Advertisement

Population structure of the Atlantic spotted dolphin (Stenella frontalis) inferred through ecological markers

  • Paula Méndez-FernandezEmail author
  • Satie Taniguchi
  • Marcos C. O. Santos
  • Irma Cascão
  • Sophie Quérouil
  • Vidal Martín
  • Marisa Tejedor
  • Manuel Carrillo
  • Caroline Rinaldi
  • Renato Rinaldi
  • Dalia C. Barragán-Barrera
  • Nohelia Farías-Curtidor
  • Susana Caballero
  • Rosalinda C. Montone
Article

Abstract

Population structure studies play an increasingly integral role in conservation and management of marine mammal species. Genetic markers are commonly used; however, ecological markers (i.e. chemical compounds) are a fairly recent and useful tool to investigate ecological management units. The objective of this study is to investigate the population structure of the Atlantic spotted dolphin (Stenella frontalis) within its distribution in the Atlantic Ocean using data from stable isotopes of δ13C and δ15N and persistent organic pollutants as ecological markers. Based on previous studies that addressed distribution, morphometric analyses and molecular and ecological markers, we hypothesize that there are several ecological management units within the Atlantic Ocean. Our results confirmed population differentiation previously detected using genetic markers. Additionally, dolphins from the south-eastern coast of Brazil do not show complete ecological segregation from the Caribbean ones, while molecular analyses suggested genetic differentiation between the two regions. In the light of these results, we propose that at least two ecological management units should be considered, east and west of the Atlantic Ocean; however, the presence of one or two management units along the Atlantic coast of Central and South America needs further investigation.

Keywords

Ecological management units Stable isotopes Persistent organic pollutants Stenella frontalis Atlantic Ocean 

Notes

Acknowledgements

This work has been made possible thanks to all members of the institutions and organizations that assist with field and data collection. We also gratefully acknowledge B. Lebreton and G. Guillou from Littoral Environnement et Sociétés (LIENSs) of the University of La Rochelle as well as the personnel of the Organic Marine Chemistry Laboratory (LabQOM) of the Instituto Oceanográfico da Universidade de São Paulo for their help on chemical analyses. We also wish to thank J. Kiszka for his help on data collection. This work was supported through the project “Population structure and contamination status of Atlantic spotted dolphin (Stenella frontalis)” funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 406814/2013-9). PMF was supported by a post-doctoral grant from the CNPq under the program “Ciências sem Fronteiras”, and by a fieldwork grant of the Society for Marine Mammalogy (SMM). Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) funded research on mapping cetacean occurrence and biopsy sampling along the coast of São Paulo state from 2013 to 2015 (Auxílio à Pesquisa, process # 2011/51543-9). MCOS was sponsored by the CNPq under the program Produtividade em Pesquisa from 2011 to 2014 (process # 308331/2010-9). Fieldwork in Colombia was supported by the Rufford Foundation, the Society for Marine Mammalogy, and Sciences Faculty of Universidad de los Andes (“Proyecto Semilla” – Calls 2013-3/2015-1, projects: “Diversidad genética del delfín nariz de botella en la Guajira, Caribe colombiano” and “Ocurrencia, distribución y estatus genético preliminar de delfínidos en la Guajira, Caribe colombiano”). Finally, authors kindly wish to thanks the two anonymous reviewers for their great and constructive revision.

Supplementary material

10452_2019_9722_MOESM1_ESM.docx (30 kb)
Supplementary material 1 (DOCX 29 kb)

References

  1. Adams LD, Rosel PE (2006) Population differentiation of the Atlantic spotted dolphin (Stenella frontalis) in the western North Atlantic, including the Gulf of Mexico. Mar Biol 148:671–681CrossRefGoogle Scholar
  2. Aguilar A, Borrell A, Pastor T (1999) Biological factors affecting variability of persistent pollutant levels in cetaceans. J Cetacean Res Manag 1:83–116Google Scholar
  3. Andrewartha HG, Birch LC (1984) The ecological web. University Chicago Press, ChicagoGoogle Scholar
  4. Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13(4):729–744CrossRefPubMedGoogle Scholar
  5. Banguera-Hinestroza E, Bjørge A, Reid RJ, Jepson P, Hoelzel AR (2010) The influence of glacial epochs and habitat dependence on the diversity and phylogeography of a coastal dolphin species: Lagenorhynchus albirostris. Conserv Genet 11(5):1823–1836CrossRefGoogle Scholar
  6. Born EW, Outridge P, Riget FF, Hobson KA, Dietz R et al (2003) Population substructure of North Atlantic minke whales (Balaenoptera acutorostrata) inferred from regional variation of elemental and stable isotopic signatures in tissues. J Mar Syst 43(1–2):1–17CrossRefGoogle Scholar
  7. Borrell A, Aguilar A (2005) Differences in DDT and PCB residues between common and striped dolphins from the southwestern Mediterranean. Arch Environ Contam Toxicol 48(4):501–508CrossRefPubMedGoogle Scholar
  8. Borrell A, Aguilar A, Tornero V, Sequeira M, Fernandez G, Alis S (2006) Organochlorine compounds and stable isotopes indicate bottlenose dolphin subpopulation structure around the Iberian Peninsula. Environ Intern 32:516–523CrossRefGoogle Scholar
  9. Caballero S, Santos MCdO, 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 48:263–270CrossRefGoogle Scholar
  10. Cañadas A, Sagarminaga R, Garcia-Tiscar S (2002) Cetacean distribution related with depth and slope in the Mediterranean waters off southern Spain. Deep Sea Res 49:2053–2073CrossRefGoogle Scholar
  11. Caurant F, Chouvelon T, Lahaye V, Méndez-Fernandez P, Rogan E et al (2009) The use of ecological tracers for discriminating populations: the case of the short-beaked common dolphin Delphinus delphis in the European Atlantic waters. Rep Int Whal Comm Spec Issue, MadeiraGoogle Scholar
  12. Coyle T (1998) Stock identification and fisheries management: the importance of using several methods in a stock identification study. In: Hancock DA (ed) Taking stock: defining and managing shared resources. Australian Society for Fishery Biology, Sydney, pp 173–182Google Scholar
  13. Crawford TJ (1984) What is a population? In: Shorrocks B (ed) Evolutionary ecology. Blackwell, Oxford, pp 135–173Google Scholar
  14. Cruz MJ, Machete M, Menezes G, Rogan E, Silva MA (2018) Estimating common dolphin bycatch in the pole-and-line tuna fishery in the Azores. PeerJ 6:4285CrossRefGoogle Scholar
  15. Danilewicz D, Ott PH, Secchi ER, Andriolo A, Zerbini AN (2013) Occurrence of the Atlantic spotted dolphin, Stenella frontalis, in southern Abrolhos Bank, Brazil. MB Records 6Google Scholar
  16. DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506CrossRefGoogle Scholar
  17. Di Beneditto AM, Ramos RMA, Siciliano S, Santos RA, Bastos G, Fagundesnetto E (2001) Stomach contents of delphinids from Rio de Janeiro, southeastern Brazil. Aquat Mamm 27:24–28Google Scholar
  18. Do Amaral KB, Alvares DJ, Heinzelmann L, Borges-Martins M, Siciliano S, Moreno IB (2015) Ecological niche modeling of Stenella dolphins (Cetartiodactyla: Delphinidae) in the southwestern Atlantic Ocean. J Exp Mar Biol Ecol 472:166–179CrossRefGoogle Scholar
  19. Evans PGH, Teilmann J (2009) Report of ASCOBANS/HELCOM small cetacean population structure workshop. ASCOBANS, Bonn, GermanyGoogle Scholar
  20. Fernandez R, Santos MB, Carrilo M, Tejedor M, Pierce GJ (2009) Stomach contents of cetaceans stranded in the Canary Islands 1996–2006. J Mar Biol Assoc UK 89(5):873–883CrossRefGoogle Scholar
  21. Fontaine MC, Baird SJ, Piry S, Ray N, Tolley KA, Duke S et al (2007) Rise of oceanographic barriers in continuous populations of a cetacean: the genetic structure of harbour porpoises in Old World waters. BMC Biol 5(1):30CrossRefPubMedPubMedCentralGoogle Scholar
  22. Fontaine MC, Tolley KA, Michaux JR, Birkun A, Ferreira M et al (2010) Genetic and historic evidence for climate-driven population fragmentation in a top cetacean predator: the harbour porpoises in European water. Proc R Soc Lond B Biol Sci 277(1695):2829–2837CrossRefGoogle Scholar
  23. Foote AD, Newton J, Piertney SB, Willerslev E, Gilbert MTP (2009) Ecological, morphological and genetic divergence of sympatric North Atlantic killer whale populations. Mol Ecol 18(24):5207–5217CrossRefPubMedGoogle Scholar
  24. Fruet PF, Dalla Rosa L, Genoves RC, Valiati VH, De Freitas TRO, Möller LM (2016) Biopsy darting of common bottlenose dolphins (Tursiops truncatus) in southern Brazil: evaluating effectiveness, short-term responses and wound healing. Lat Am J Aquat Mamm 11(1–2):121–132Google Scholar
  25. Fullard KJ, Early G, Heide-Jørgensen MP, Bloch D, Rosing-Asvid A, Amos W (2000) Population structure of long-finned pilot whales in the North Atlantic: a correlation with sea surface temperature? Mol Ecol 9(7):949–958CrossRefPubMedGoogle Scholar
  26. Geraci JR, Lounsbury VJ (1993) Marine mammals ashore: a field guide for strandings. Texas A and M Sea Grant College Program, pp 304Google Scholar
  27. Giménez J, De Stephanis R, Gauffier P, Esteban R, Verborgh P (2011) Biopsy wound healing in long-finned pilot whales (Globicephala melas). Vet Record 168(4):101CrossRefGoogle Scholar
  28. Giménez J, Gómez-Campos E, Borrell A, Cardona L, Aguilar A (2013) Isotopic evidence of limited exchange between Mediterranean and eastern North Atlantic fin whales. Rapid Com Mass Spectrosc 27(15):1801–1806CrossRefGoogle Scholar
  29. Giménez J, Ramírez F, Almunia J, Forero MG, De Stephanis R (2016) From the pool to the sea: applicable isotope turnover rates and diet to skin discrimination factors for bottlenose dolphins (Tursiops truncatus). J Exp Mar Biol Ecol 475:54–61CrossRefGoogle Scholar
  30. Giménez J, Louis M, Barón E, Ramírez F, Verborgh P et al (2017) Towards the identification of ecological management units: a multidisciplinary approach for the effective management of bottlenose dolphins in the southern Iberian Peninsula. Aquat Cons Mar Fresh Ecosyst 28(1):205–215CrossRefGoogle Scholar
  31. Herzing DL, Elliser CR (2013) Nocturnal feeding of Atlantic spotted dolphins (Stenella frontalis) in the Bahamas. Mar Mammal Sci 30:367–373CrossRefGoogle Scholar
  32. Hobson KA (1998) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326CrossRefGoogle Scholar
  33. Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94(1):181–188CrossRefGoogle Scholar
  34. ICES (2014) Report of the working group on marine mammals (WGMME), 10–13, Woods Hole, Massachusetts, USA. ICES CM 2014/ACOM:27, 234 ppGoogle Scholar
  35. Jefferson TA, Webber MA, Pitman RL (eds) (2008) Marine mammals of the world. A comprehensive guide to their identification. Academic Press, London, p 73Google Scholar
  36. Kowarski KA, Augusto JF, Frasier TR, Whitehead H (2014) Effects of remote biopsy sampling on long-finned pilot whales (Globicephala melas) in Nova Scotia. Aquat Mamm 40(2):117–125CrossRefGoogle Scholar
  37. Krützen M, Barre LM, Möller LM, Heithaus MR, Simms C, Sherwin WB (2002) A biopsy system for small cetaceans: darting success and wound healing in Tursiops spp. Mar Mamm Sci 18:863–878CrossRefGoogle Scholar
  38. Kuiken T, Hartmann M (1991) Proceedings of the first European Cetacean Society workshop on ‘Cetacean pathology: dissection techniques and tissue sampling’. ECS Newslett 17:1–39Google Scholar
  39. Lopes XM, Santos MCdO, Silva ED, Bassoi M, Santos RAD (2012) Feeding habits of the atlantic spotted dolphin, Stenella frontalis, in southeastern Brazil. Braz J Oceanogr 60(2):189–198CrossRefGoogle Scholar
  40. 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 B Biol Sci 266(1417):347–354CrossRefGoogle Scholar
  41. McMahon KW, Hamady LL, Thorrold SR (2013) A review of ecogeochemistry approaches to estimating movements of marine animals. Limnol Oceanogr 58(2):697–714CrossRefGoogle Scholar
  42. Melo CLL, Santos RA, Bassoi M, Araújo AC, Lailson-Brito J, Dorneles PR, Azevedo AF (2010) Feeding habits of delphinids (Mammalia: Cetacea) from Rio de Janeiro State, Brazil. J Mar Biol Assoc UK 90(8):1509–1515CrossRefGoogle Scholar
  43. Méndez-Fernandez P, Taniguchi S, Santos MCdO, Cascão I, Quérouil S et al (2018) Contamination status by persistent organic pollutants of the Atlantic spotted dolphin (Stenella frontalis) at the metapopulation level. Environ Poll 236:785–794CrossRefGoogle Scholar
  44. Mesa-Gutiérrez R, Barragán-Barrera D, Chávez-Carreño D, Farías-Curtidor N, Caballero S (2015) Population structure of the Atlantic spotted dolphin (Stenella frontalis) in the Caribbean. MsC thesis, Universidad de los andes, ColombiaGoogle Scholar
  45. Moreno IB, Zerbini A, Danilewicz D, Santos MCdO, Simões-Lopes PC et al (2005) Distribution and habitat characteristics of dolphins of the genus Stenella (Cetacea: Delphinidae) in the Southwest Atlantic Ocean. Mar Ecol Prog Ser 300:229–240CrossRefGoogle Scholar
  46. Murphy S, Mirimin L, Rogan E (2007) Stock structure reports for bottlenose dolphins Tursiops truncatus, striped dolphins Stenella coeruleoalba, and white-sided dolphins Lagenorhynchus acutus in the Northeast Atlantic. NECESSITY Contract 501605 Periodic Activity Report No 2Google Scholar
  47. Murphy S, Natoli A, Amaral AR, Mirimin L, Viricel A et al (2009) Short-beaked common dolphin Delphinus delphis. In: ASCOBANS/HELCOM Small cetacean population structure workshop. 8–10 October 2007 at UN Campus, Hermann-Ehlers-Str. 10, 53113 Bonn, Germany 111–130Google Scholar
  48. Nieri M, Grau E, Lamarche B, Aguilar A (1999) Mass mortality of Atlantic spotted dolphins (Stenella frontalis) caused by a fishing interaction in Mauritania. Mar Mamm Sci 15:847–854CrossRefGoogle Scholar
  49. Nordstrom CA, Wilson LJ, Sara IJ, Tollit DJ (2008) Evaluating quantitative fatty acid signature analysis (QFASA) using harbour seals Phoca vitulina richardsi in captive feeding studies. Mar Ecol Prog Ser 360:245–263CrossRefGoogle Scholar
  50. Oremus M (2008) Genetic and demographic investigation of population structure and social system in four delphinid species. PhD thesis, University of AucklandGoogle Scholar
  51. Paro AD, Rojas E, Wedekin LL (2014) Southernmost record of the Atlantic spotted dolphin, Stenella frontalis in the south-west Atlantic Ocean. Mar Biol Assoc 7:e78Google Scholar
  52. Perrin WF (2002) Stenella frontalis. Mamm Species 702:1–6CrossRefGoogle Scholar
  53. Perrin WF, Mitchell ED, Mead JG, Caldwell DK, Caldwell MC et al (1987) Revision of the spotted dolphins, Stenella spp. Mar Mamm Sci 3:99–170CrossRefGoogle Scholar
  54. Perrin WF, Caldwell DK, Caldwell MC (1994) Atlantic spotted dolphin Stenella frontalis (Cuvier G 1829). In: Ridgway SH, Harrison R (eds) Handbook of marine mammals, vol 5. The first book of Dolphins. Academic Press, New York, pp 173–190Google Scholar
  55. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Ann Rev Ecol Syst 18(1):293–320CrossRefGoogle Scholar
  56. Quérouil S, Silva MA, Cascão I, Magalhães S, Seabra MI et al (2008) Why do dolphins form mixed-species associations in the Azores? Ethology 114(12):1183–1194CrossRefGoogle Scholar
  57. Quérouil S, Freitas L, Cascão I, Alves F, Dinis A, Almeida JR et al (2010) Molecular insight into the population structure of common and spotted dolphins inhabiting the pelagic waters of the Northeast Atlantic. Mar Biol 157(11):2567–2580CrossRefGoogle Scholar
  58. Quérouil S, Kiszka J, Cordeiro AR, Cascão I, Freitas L et al (2013) Investigating stock structure and trophic relationships among island-associated dolphins in the oceanic waters of the North Atlantic using fatty acid and stable isotope analyses. Mar Biol 160(6):1325–1337CrossRefGoogle Scholar
  59. R Core Team (2013) R: A Language and Environment for Statistical Computing. RFoundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  60. Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9(5):615–629CrossRefPubMedGoogle Scholar
  61. Silva MA, Prieto R, Cascão I, Seabra MI, Machete M et al (2014) Spatial and temporal distribution of cetaceans in the mid-Atlantic waters around the Azores. Mar Biol Res 10(2):123–137CrossRefGoogle Scholar
  62. Swanson HK, Lysy M, Power M, Stasko AD, Johnson JD, Reist JD (2015) A new probabilistic method for quantifying n-dimensional ecological niches and niche overlap. Ecology 96:318–324CrossRefPubMedGoogle Scholar
  63. Van Waerebeek K, Ndiaye E, Djiba A, Diallo M (2000) A survey of the conservation status of cetaceans in Senegal, the Gambia and Guinea-Bissau WAFCET-I Report. Convention on the Conservation of Migratory Species (CMS); UNEPGoogle Scholar
  64. Viricel A, Rosel PE (2014) Hierarchical population structure and habitat differences in a highly mobile marine species: the Atlantic spotted dolphin. Mol Ecol 23(20):5018–5035CrossRefPubMedGoogle Scholar
  65. Weijs L, Covaci A, Das K, Blust R (2010) Physiologically based pharmacokinetic (PBPK) models for the bioaccumulation of PBDEs in male harbour porpoises. Organohalogen Compd 72:672–675Google Scholar
  66. Weijs L, Covaci A, Yang RSH, Das K, Blust R (2011) A non-invasive approach to study lifetime exposure and bioaccumulation of PCBs in protected marine mammals: PBPK modeling in harbor porpoises. Toxicol Appl Pharmacol 256:136–145CrossRefPubMedGoogle Scholar
  67. Weir CR (2010) A review of cetacean occurence in West African waters from the Gulf of Guinea to Angola. Mamm Rev 40:2–39CrossRefGoogle Scholar
  68. Wiszniewski J, Lusseau D, Möller LM (2010) Female bisexual kinship ties maintain social cohesion in a dolphin network. Anim Behav 80(5):895–904CrossRefGoogle Scholar
  69. Xu S, Ren W, Zhou X, Zhou K, Yang G (2010) Sequence polymorphism and geographical variation at a positively selected MHC-DRB gene in the finless porpoise (Neophocaena phocaenoides): implication for recent differentiation of the Yangtze finless porpoise? J Mol Evol 71:6–22CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Paula Méndez-Fernandez
    • 1
    • 2
    Email author
  • Satie Taniguchi
    • 1
  • Marcos C. O. Santos
    • 3
  • Irma Cascão
    • 4
    • 5
  • Sophie Quérouil
    • 6
  • Vidal Martín
    • 7
  • Marisa Tejedor
    • 7
  • Manuel Carrillo
    • 8
  • Caroline Rinaldi
    • 9
  • Renato Rinaldi
    • 9
  • Dalia C. Barragán-Barrera
    • 10
    • 11
  • Nohelia Farías-Curtidor
    • 11
  • Susana Caballero
    • 10
  • Rosalinda C. Montone
    • 1
  1. 1.Laboratório de Química Orgânica Marinha, Instituto OceanográficoUniversidade de São PauloSão PauloBrazil
  2. 2.Observatoire PELAGIS, UMS 3462 du CNRS, Pôle AnalytiqueLa Rochelle UniversitéLa RochelleFrance
  3. 3.Laboratório de Biologia da Conservação de Mamíferos Aquáticos, Instituto OceanográficoUniversidade de São PauloSão PauloBrazil
  4. 4.Department of Oceanography and Fisheries & Okeanos CentreUniversity of the AzoresHortaPortugal
  5. 5.Marine and Environmental Sciences Centre (MARE) & Institute of Marine Research (IMAR)University of the AzoresHortaPortugal
  6. 6.ISEMUniv Montpellier, CNRS, EPHE, IRDMontpellierFrance
  7. 7.Sociedad para el Estudio de Cetáceos del Archipiélago Canario (SECAC)ArrecifeSpain
  8. 8.Tenerife ConservaciónLa LagunaSpain
  9. 9.Association Evasion Tropicale (AET)Pigeon BouillanteFrance
  10. 10.Laboratorio de Ecología Molecular de Vertebrados Acuáticos (LEMVA), Departamento de Ciencias BiológicasUniversidad de los AndesBogotáColombia
  11. 11.Fundación Macuáticos ColombiaMedellínColombia

Personalised recommendations