Conservation Genetics

, Volume 19, Issue 6, pp 1505–1512 | Cite as

Population genetics of the endangered Maugean skate (Zearaja maugeana) in Macquarie Harbour, Tasmania

  • Kay WeltzEmail author
  • Jeremy M. Lyle
  • Jayson M. Semmens
  • Jennifer R. Ovenden
Research Article


The Maugean skate (Zearaja maugeana) has only been recorded in two remote and isolated estuaries on the west coast of Tasmania, Australia. While the population status in one of these estuaries (Bathurst Harbour) is uncertain, it is likely that Macquarie Harbour now represents the sole remaining habitat for this species. Environmental conditions, in particular dissolved oxygen levels and benthic biodiversity, in Macquarie Harbour have deteriorated in recent years, impacted by increased nutrient inputs from an expanding salmonid aquaculture industry. These environmental changes are believed to pose a threat to the persistence of the Maugean skate. In assessing the risks for this rare and range-restricted species, it is vital to consider genetic information when developing management strategies. Both mitochondrial and microsatellite markers showed that the species has low genetic diversity; with no detectable genetic diversity in over 3000 base pairs surveyed from the mitochondrial genome, low average microsatellite heterozygosity (0.35 ± 0.11), a low average number of alleles per locus (2.1 ± 0.4) across eight microsatellite loci and no overall population structure within the microsatellite loci (Fst = − 0.002, p = 0.718 ± 0.012). There was also evidence of a recent bottleneck or founder event, which may explain the low observed genetic diversity. While the species may have existed with low genetic diversity for many generations, the results of this study represent a flag for conservation concern for the Maugean skate. Given that Macquarie Harbour may be its last remaining habitat, any threats to the species resulting in local extinction could equate to global loss of this unique skate species.


Endangered elasmobranch Genetic diversity Bottleneck/founder event Extinction risk Conservation Environmental health 



This study forms part of a doctoral thesis by Kay Weltz and was supported by a Tasmanian Graduate Research Scholarship, the Winifred Violet Scott Charitable Trust, the Holsworth Wildlife Research Endowment and the Fisheries Research and Development Corporation (Project 2013/008). The authors would like to thank Justin Bell, Graeme Ewing, Edward Forbes, David Moreno and Jaime McAllister for field assistance, and Adam Smolenski and Sharee McCammon for assistance and guidance with the laboratory aspects of the study. All research was conducted with approval from the University of Tasmania Animal Ethics Committee (#A0011882) and the Department of Primary Industries, Parks, Water and Environment (Permit #11055).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Bell JD, Lyle JM, Semmens JM, Awruch C, Moreno D, Currie S, Morash A, Ross J, Barrett N (2016) Movement, habitat utilisation and population status of the endangered Maugean skate and implications for fishing and aquaculture operations in Macquarie Harbour. FRDC Final Report Project No. 2013/008. Institute for Marine and Antarctic Studies, Hobart, January.Google Scholar
  2. Briggs JC (2012) Marine species invasions in estuaries and harbors. Mar Ecol Prog Ser 449:297–302CrossRefGoogle Scholar
  3. Brook BW, Tonkyn DW, O’Grady JJ, Frankham R (2002) Contribution of inbreeding to extinction risk in threatened species. Conserv Ecol 6:16–16CrossRefGoogle Scholar
  4. Chapman DD, Simpfendorfer CA, Wiley TR, Poulakis GR, Curtis C, Tringali M, Carlson JK, Feldheim KA (2011) Genetic diversity despite population collapse in a critically endangered marine fish: the smalltooth sawfish (Pristis pectinata). J Hered 102:643–652CrossRefGoogle Scholar
  5. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedPubMedCentralGoogle Scholar
  6. Edgar GJ, Barrett NS, Graddon DJ (1999) A classification of Tasmanian estuaries and assessment of their conservation significance using ecological and physical attributes, population and land use. Published by the Marine Research Laboratories (Tasmanian Aquaculture and Fisheries Institute), University of TasmaniaGoogle Scholar
  7. Edgar GJ, Last PR, Barrett NS, Gowlett-Holmes K, Driessen M, Mooney P (2010) Conservation of natural wilderness values in the Port Davey marine and estuarine protected area, south-western Tasmania. Aquat Conserv: Mar Freshw Ecosyst 20:297–311CrossRefGoogle Scholar
  8. Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10.3:564–567CrossRefGoogle Scholar
  9. Frankham R, Ballou JD, Briscoe DA (2010) Introduction to conservation genetics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  10. Franklin IR, Frankham R (1998) How large must populations be to retain evolutionary potential? Anim Conserv 1:69–73CrossRefGoogle Scholar
  11. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite data. Mol Ecol 10:305–318CrossRefGoogle Scholar
  12. Griffiths AM, Sims DW, Johnson A, Lynghammar A, McHugh M, Bakken T, Genner MJ (2010) Levels of connectivity between longnose skate (Dipturus oxyrinchus) in the Mediterranean Sea and the northeastern Atlantic Ocean. Conserv Genet 12:577–582CrossRefGoogle Scholar
  13. Hawkins JP, Roberts CM, Clark V (2000) The threatened status of restricted-range coral reef fish species. Anim Conserv 3:81–88CrossRefGoogle Scholar
  14. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649CrossRefGoogle Scholar
  15. Lacy RC (1987) Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection and population subdivision. Conserv Biol 1:143–158CrossRefGoogle Scholar
  16. Last PR, Gledhill DC (2007) The Maugean Skate, Zearaja maugeana sp. nov. (Rajiformes: Rajidae)—a micro-endemic, Gondwanan relict from Tasmanian estuaries. Zootaxa 1494:45–65Google Scholar
  17. Luikart G, Sherwin WB, Steele BM, Allendorf FW (1998) Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Mol Ecol 7:963–974CrossRefGoogle Scholar
  18. Meglécz E, Costedoat C, Dubut V, Gilles A, Malausa T, Pech N, Martin JF (2010) QDD: a user-friendly program to select microsatellite markers and design primers from large sequencing projects. Bioinformatics 26:403–404CrossRefGoogle Scholar
  19. MHDOWG (2015) Macquarie Harbour Dissolved Oxygen Working Group (MHDOWG) Update Report. Department Of Primary Industries, Parks, Water and Environment (DPIPWE). Hobart, Tasmania. Accessed 10 Jan 2016
  20. Nance HA, Klimley P, Galván-Magaña F, Martínez-Ortíz J, Marko PB (2011) Demographic processes underlying subtle patterns of population structure in the scalloped hammerhead shark, Sphyrna lewini. PLoS ONE 6:e21459CrossRefGoogle Scholar
  21. Oliver MK, Piertney SB (2012) Selection maintains MHC diversity through a natural population bottleneck. Mol Biol Evol 29:1713–1720CrossRefGoogle Scholar
  22. Ovenden JR, White RWG (1990) Mitochondrial and allozyme genetics of incipient speciation in an landlocked population of Galaxias truttaceus (Pisces: Galaxiidae). Genetics 124:701–716PubMedPubMedCentralGoogle Scholar
  23. Ovenden J, Peel D, Street R, Courtney A, Hoyle S, Peel S, Podlich H (2007) The genetic effective and adult census size of an Australian population of tiger prawns (Penaeus esculentus). Mol Ecol 16:127–138CrossRefGoogle Scholar
  24. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539CrossRefGoogle Scholar
  25. Peery MZ, Kirby R, Reid BN, Stoelting R, Jonathan N, Robinson S, Va C (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418CrossRefGoogle Scholar
  26. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: A computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  27. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  28. Revill AT, Ross J, Thompson PA (2016) Investigating dissolved oxygen drawdown in Macquarie Harbour. Report to Huon Aquaculture. Commonwealth Scientific and Industrial Research Organisation (CSIRO), Hobart, Tasmania. Accessed 23 June 2017
  29. Ross J, Wild-Allen K, Macleod C (2017) Environmental research in Macquarie Harbour: Understanding oxygen dynamics and the importance for benthic recovery in Macquarie Harbour Progress Report September 2017 FRDC project number 2016/067. Institute for Marine and Antarctic Studies, University of Tasmania, Private Bag 49, Hobart TAS 7001. Accessed 20 Jan 2018
  30. Ross DJ, Hartstein N, Macleod CM, Auluck M, Lucieer V, Cook P, Valentine J (2015) Characterising benthic pelagic interactions in Macquarie Harbour—organic matter processing in sediments and the importance for nutrient dynamics. FRDC Final Report Project No. 2012/047.Google Scholar
  31. Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106CrossRefGoogle Scholar
  32. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386PubMedGoogle Scholar
  33. Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494CrossRefGoogle Scholar
  34. Schluessel V, Broderick D, Collin SP, Ovenden JR (2010) Evidence of extensive population structure in the white spotted eagle ray Aetobatus narinari within the Indo-Pacific inferred from mitochondrial gene sequences. J Zool (London) 281:46–55CrossRefGoogle Scholar
  35. Stow A, Zenger K, Briscoe D, Gillings M, Peddemors V, Otway N, Harcourt R (2006) Isolation and genetic diversity of endangered grey nurse shark (Carcharias taurus) populations. Biol Let 2:308–311CrossRefGoogle Scholar
  36. Taillebois L, Dudgeon C, Maher S, Crook DA, Saunders TM, Barton DP, Taylor JA, Welch DJ, Newman SJ, Travers MJ, Saunders RJ, Ovenden J (2016) Characterization, development and multiplexing of microsatellite markers in three commercially exploited reef fish and their application for stock identification. PeerJ 4:e2418CrossRefGoogle Scholar
  37. Treloar MA, Barrett NS, Edgar GJ (2017) Biology and ecology of Zearaja maugeana, an endangered skate restricted to two south-western Tasmanian estuaries. Mar Freshw Res 68:821–830. CrossRefGoogle Scholar
  38. Vargas-Caro CB, Bustamante C, Bennett MB, Ovenden JR (2016) The complete validated mitochondrial genome of the yellownose skate Zearaja chilensis (Guichenot 1848) (Rajiformes, Rajidae). Mitochondrial DNA Part A 27:1227–1228CrossRefGoogle Scholar
  39. Vargas-Caro C, Bustamante C, Bennett MB, Ovenden JR (2017) Towards sustainable fishery management for skates in South America: the genetic population structure of Zearaja chilensis and Dipturus trachyderma (Chondrichthyes, Rajiformes) in the south-east Pacific Ocean. PLoS ONE 12:1–23CrossRefGoogle Scholar
  40. Williams SM, Pepperell JG, Corley SW, Ovenden JR (2015) Isolation and characterisation of 18 polymorphic microsatellite loci for black marlin (Istiompax indica) and their utility for Pacific billfish species. Fish Res 166:29–32CrossRefGoogle Scholar
  41. Worm B et al (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314:787–790.CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Fisheries and Aquaculture CentreInstitute for Marine and Antarctic Studies (IMAS)TaroonaAustralia
  2. 2.Molecular Fisheries Laboratory, School of Biomedical SciencesUniversity of QueenslandSt LuciaAustralia

Personalised recommendations