software for exact tests and ecumenicism. J Her 86:248–249

    Google Scholar 

  • Repenning CA, Peterson RS, Hubbs CL (1971) Contributions to the systematics of the southern fur seals, with particular reference to the Juan Fernández and Guadalupe species. In: Burt WH (ed) Antarctic Pinnipedia, vol 18. Antarctic Research, American Geophysical Union, pp 1–34

  • Rice DW (1998) Marine Mammals of the World. Special Publication No. 4. Society for Marine Mammalogy

  • Robalo JI, Doadrio I, Valente A, Almada VC (2007) Identification of ESUs in the critically endangered Portuguese minnow Chondrostoma lusitanicum Collares-Pereira 1980, based on a phylogeographical analysis. Cons Gen (in press). doi:10.1007/s10592-006-9275-x

  • Rohlf FJ (1993) Relative warps analysis and an example of its application to mosquito wings. Contributions to morphometrics. Monografias del Museu Nacional de Ciencias Naturales 8. Madrid, Spain, p 240

    Google Scholar 

  • Rohlf FJ (2000) Tps Regr, ver. 1.25 © 2000. Dept. Ecology and Evolution, State University of New York at Stony Brook

  • Rohlf FJ (2002) TpsRelW, ver. 1.25. © 2002. Dept. Ecology and Evolution, State University of New York at Stony Brook

  • Rohlf FJ (2003) TpsDig, ver. 1.32 © 2003. Dept. Ecology and Evolution, State University of New York at Stony Brook

  • Rohlf FJ, Marcus LF (1993) A revolution in morphometrics. TREE 8:129–132

    Google Scholar 

  • Rosas FCW, Pinedo MC, Marmontel M, Haimovici M (1994) Seasonal movements of the South American sea lion (Otaria flavescens, Shaw) off the Rio Grande do Sul coast, Brazil. Mammalia 58:51–59

    Article  Google Scholar 

  • Ryder OA (1986) Species conservation and systematics: the dilemma of subspecies. TREE 1:9–10

    Google Scholar 

  • Seal Conservation Society (2006) South American Fur Seal. Available via http://www.pinnipeds.org/species/samfursl.htm. Accessed 30 March 2006

  • Simões-Lopes PC, Drehmer CJ, Ott PH (1995) Nota sobre os Otariidae e Phocidae (Mammalia: Carnivora) da costa norte do Rio Grande do Sul e Santa Catarina, Brasil. Biociências 3:173–181

    Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    PubMed  CAS  Google Scholar 

  • Slice DE (1994) GRF-ND, Generalized rotational fitting of n-dimensional landmark data. Dept. Ecology and Evolution, State University of New York at Stony Brook

  • Sokal RR, Rohlf, FJ (1981) Biometry, the principals and practice of statistics in biological research, 3rd edn. New York

  • Stevens MA, Boness DJ (2003) Influences of habitat features and human disturbance on use of breeding sites by a declining population of southern fur seals (Arctocephalus asutralis). J Zool Lond 260:154–152

    Article  Google Scholar 

  • Tolley KA, Vikingsson GA, Rosel P (2001) Mitochondrial DNA sequencevariation and phylogeographic patterns in harbour porpoises (Phocoena phocoena) from the North Atlantic. Cons Gen 2:349–361

    Article  CAS  Google Scholar 

  • Túnez JI, Centrón D, Cappozzo HL, Cassini MH (2007) Geographic distribution and diversity of mitochondrial DNA haplotypes in South American sea lions (Otaria flavescens) and fur seals (Arctocephalus australis). Mamm Biol 72:193–203

    Article  Google Scholar 

  • 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 4:535–538

    Article  CAS  Google Scholar 

  • Vaz-Ferreira R (1982) Arctocephalus australis Zimmerman, South American fur seal. In: Mammals in the seas. FAO Fisheries series, Small cetaceans, seals, sirenians and otters, vol 4, pp 497–508

  • Vaz-Ferreira R, Bianco J (1998) Explotación, sobrevivencia y preservación de los otariideos en el Uruguay. Paper presented at the 8a Reunião de Trabalho de Especialistas em Mamíferos Aquáticos da América do Sul e 2° Congresso da Sociedade Latinoamericana de Especialistas em Mamíferos Aquáticos de América do Sul, Olinda, 25–29 October 1998, p 221

  • Vieira CC (1955) Lista remissiva dos mamíferos do Brasil. Arquivos Zoologia do Estado de São Paulo 8:341–474

    Google Scholar 

  • Vogler AP, DeSalle R (1994) Diagnosing units of conservation management. Cons Biol 6:170–178

    Google Scholar 

  • Wada S, Masayuki O, Yamada T (2003) A newly discovered species of living baleen whale. Nature 426:278–281

    Article  PubMed  CAS  Google Scholar 

  • Walsh PS, Metzger DA, Higuchi R (1991) Chelex100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotech 10:506–513

    CAS  Google Scholar 

  • Walsh PS, Ehrlich HA, Higuchi R (1992) Preferential amplification of alleles: mechanisms and solutions. PCR Meth Appl 1:241–250

    CAS  Google Scholar 

  • Wang JY, Chou LS, White BN (1999) Mitochondrial DNA analysis of sympatric morphotypes of bottlenose dolphins (genus: Tursiops) in Chinese waters. Mol Ecol 8:1603–1612

    Article  PubMed  CAS  Google Scholar 

  • Wang JY, Chou LS, White BN (2000) Differences in the external morphology of two sympatric species of bottlenose dolphins (genus Tursiops) in the waters of China. J Mamm 81:1157–1165

    Article  Google Scholar 

  • Waples RS (1991) Pacific Salmon, Oncorhynchus spp. and the definition of species under the endangered species act. Mar Fish Rev 53:11–22

    Google Scholar 

  • Waples RS (1995) Evolutionary significant units and the conservation of biological diversity under the Endangered Species Act. In: Nielsen JL, Powers GA (eds) Evolution and the aquatic ecosystem: defining unique units in population conservation. American Fisheries Society, Bethesda, pp 8–27

    Google Scholar 

  • Waples RS (1998) Evolutionarily significant units, distinct population segments, and the endangered species act: reply to Pennock and Dimmick. Cons Biol 12:718–721

    Article  Google Scholar 

  • Warner RR, Chesson PL (1985) Coexistence mediated by recruitment fluctuations: a field guide to the storage effect. The Am Nat 125:769–787

    Article  Google Scholar 

  • Waser PM, Strobeck C (1998) Genetic signatures of interpopulation dispersal. TREE 13:43–44

    Google Scholar 

  • Wayne RK (1992) On the use of molecular genetic characters to investigate species status. Cons Biol 6:590–592

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wood CJ (1998) Movement of bottlenose dolphins around the south-west coast of Britain. J Zool 246:155–163

    Article  Google Scholar 

  • Wright S (1965) The interpretation of population structure by statistics with special regard to systems of mating. Evolution 19:395–420

    Article  Google Scholar 

  • Wynen LP, Goldsworthy SD, Insley SJ, Adams M, Bickham J.W, Francis J, Gallo JP, Hoelzel AR, Majluf P, White RWG, Slade R (2001) Phylogenetic Relationships within the Eared Seals (Otariidae: Carnivora): Implications for the Historical Biogeography of the Family. Mol Phyl Evol 21:270–284

    Article  CAS  Google Scholar 

  • Zelditch M, Swiderski D, Sheets DH, Fink W (2004) Geometric Morphometrics For Biologists: a primer. Elsevier Academic Press, San Diego

    Google Scholar 

  • Zimmerman EAW Von (1783) Geographische Geshichte des Menschen, und der Allgemeiss Verbreiteten Vierfüssigen Thiere. Leipzig 3:1778–1783

    Google Scholar 

Download references

Acknowledgements

Thanks to the collection managers: Paulo César Simões-Lopes (LAMAQ/UFSC, Florianópolis, Brazil); Ignacio B. Moreno (GEMARS/CECLIMAR, Porto Alegre, Brazil), Cibele Andruziak (MCN/FZBRS, Porto Alegre, Brazil); Charles Potter and James Mead (NMNH, Washington DC, USA); Robert Randall (AMNH, New York, USA); Paula Jenkins, Robert Harbour and Daphne (BMNH, London, UK); Andrey Friday (Museum of Zoology, University of Cambridge, Cambridge, UK); Walter Sielfeld (UAP, Iquique, Chile); Claudio Venegas (IP, Punta Arenas, Chile); Luis Cappozzo and Olga Vacaro (MACN “Bernardino Rivadávia”, Buenos Aires, Argentina); Diego Rodriguez and Ricardo Bastida (FCN, Mar del Plata, Argentina); Natalie P. Goodal (Museo Acatushún, Ushuaia, Argentina); Ernesto Piana (CADIC, Ushuaia, Argentina); Enrique Crespo (CENPAT, Puerto Madryn, Argentina), Milena Roca Fabián (Proyecto Punta San Juan, Lima, Peru), Alfredo Le Bas and Mario Clara (FCN, Montevideo, Uruguay). To Daniel Danilewicz, Mauricio Tavares, Rodrigo Machado, Paulo H. Ott, Ignacio B. Moreno and Márcio Borges-Martins for collaborating in necropsies on the Brazilian coast; to the research team of the Punta San Juan Project (1997 and 2003): Nora Rueda, Gabriela Battistini, Rosana Paredes, Carlos Zavalaga, Diana, and Juan Cervantes-Sanchez, Milena Roca Fabián, Susana Cárdenas, Armando Valdés-Velásquez, Marco Cardeña, Manuel Apaza and Pedro Llerena for the helping in the sampling activity in Peru. To Cristine Trinca for your great help with Structure program and to Marcus Guidoti for formatting part of data set. To Diego Astua de Moraes and Milton E. Menezes, who kindly prepared the Fig 2 and to Ignacio B. Moreno who prepared the Fig. 1. To the anonymous referees whose valuable comments improved this article.

To Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), which provided the PhD grant to Larissa Rosa de Oliveira (FAPESP 00/00248-2, 00/01340-0), to Society for Marine Mammalogy (grants-in-aid program) for partially funding the museum visits, and also to MCT/CNPq/Prosul (CNPq 490281/2005-2) for funding field activities in order to collect tissue samples. This study is part of the dissertation presented by Larissa Rosa de Oliveira, submitted in partial fulfillment for a PhD degree in Biology (Genetics) at Universidade de São Paulo, Brazil. Samples were collected under permission of license number 022-2004-INRENA-IFFS-DCB in Peru and IBAMA-105/98 in Brazilian coast. This paper is GEMARS contribution 19.

Author information

Author notes

  1. Larissa Rosa de Oliveira

    Present address: Grupo de Estudos de Mamíferos Aquáticos do Rio Grande do Sul (GEMARS), Rua Felipe Néri 382/203, Porto Alegre, RS, 90550-140, Brazil

Authors and Affiliations

  1. Laboratório de Biologia Evolutiva e Conservação de Vertebrados (LABEC), Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, Cidade Universitária, Sao Paulo, SP, 05508-090, Brazil

    Larissa Rosa de Oliveira & João Stenghel Morgante

  2. Centro de Estudos Costeiros, Limnológicos e Marinhos da Universidade Federal do Rio Grande do Sul (CECLIMAR/UFRGS), Av. Tramandaí, 976, Tramandai, RS, 95625-000, Brazil

    Larissa Rosa de Oliveira

  3. Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK

    Joseph I. Hoffman & William Amos

  4. Laboratório de Mastozoologia, Museu de Zoologia da Universidade de São Paulo, Av. Nazaré, 481, Ipiranga, Sao Paulo, SP, 04299-970, Brazil

    Erika Hingst-Zaher

  5. Unidad de Biología de la Conservación, Universidad Peruana Cayetano Heredia (UPCH), Armendáriz 445, Miraflores, Lima, 18, Peru

    Patricia Majluf

  6. Laboratório de Mamíferos Marinhos e Tartarugas Marinhas, Departamento de Oceanografia, Programa de Pós-Graduação em Oceanografia Biológica, Cx. Postal, 474, Rio Grande, RS, 96201-900, Brazil

    Mônica M. C. Muelbert

Authors
  1. Larissa Rosa de Oliveira
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Joseph I. Hoffman
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Erika Hingst-Zaher
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Patricia Majluf
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Mônica M. C. Muelbert
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. João Stenghel Morgante
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. William Amos
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Larissa Rosa de Oliveira.

Appendix

Appendix

Specimens examined in the skull morphometrics study. The 240 adult specimens (235 Arctocephalus australis and 5 A. gazella) used in this study were obtained from the following collections:

Grupo de Estudos de Mamíferos Aquáticos do Rio Grande do Sul, Brazil (GEMARS: 0173; 0176; 0185; 0208; 0218; 0256; 0259; 0263; 0278; 0280; 0293; 0297; 0298; 0302; 0308; 0316; 0321; 0338; 0359; 0361; 0364; 0368; 0425; 0429; 0436; 0439; 0445; 0450; 0537; 0542; 0544; 0558; 0561; 0578; 0581; 0582; 0584; 0586; 0589; 0655; 0661; 0681; 0694; 0706; 0721; 0739; 0801), Museu de Ciências Naturais da Fundação Zoobotânica do Rio Grande do Sul, Brazil (MCN-FZB: 2630; 2637; 2688; 2706; 2886), Laboratório de Mamíferos Aquáticos da Universidade Federal de Santa Catarina, Brazil (LAMAQ-UFSC: 1057; 1063; 135; 1142; 1143; 1149; 1153; 1154; 1156; 1157; 1158; 1159; 1160; 1163; 1166; 1167; 1169; 1170; 1228; 1274), Laboratório de Mamíferos Aquáticos e Tartarugas Marinhas da Fundação Universidade do Rio Grande, Brazil (LMM-FURG: s/no.7; 0101; 0608; 0609; 0663; 0684; 0726; 0731; 0732; 0750; 0754; 0840; 0863; 0890; 1258; 1282; 1336; 1338; 1340; 1341; 1342; 1346; 1431; 1435; 1437; 1438; 1442; 1444; 1464; 1535; 1549; 1554; 1657; 1690; 1738; 1742; 1748; 1781; 1808; 1813; 1815; 1824; 1859; 1898; 1903; 1985; 2045; 2084; 2121; 2267), Centro Nacional Patagónico, Argentina (CENPAT: Aa16), American Museum of Natural History, USA (AMNH: 205916; 205917; 205918; 254562; 254563; 254564; 254565; 254569), Facultad de Ciencias Naturales, Uruguay (FCN: 1522; 1580), National Museum of Natural History – Smithsonian Institution, USA (NMNH: 239140; 504895), British Museum of Natural History, UK (BMNH: 1947.7.16.4; 1984.911; 1984.912; 1984.918; 1984.920; 1984.921; 1984.923; 1984.924; 1984.926; 1984.927; 1984.928; 1984.930; 1984.931; 1984.932; 1984.933; 1984.934; 1984.935; 1984.939; 1984.942a; 1984.947; 1984.948; 1984.949; 1984.969; 1984.972; 1984.973; 1984.975; 1984.978), Proyecto Punta San Juan, Peru (PSJ: 0005; 0008; 0009; 0078; 0143; 0168; 0178; 0180; 0209; 0210; 0216; 0217; 0220; 0221; 0222; 0234; 0236; 0237; 0238; 0239; 0240; 0241; 0242; 0261; 0262; 0263; 0264; 0265; 0266; 0267; 0268; 0287; 0295; 0297; 0298; 0300; 0302; 0304; 0306; 0307; 0319; 0320; 0321; 0322; 0323; 0324; 0325; 0326; 0327; 0328; 0329; 0330; 0331; 0367; 0368; 0369; 0370; 0371; 0372; 0373; 0374; 0375; 0376; 0377; 0378; 0379; 0417; 0418; 0447; 0448; 0450; 0460; 0461; 0462) and Museum of Zoology, University of Cambridge, UK (K.7321K; K.7321L; K.7321M; K.7321N; K.7321O). Total sample examined: Arctocephalus australis from Uruguay (n = 133) and Arctocephalus australis from Peru (n = 102); Arctocephalus gazella (n = 5).

Rights and permissions

Reprints and permissions

About this article

Cite this article

de Oliveira, L.R., Hoffman, J.I., Hingst-Zaher, E. et al. Morphological and genetic evidence for two evolutionarily significant units (ESUs) in the South American fur seal, Arctocephalus gazella . Conserv Genet 9, 1451–1466 (2008). https://doi.org/10.1007/s10592-007-9473-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-007-9473-1

Keywords