Conservation Genetics

, Volume 11, Issue 6, pp 2207–2218 | Cite as

Molecular identification of small cetacean samples from Peruvian fish markets

  • Athanasia C. Tzika
  • Eva D’Amico
  • Joanna Alfaro-Shigueto
  • Jeffrey C. Mangel
  • Koen Van Waerebeek
  • Michel C. Milinkovitch
Research Article

Abstract

In the last 60 years, incidental entanglement in fishing gears (so called by-catch) became the main cause of mortality worldwide for small cetaceans and is pushing several populations and species to the verge of extinction. Thus, monitoring and quantifying by-catches is an important step towards proper and sustainable management of cetacean populations. Continuous studies indicated that by-catches and directed takes of small cetaceans in Peru greatly increased since 1985. Legal measures banning cetacean takes, enforced in 1994 and 1996, ironically made monitoring highly problematic as fishers continue catching these animals but utilize or dispose of carcasses clandestinely. Hence, in locations where cetaceans are landed covertly or already butchered, molecular genetic methods can provide the only means of identification of the species, sex, and sometimes the population of each sample. Here, we generate and analyse a fragment of the mitochondrial DNA cytochrome b gene and 5 nuclear microsatellite markers from 182 meat and skin samples of unidentified small cetaceans collected at three Peruvian markets between July 2006 and April 2007. Our results, compared to past surveys, indicate that Lagenorhynchus obscurus, Phocoena spinipinnis, Tursiops truncatus, Delphinus capensis, and D. delphis continue to be caught and marketed, but that the relative incidence of P. spinipinnis is highly reduced, possibly because of population depletion. The small number of possible sampling duplicates demonstrates that a high monitoring frequency is required for a thorough evaluation of incidental catches in the area. A wide public debate on by-catch mitigation measures is greatly warranted in Peru.

Keywords

By-catch mortality Cetacean Microsatellites Mitochondrial DNA 

Supplementary material

10592_2010_106_MOESM1_ESM.docx (109 kb)
Supplementary material 1 (DOCX 109 kb)

References

  1. Alfaro Shigueto J, Dutton PH, Van Bressem M, Mangel JC (2007) Interactions between leatherback turtles and Peruvian artisanal fisheries. Chelonian Conserv Biol 6:129–134CrossRefGoogle Scholar
  2. Alfaro Shigueto J, Mangel JC, Seminoff JA, Dutton PH (2008) Demography of loggerhead turtles Caretta caretta in the southeastern Pacific Ocean: fisheries-based observations and implications for management. Endanger Species Res 5:129–135CrossRefGoogle Scholar
  3. Amaral AR, Sequeira M, Martínez-Cedeira J, Coelho MM (2007) New insights on population genetic structure of Delphinus delphis from the northeast Atlantic and phylogenetic relationships within the genus inferred from two mitochondrial markers. Mar Biol 151:1967–1976CrossRefGoogle Scholar
  4. Anonymous (1996) Ley 26585. Declaran a delfines y otros mamíferos marinos como especies legalmente protegidas. Diario El Peruano, Normas Legales, Lima, 9 de Abril de 1996, 138665Google Scholar
  5. Au WWL (1994) Sonar detection of gillnets by dolphins: theoretical predictions. In: Perrin WF, Donovan GP, Barlow J (eds) Gillnets and cetaceans. Reports of the International Whaling Commission. Cambridge, pp 565–578Google Scholar
  6. Awkerman JA, Huyvaert KP, Mangel JC, Alfaro-Shigueto J, Anderson DJ (2006) Incidental and intentional catch threatens Galapagos waved albatross. Biol Conserv 133:483–489CrossRefGoogle Scholar
  7. Baker CS (2008) A truer measure of the market: the molecular ecology of fisheries and wildlife trade. Mol Ecol 17:3985–3998CrossRefPubMedGoogle Scholar
  8. Baker CS, Cooke JG, Lavery S et al (2007) Estimating the number of whales entering trade using DNA profiling and capture-recapture analysis of market products. Mol Ecol 16:2617–2626CrossRefPubMedGoogle Scholar
  9. Baker CS, Hamner RM, Brownell RLJ, Wade PR (2010) Stock structure of western North Pacific minke whales based on mtDNA haplogroups from ‘bycatch’ and scientific whaling. International Whaling Commission. Working group report, 31 March 2010Google Scholar
  10. Béné C (2005) Increasing the contribution of small-scale fisheries to poverty alleviation and food security. In: Nations Faaoot U (ed) FAO Technical Guidelines for Responsible Fisheries. Rome, 79 ppGoogle Scholar
  11. Bensasson D, Zhang D, Hartl DL, Hewitt GM (2001) Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends Ecol Evol 16:314–321CrossRefPubMedGoogle Scholar
  12. Berrios R (1983) In: Centre IDR (ed) Towards an overview of Peru’s fishing industry: problems and prospects. Regional Office for Latin America and the CaribbeanGoogle Scholar
  13. Bérubé M, Palsbøll P (1996) Identification of sex in cetaceans by multiplexing with three ZFX and ZFY specific primers. Mol Ecol 5:283–287PubMedGoogle Scholar
  14. Brown MR, Corkeron PJ, Hale PT, Schultz KW, Bryden MM (1995) Evidence for a sex-segregated migration in the humpback whale (Megaptera novaeangliae). Proc R Soc Lond B 259:229–234CrossRefGoogle Scholar
  15. Cai J, Leung P, Pan M, Pooley S (2005) Economic linkage impacts of Hawaii’s longline fishing regulations. Fish Res 74:232–242CrossRefGoogle Scholar
  16. Cassens I, Vicario S, Waddell VG et al (2000) Independent adaptation to riverine habitats allowed survival of ancient cetacean lineages. Proc Natl Acad Sci USA 97:11343–11347CrossRefPubMedGoogle Scholar
  17. Cassens I, Van Waerebeek K, Best PB et al (2005) Evidence for male dispersal along the coasts but no migration in pelagic waters in dusky dolphins (Lagenorhynchus obscurus). Mol Ecol 14:107–121CrossRefPubMedGoogle Scholar
  18. Clapham P, Van Waerebeek K (2007) Bushmeat and bycatch: the sum of the parts. Mol Ecol 16:2607–2609CrossRefPubMedGoogle Scholar
  19. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660CrossRefPubMedGoogle Scholar
  20. Collins T, Minton G, Baldwin R et al. (2002) A preliminary assessment of the frequency, distribution and causes of mortality of beach cast cetaceans in the Sultanate of Oman, January 1999 to February 2002. In: IWC Scientific Committee document SC/54/O4. Shimonoseki, JapanGoogle Scholar
  21. Cox TM, Read AJ, Swanner D, Urian K, Waples D (2003) Behavioural response of bottlenose dolphins, Tursiops truncatus, to gillnets and acoustic alarms. Biol Conserv 115:203–212CrossRefGoogle Scholar
  22. D’Agrossa S, Lennert-Cody C, Vidal O (2000) Vaquita bycatch in Mexico’s artisanal gillnets fisheries: driving a small population to extinction. Conserv Biol 14:110–119Google Scholar
  23. Dawson SM (1991) Modifying gillnets to reduce entanglement of cetaceans. Mar Mamm Sci 7:274–282CrossRefGoogle Scholar
  24. Du Buy H, Riley F (1967) Hybridization between the nuclear and kinetoplast DNA’s of Leishmania enriettii and between nuclear and mitochondrial DNA’s of mouse liver. Proc Natl Acad Sci USA 57:790–797CrossRefPubMedGoogle Scholar
  25. García-Godos I (1992) Captura estacional de cetáceos menores en la caleta de Ancón. In: Memoria X Congreso Nacional de Biología. Lima, Peru, pp 273–279Google Scholar
  26. Goodson AD, Mayo RH, Klinowska M, Bloom PRS (1994) Field testing passive acoustic devices designed to reduce the entanglement of small cetaceans in fishing gear. In: Perrin WF, Donovan GP, Barlow J (eds) Gillnets and cetaceans. Reports of the International Whaling Commission. Cambridge, pp 597–605Google Scholar
  27. Haelters J, Camphuysen KCJ (2009) In: Report to IFAW EO, Boulevard Charlemagne 1, Brussels (ed) The harbour porpoise in the southern North Sea: abundance, threats and research- & management proposals. Brussels, Belgium, 56 ppGoogle Scholar
  28. Hellborg L, Ellegren H (2003) Y chromosome conserved anchored tagged sequences (YCATS) for the analysis of mammalian male-specific DNA. Mol Ecol 12:283–291CrossRefPubMedGoogle Scholar
  29. IWC (1994) Report of the workshop on mortality of cetaceans in passive fishing nets and traps. In: Perrin WF, Donovan GP, Barlow J (eds) Gillnets and cetaceans. Reports of the International Whaling Commission. Cambridge, pp 2–71Google Scholar
  30. Kastelein RA, de Haan D, Vaughan N, Staal C, Schooneman NM (2001) The influence of three acoustic alarms on the behavior of harbor porpoises (Phocoena phocoena) in a floating pen. Mar Environ Res 52:351–371CrossRefPubMedGoogle Scholar
  31. Laidre KL, Heagerty PJ, Heide-Jørgensen MP, Witting L, Simon M (2009) Sexual segregation of common minke whales (Balaenoptera acutorostrata) in Greenland, and the influence of sea temperature on the sex ratio of catches. ICES J Mar Sci 66:2253–2266CrossRefGoogle Scholar
  32. Leeney RH, Berrow S, McGrath D et al (2007) Effects of pingers on the behavior of bottlenose dolphins. J Mar Biol Assoc UK 87:129–133CrossRefGoogle Scholar
  33. Lemmon AR, Milinkovitch MC (2002) The metapopulation genetic algorithm: an efficient solution for the problem of large phylogeny estimation. Proc Natl Acad Sci USA 99:10516–10521CrossRefPubMedGoogle Scholar
  34. Lowry N, Teilmann J (1994) Bycatch and bycatch reduction of the harbour porpoise (Phocoena phocoena) in Danish waters. Report to the international Whaling Commision (special issue), vol 15, pp 203–209Google Scholar
  35. Mangel JC, Alfaro-Shigueto J, Van Waerebeek K et al (2010) Small cetacean captures in Peruvian artisanal fisheries: high despite protective legislation. Biol Conserv 143:136–143CrossRefGoogle Scholar
  36. Martin AR, da Silva VMF (2004) River dolphins and flooded forest: seasonal habitat use and sexual segregation of botos (Inia geoffrensis) in an extreme cetacean environment. J Zool 263:295–305*****CrossRefGoogle Scholar
  37. Mattson MC, Mullin KD, Ingram GW, Hoggard W (2006) Age structure and growth of the Bottlenose dolphin (Tursiops truncatus) from strandings in teh Mississippi sound region of the north-central gulf of Mexico from 1986 to 2003. Mar Mammal Sci 22:654–666CrossRefGoogle Scholar
  38. Milinkovitch MC, LeDuc R, Tiedemann R, Dizon AE (2002) Applications of molecular data in cetacean taxonomy and population genetics with special emphasis on defining species boundaries. In: Evans PGH, Raga JA (eds) Marine mammals: biology and conservation. Kluwer Academic Press, New York, pp 325–359Google Scholar
  39. Mucientes GR, Queiroz N, Sousa LL, Tarroso P, Sims DW (2009) Sexual segregation of pelagic sharks and the potential threat from fisheries. Biol Lett 5:156–159CrossRefPubMedGoogle Scholar
  40. Natoli A, Canadas A, Peddemors VM et al (2006) Phylogeography and alpha taxonomy of the common dolphin (Delphinus sp.). J Evol Biol 19:943–954CrossRefPubMedGoogle Scholar
  41. Northridge SP (1996) A review of marine mammal bycatch observer schemes with recommendations for best practice. In: JNCC Report. Aberdeen, UKGoogle Scholar
  42. Peckham SH, Maldonado Diaz D, Walli A et al (2007) Small-scale fisheries bycatch jeopardizes endangered Pacific loggerhead turtles. PLoS One 2:e1041CrossRefPubMedGoogle Scholar
  43. Read AJ, Van Waerebeek K, Reyes JC, McKinnon JS, Lehman LC (1988) The exploitation of small cetaceans in coastal Peru. Biol Conserv 46(1):53–70Google Scholar
  44. Read AJ, Drinker P, Northridge SP (2006) Bycatch of marine mammals in U.S. and global fisheries. Conserv Biol 20:163–169CrossRefPubMedGoogle Scholar
  45. Reeves RR, Berggren P, Crespo EA et al. (2005) Global priorities for reduction of cetacean bycatch. Report to the World Wide Fund for Nature. 29 ppGoogle Scholar
  46. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
  47. Rosa S, Milinkovitch MC, Van Waerebeek K et al (2005) Population structure of nuclear and mitochondrial DNA variation among South American Burmeister’s porpoises (Phocoena spinipinnis). Conserv Genet 6:431–443CrossRefGoogle Scholar
  48. Rosel PE (2003) PCR-based sex determination in Odontocete cetaceans. Conserv Genet 4:647–649CrossRefGoogle Scholar
  49. Rosel PE, Dizon AE, Heyning JE (1994) Genetic analysis of sympatric morphotypes of common dolphins (genus Delphinus). Mar Biol 119:159–167CrossRefGoogle Scholar
  50. Ross HA, Lento GM, Dalebout ML et al (2003) DNA surveillance: web-based molecular identification of whales, dolphins, and porpoises. J Hered 94:111–114CrossRefPubMedGoogle Scholar
  51. Sanino GP, Van Waerebeek K, Van Bressem M, Pastene LA (2005) A preliminary note on population structure in eastern South Pacific common bottlenose dolphins, Tursiops truncatus. J Cetac Res Manag 7:65–70Google Scholar
  52. Tezanos-Pinto G, Baker CS, Russell K et al (2009) A worldwide perspective on the population structure and genetic diversity of bottlenose dolphins (Tursiops truncatus) in New Zealand. J Hered 100:11–24CrossRefPubMedGoogle Scholar
  53. Trippel EA, Wang JY, Strong MB, Carter LS, Conway JD (1996) Incidental mortality of harbour porpoise (Phocoena phocoena) by the gill-net fishery in the lower Bay of Fundy. Can J Fish Aquat Sci 53:1294–1300CrossRefGoogle Scholar
  54. Turner JP, Worthy GAJ (2003) Skull morphometry of bottlenose dolphins (Tursiops truncatus) from the Gulf of Mexico. J Mammal 84:665–672CrossRefGoogle Scholar
  55. UN General Assembly (1991) Large-scale pelagic drift-net fishing and its impact on the living marine resources of the world’s oceans and seas. 79th plenary meeting. A/RES/46/215, 20 December 1991Google Scholar
  56. Van Waerebeek K (1994) A note on the status of the dusky dolphins (Lagenorhynchus obscurus) off Peru. In: Perrin WF, Donovan GP, Barlow J (eds) Gillnets and cetaceans. Reports of the International Whaling Commission. Cambridge, pp 525–527Google Scholar
  57. Van Waerebeek K, Reyes JC (1994a) Interactions between small cetaceans and Peruvian fisheries in 1988/89 and analysis of trends. Reports of the International Whaling Commission. Cambridge, pp 495–502Google Scholar
  58. Van Waerebeek K, Reyes JC (1994b) Post-ban small cetacean takes off Peru: a review. Reports of the International Whaling Commission. Cambridge, pp 503–520Google Scholar
  59. Van Waerebeek K, Reyes JC, Read AJ, McKinnon JS (1990) Preliminary observations of bottlenose dolphins from the Pacific coast of South America. In: Leatherwood S, Reeves RR (eds) The bottlenose dolphin. Academic Press, San Diego, pp 143–154Google Scholar
  60. Van Waerebeek K, Van Bressem M-F, Felix F et al (1997) Mortality of dolphins and porpoises in coastal fisheries off Peru and southern Ecuador in 1994. Biol Conserv 81:43–49CrossRefGoogle Scholar
  61. Van Waerebeek K, Van Bressem M-F, Alfaro-Shigueto J et al. (1999) A preliminary analysis of recent captures of small cetaceans in Peru and Chile. In: IWC Scientific Committee document SC/51/SM17. Grenada, p 12Google Scholar
  62. Van Waerebeek K, Alfaro-Shigueto J, Montes D et al. (2002) Fisheries related mortality of small cetaceans in neritic waters of Peru in 1999–2001. In: IWC Scientific Committee document SC/54/SM10. Shimonoseki, Japan,, p 5Google Scholar
  63. Xiong Y, Brandley MC, Xu S, Zhou K, Yang G (2009) Seven new dolphin mitochondrial genomes and a time-calibrated phylogeny of whales. BMC Evol Biol 9:20CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Athanasia C. Tzika
    • 1
    • 2
  • Eva D’Amico
    • 3
  • Joanna Alfaro-Shigueto
    • 4
    • 5
  • Jeffrey C. Mangel
    • 4
    • 5
  • Koen Van Waerebeek
    • 6
  • Michel C. Milinkovitch
    • 1
  1. 1.Laboratory of Artificial and Natural Evolution (LANE), Department of Genetics and EvolutionUniversity of Geneva, Sciences IIIGenève 4Switzerland
  2. 2.Evolutionary Biology and EcologyUniversité Libre de BruxellesBrusselsBelgium
  3. 3.I.R.I.B.H.M.Université Libre de BruxellesGosseliesBelgium
  4. 4.Pro DelphinusOctavio BernalLima 11Peru
  5. 5.University of Exeter, Center for Ecology and ConservationPenrynUK
  6. 6.Peruvian Centre for Cetacean Research (CEPEC)Museo de Delfines, PucusanaLimaPeru

Personalised recommendations