Conservation Genetics

, Volume 16, Issue 4, pp 801–809 | Cite as

Molecular analyses confirm genetically distinct populations of two indigenous estuarine fish species in an isolated coastal lake: implications for the management of introduced ichthyofauna

  • Nikki Phair
  • Jaco Barendse
  • M. Kyle S. Smith
  • Sophie von der Heyden
Research Article

Abstract

Groenvlei is a coastal, near-freshwater lake in the Garden Route region of South Africa, which became isolated from the ocean about 4,000 years ago due to sea level regression. It contains only two native fish species—Atherina breviceps and Gilchristella aestuaria—and several non-native species, including the illegally introduced common carp (Cyprinus carpio). Options for controlling this highly invasive species in Groenvlei are presently being considered and as such, it is pertinent that the conservation status of native species be assessed. Mitochondrial DNA analyses support significant divergence of both native fish species inhabiting Groenvlei from nearby populations. Additionally, genetic structuring of A. breviceps populations inhabiting other sampling localities was also detected. In Groenvlei, populations of both species displayed slightly lower haplotype diversity and much lower nucleotide diversity than those inhabiting nearby estuaries. Given the level of genetic divergence, native fish populations in Groenvlei should be recognised as a distinct management unit. It is acknowledged that invasive species, such as carp, pose a serious threat to the Groenvlei ecosystem. However, the divergence of the Groenvlei populations—as evidenced by this study—implies that any large-scale actions aimed at removing invasive ichthyofauna should not impact the native species because the unique evolutionary signals of both populations could be destroyed. Our results highlight the importance of incorporating a genetic approach to understanding the evolutionary history of southern African estuarine species and decision-making processes supporting conservation of biodiversity in the region.

Keywords

Groenvlei Introduced ichthyofauna Estuary Atherina breviceps Gilchristella aestuaria Phylogeography South Africa 

References

  1. Allanson B, Baird D (eds) (2008) Estuaries of South Africa. Cambridge University Press, CambridgeGoogle Scholar
  2. Anonymous (1969) Department of Nature Conservation, Provincial Administration of the Cape of Good Hope, Republic of South Africa, Report, No. 25 1968/69Google Scholar
  3. Bajer PG, Sullivan G, Sorensen PW (2009) Effects of a rapidly increasing population of common carp on vegetative cover and waterfowl in a recently restored Midwestern shallow lake. Hydrobiologia 632:235–245CrossRefGoogle Scholar
  4. Bateman MD, Carr AS, Dunajko AC, Holmes PJ, Roberts DL, McLaren SJ, Bryant RG, Marker ME, Murray-Wallace CV (2011) The evolution of coastal barrier systems: a case study of the Middle-Late Pleistocene Wilderness barriers, South Africa. Quat Sci Rev 30:63–81CrossRefGoogle Scholar
  5. Beger M, Selkoe KA, Treml E, Barber PH, von der Heyden S, Crandall ED, Toonen RJ, Riginos C (2014) Evolving coral reef conservation with genetic information. Bull Mar Sci 90:159–185CrossRefGoogle Scholar
  6. Beheregaray LB, Sunnucks P (2001) Fine-scale genetic structure, estuarine colonization and incipient speciation in the marine silverside fish Odontesthes argentinensis. Mol Ecol 10:2849–2866PubMedCrossRefGoogle Scholar
  7. Beheregaray LB, Sunnucks P, Brisco DA (2002) A rapid fish radiation associated with the last sea-level changes in southern Brazil: the silverside Odontesthes perugiae complex. Proc R Soc B 269:65–73PubMedCentralPubMedCrossRefGoogle Scholar
  8. Bermingham E, Avise JC (1986) Molecular zoogeography of freshwater fishes in the southern Unites States. Genetics 113:939–965PubMedCentralPubMedGoogle Scholar
  9. Bossart JL, Pashley Prowell D (1998) Genetic estimates of population structure and gene flow: limitations, lessons and new directions. Trends Ecol Evol 13:202–206PubMedCrossRefGoogle Scholar
  10. Bowen BW, Shanker K, Yasuda N, Malay MCD, von der Heyden S, Paulay G, Rocha LA, Selkoe KA, Barber PH, Williams ST et al (2014) Phylogeography unplugged: comparative surveys in the genomic era. Bull Mar Sci 90:13–46CrossRefGoogle Scholar
  11. Cambray JA (2003) Impact on indigenous species biodiversity caused by the globalisation of alien recreational freshwater fisheries. Hydrobiologia 500:217–230CrossRefGoogle Scholar
  12. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659PubMedCrossRefGoogle Scholar
  13. Coetzee DJ (1980) Zooplankton and environmental conditions in Groenvlei, southern Cape, during 1976. J Limnol Soc S Afr 6:5–11Google Scholar
  14. Coetzee DJ (1982) Stomach content analyses of Gilchristella aestuarius and Hepsetia breviceps from the Swartvlei system and Groenvlei, southern Cape. S Afr J Zool 17:59–66Google Scholar
  15. DeVaney SC, McNyset KM, Williams JB, Peterson AT, Wiley EO (2009) A tale of four “carp”: invasion potential and ecological niche modeling. PLoS ONE 4:e5451PubMedCentralPubMedCrossRefGoogle Scholar
  16. Driver A, Sink, KJ, Nel JN, Holness S, Van Niekerk L, Daniels F, Jonas Z, Majiedt PA, Harris L, Maze K (2012) National Biodiversity Assessment 2011: an assessment of South Africa’s biodiversity and ecosystems. Synthesis Report. South African National Biodiversity Institute and Department of Environmental Affairs, PretoriaGoogle Scholar
  17. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Heled J, Kearse M (2010) Geneious v6. 1.3. Created by Biomatters. Available from http://www.geneious.com/
  18. Ellender BR, Weyl OLF (2014) A review of current knowledge, risk and ecological impacts associated with non-native freshwater fish introductions in South Africa. Aquat Invasions 9:117–132CrossRefGoogle Scholar
  19. Ellender BR, Woodford DJ, Weyl OLF, Cowx IG (2014) Managing conflicts arising from fisheries enhancements based on non-native fishes in southern Africa. J Fish Biol. doi:10.1111/jfb.12512 PubMedGoogle Scholar
  20. 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 10:564–567PubMedCrossRefGoogle Scholar
  21. Francisco SM, Congiu L, von der Heyden S, Almada VC (2011) Multilocus phylogenetic analysis of the genus Atherina (Pisces: Atherinidae). Mol Phylogenet Evol 61:71–78PubMedCrossRefGoogle Scholar
  22. Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752PubMedCrossRefGoogle Scholar
  23. Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426CrossRefGoogle Scholar
  24. Harris LN, Taylor EB (2010) Pleistocene glaciations and contemporary genetic diversity in a Beringian fish, the broad whitefish, Coregonus nasus (Pallas): inferences from microsatellite DNA variation. J Evol Biol 23:72–86PubMedCrossRefGoogle Scholar
  25. Harrison TD, Whitfield AK (1995) Fish community structure in three temporarily open/closed estuaries on the Natal coast. Ichthyol Bull JLB Smith Inst Ichthyol 64:1–80Google Scholar
  26. Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913PubMedCrossRefGoogle Scholar
  27. Illenberger WK (1996) The geomorphologic evolution of the Wilderness dune cordons, South Africa. Quat Int 33:11–20CrossRefGoogle Scholar
  28. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New YorkGoogle Scholar
  29. Klossa-Kilia E, Papasotiropoulos V, Tryfonopoulos G, Alahiotis S, Kilias G (2007) Phylogenetic relationships of Atherina hepsetus and Atherina boyeri (Pisces: Atherinidae) populations from Greece, based on mtDNA sequences. Proc Linn Soc Lond 92:151–161Google Scholar
  30. Koehn JD (2004) Carp (Cyprinus carpio) as a powerful invader in Australian waterways. Freshw Biol 49:882–894CrossRefGoogle Scholar
  31. Lee WJ, Conroy J, Howell WH, Kocher TD (1995) Structure and evolution of teleost mitochondrial control regions. J Mol Evol 41:54–66PubMedCrossRefGoogle Scholar
  32. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452PubMedCrossRefGoogle Scholar
  33. Liu JX, Gao TX, Wu SF, Zhang YP (2007) Pleistocene isolation in the Northwestern Pacific marginal seas and limited dispersal in a marine fish, Chelon haematocheilus (Temminck & Schlegel, 1845). Mol Ecol 16:275–288PubMedCrossRefGoogle Scholar
  34. Lougheed VL, Crosbie B, Chow-Fraser P (1998) Predictions on the effect of common carp (Cyprinus carpio) exclusion on water quality, zooplankton, and submergent macrophytes in a Great Lakes wetland. Can J Fish Aquat Sci 55:1189–1197CrossRefGoogle Scholar
  35. Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world’s worst invasive alien species: a selection from the global invasive species database. Invasive species specialist group of the World Conservation Union (IUCN), AucklandGoogle Scholar
  36. Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197CrossRefGoogle Scholar
  37. Marr SM, Impson ND, Tweddle D (2012) An assessment of a proposal to eradicate non-native fish from priority rivers in the Cape Floristic Region, South Africa. Afr J Aquat Sci 37:131–142CrossRefGoogle Scholar
  38. Martin ARH (1960) The ecology of Groenvlei, a South African fen: part I. The primary communities. J Ecol 48:55–71CrossRefGoogle Scholar
  39. Martin ARH (1962) Evidence relating to the Quaternary history of the Wilderness Lakes. Trans Geol Soc S Afr 65:19–42Google Scholar
  40. McMillan WO, Palumbi SR (1997) Rapid rate of control-region evolution in Pacific butterfly fishes (Chaetodontidae). J Mol Evol 45:473–484PubMedCrossRefGoogle Scholar
  41. Miller SA, Crowl TA (2006) Effects of common carp (Cyprinus carpio) on macrophytes and invertebrate communities in a shallow lake. Freshw Biol 51:85–94CrossRefGoogle Scholar
  42. Mitton JB (1994) Molecular approaches to population biology. Annu Rev Ecol Evol Syst 25:45–69CrossRefGoogle Scholar
  43. Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9:373–375PubMedCrossRefGoogle Scholar
  44. Moritz C (1995) Uses of molecular phylogenies for conservation. Philos Trans R Soc Lond B 349:113–118CrossRefGoogle Scholar
  45. National Environmental Management: Biodiversity Act 10 of 2004, Gazette No. 26436, Notice No. 700. Commencement date: 1 Sept 2004Google Scholar
  46. National Environmental Management: Protected Areas Act 57 of 2003 Gazette No. 26025, Notice No. 181. Commencement date: 1 Nov 2004Google Scholar
  47. Neira FJ, Beckley LE, Whitfield AK (1988) Larval development of the Cape silverside, Atherina breviceps Cuv. and Val., 1835 (Teleostei, Atherinidae) from southern Africa. S Afr J Zool 23:176–183Google Scholar
  48. Olds AA, Smith MKS, Weyl OLF, Russell IA (2011) Invasive alien freshwater fishes in the Wilderness Lakes system, a wetland of international importance in the Western Cape Province, South Africa. Afr Zool 46:179–184CrossRefGoogle Scholar
  49. Palsbøll PJ, Bérubé M, Allendorf FW (2007) Identification of management units using population genetic data. Trends Ecol Evol 22:11–16PubMedCrossRefGoogle Scholar
  50. Parkos JJ, Santucci VJ, Wahl DH (2003) Effects of adult common carp (Cyprinus carpio) on multiple trophic levels in shallow mesocosms. Can J Fish Aquat Sci 60:182–192CrossRefGoogle Scholar
  51. Parsons R (2009) Is Groenvlei really fed by groundwater discharged from the Table Mountain Group (TMG) Aquifer? Water SA 35:657CrossRefGoogle Scholar
  52. Pressey RL, Cabeza M, Watts ME, Cowling RM, Wilson KA (2007) Conservation planning in a changing world. Trends Ecol Evol 22:583–592PubMedCrossRefGoogle Scholar
  53. Ricciardi A, MacIsaac HJ (2011) Impacts of biological invasions on freshwater ecosystems. In: Richardson DM (ed) Fifty years of invasion ecology, 1st edn. Blackwell, Oxford, pp 211–224Google Scholar
  54. Rosenbaum HC, Pomilla C, Mendez M, Leslie M, Best PB, Findlay KP, Minton G, Ersts PJ, Collins TJQ, Engel MH, Bonatto S, Kotze PGH, Meÿer M, Barendse J, Thornton M, Razafindrakoto Y, Ngouessono S, Vely M, Kiszka J (2009) Population structure of humpback whales from their breeding areas in the South Atlantic and Indian Oceans. PLoS ONE 4:e7318PubMedCentralPubMedCrossRefGoogle Scholar
  55. Russell IA, Randall RM, Cole N, Kraaij T, Kruger N (2012) Garden Route National Park, Wilderness coastal section, state of knowledge. South African National Parks. Unpublished reportGoogle Scholar
  56. Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332CrossRefGoogle Scholar
  57. Smith MM, Heemstra PC (1986) Smith’s sea fishes. Springer, Berlin, p 1038CrossRefGoogle Scholar
  58. Teske PR, von der Heyden S, McQuaid CD, Barker NP (2011) A review of marine phylogeography in southern Africa, S Afr J Sci, 107, Art #514Google Scholar
  59. Toms JA, Compton JS, Smale M, von der Heyden S (2014) Variation in palaeo-shorelines explains contemporary population genetic patterns of rocky shore species. Biol Lett 10:20140330PubMedCentralPubMedCrossRefGoogle Scholar
  60. von der Heyden S (2009) Why do we need to integrate population genetics into South African marine protected area planning? Afr J Mar Sci 31:263–269CrossRefGoogle Scholar
  61. von der Heyden S, Lipinski MR, Matthee CA (2010) Remarkably low mtDNA control region diversity in an abundant demersal fish. Mol Phylogenet Evol 55:1183–1188PubMedCrossRefGoogle Scholar
  62. von der Heyden S, Beger M, Toonen RJ, van Herwerden L, Juinio-Meñez A, Ravago-Gotanco R, Fauvelot C, Bernardi G (2014) The application of genetics to marine management and conservation: examples from the Indo-Pacific. Bull Mar Sci 90:123–158CrossRefGoogle Scholar
  63. Vrijenhoek RC (1994) Genetic diversity and fitness in small populations. Conserv Genet 68:37–53CrossRefGoogle Scholar
  64. Waples RS (1991) Pacific salmon, Oncorhynchus spp., and the definition of “species” under the Endangered Species Act. Mar Fish Rev 53:11–22Google Scholar
  65. Whitfield AK (1990) Life-history styles of fishes in South African estuaries. In: Smith JW (ed) Alternative life-history styles of fishes. Springer, NetherlandsGoogle Scholar
  66. Whitfield AK (1994) Fish species diversity in southern African estuarine systems: an evolutionary perspective. Environ Biol Fish 40:37–48CrossRefGoogle Scholar
  67. Whitfield AK (2000) Available scientific information on individual southern African estuarine systems. Water Research Commission Report 577/3/00, p 217Google Scholar
  68. Whitfield AK, Allanson BR, Heinecken TJE (1983) Report No. 22: Swartvlei (CMSII). In: Heydorn AEF, Grindley R (eds) Estuaries of the Cape. Part II. Synopses of available information on individual systems. CSIR Research Report 421, CSIR, StellenboschGoogle Scholar
  69. Winnepenninckx B, Backeljau T, De Wachter R (1993) Extraction of high-molecular-weight DNA from mollusks. Trends Genet 9:407PubMedCrossRefGoogle Scholar
  70. Wright D, Bishop JM, Matthee CA, von der Heyden (2015) Genetic isolation by distance reveals restricted dispersal across a range of life histories: implications for biodiversity planning across highly variable marine environments. Divers Distrib. doi:10.1111/ddi.12302
  71. Zambrano L, Martínez-Meyer E, Menezes N, Peterson AT (2006) Invasive potential of common carp (Cyprinus carpio) and Nile tilapia (Oreochromis niloticus) in American freshwater systems. Can J Fish Aquat Sci 63:1903–1910CrossRefGoogle Scholar
  72. Zavaleta ES, Hobbs RJ, Mooney HA (2001) Viewing invasive species removal in a whole-ecosystem context. Trends Ecol Evol 16:454–459CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Nikki Phair
    • 1
  • Jaco Barendse
    • 2
  • M. Kyle S. Smith
    • 3
  • Sophie von der Heyden
    • 1
  1. 1.Evolutionary Genomics Group, Department of Botany and ZoologyUniversity of StellenboschMatielandSouth Africa
  2. 2.Sustainability Research Unit / South African National ParksNelson Mandela Metropolitan University (George Campus)GeorgeSouth Africa
  3. 3.Scientific Services, South African National Parks, Rondevlei Research StationSedgefieldSouth Africa

Personalised recommendations