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

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.

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References

  1. Allanson B, Baird D (eds) (2008) Estuaries of South Africa. Cambridge University Press, Cambridge

    Google Scholar 

  2. Anonymous (1969) Department of Nature Conservation, Provincial Administration of the Cape of Good Hope, Republic of South Africa, Report, No. 25 1968/69

  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 632:235–245

    Article  Google 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 30:63–81

    Article  Google 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 90:159–185

    Article  Google 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 10:2849–2866

    CAS  PubMed  Article  Google 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 269:65–73

    PubMed Central  PubMed  Article  Google Scholar 

  8. Bermingham E, Avise JC (1986) Molecular zoogeography of freshwater fishes in the southern Unites States. Genetics 113:939–965

    CAS  PubMed Central  PubMed  Google Scholar 

  9. Bossart JL, Pashley Prowell D (1998) Genetic estimates of population structure and gene flow: limitations, lessons and new directions. Trends Ecol Evol 13:202–206

    CAS  PubMed  Article  Google 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 90:13–46

    Article  Google Scholar 

  11. Cambray JA (2003) Impact on indigenous species biodiversity caused by the globalisation of alien recreational freshwater fisheries. Hydrobiologia 500:217–230

    Article  Google Scholar 

  12. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    CAS  PubMed  Article  Google Scholar 

  13. Coetzee DJ (1980) Zooplankton and environmental conditions in Groenvlei, southern Cape, during 1976. J Limnol Soc S Afr 6:5–11

    CAS  Google 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 17:59–66

    Google 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:e5451

    PubMed Central  PubMed  Article  Google 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, Pretoria

  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 9:117–132

    Article  Google 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

    PubMed  Google 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 10:564–567

    PubMed  Article  Google 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 61:71–78

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google 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 89:415–426

    Article  Google 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 23:72–86

    CAS  PubMed  Article  Google 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 64:1–80

    Google Scholar 

  26. Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    CAS  PubMed  Article  Google Scholar 

  27. Illenberger WK (1996) The geomorphologic evolution of the Wilderness dune cordons, South Africa. Quat Int 33:11–20

    Article  Google Scholar 

  28. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York

    Google 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 92:151–161

    Google Scholar 

  30. Koehn JD (2004) Carp (Cyprinus carpio) as a powerful invader in Australian waterways. Freshw Biol 49:882–894

    Article  Google Scholar 

  31. Lee WJ, Conroy J, Howell WH, Kocher TD (1995) Structure and evolution of teleost mitochondrial control regions. J Mol Evol 41:54–66

    CAS  PubMed  Article  Google Scholar 

  32. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    CAS  PubMed  Article  Google 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 16:275–288

    CAS  PubMed  Article  Google 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 55:1189–1197

    Article  Google 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), Auckland

  36. Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197

    Article  Google 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 37:131–142

    Article  Google Scholar 

  38. Martin ARH (1960) The ecology of Groenvlei, a South African fen: part I. The primary communities. J Ecol 48:55–71

    Article  Google Scholar 

  39. Martin ARH (1962) Evidence relating to the Quaternary history of the Wilderness Lakes. Trans Geol Soc S Afr 65:19–42

    Google Scholar 

  40. McMillan WO, Palumbi SR (1997) Rapid rate of control-region evolution in Pacific butterfly fishes (Chaetodontidae). J Mol Evol 45:473–484

    CAS  PubMed  Article  Google Scholar 

  41. Miller SA, Crowl TA (2006) Effects of common carp (Cyprinus carpio) on macrophytes and invertebrate communities in a shallow lake. Freshw Biol 51:85–94

    Article  Google Scholar 

  42. Mitton JB (1994) Molecular approaches to population biology. Annu Rev Ecol Evol Syst 25:45–69

    Article  Google Scholar 

  43. Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9:373–375

    CAS  PubMed  Article  Google Scholar 

  44. Moritz C (1995) Uses of molecular phylogenies for conservation. Philos Trans R Soc Lond B 349:113–118

    Article  Google Scholar 

  45. National Environmental Management: Biodiversity Act 10 of 2004, Gazette No. 26436, Notice No. 700. Commencement date: 1 Sept 2004

  46. National Environmental Management: Protected Areas Act 57 of 2003 Gazette No. 26025, Notice No. 181. Commencement date: 1 Nov 2004

  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 23:176–183

    Google 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 46:179–184

    Article  Google Scholar 

  49. Palsbøll PJ, Bérubé M, Allendorf FW (2007) Identification of management units using population genetic data. Trends Ecol Evol 22:11–16

    PubMed  Article  Google 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 60:182–192

    Article  Google Scholar 

  51. Parsons R (2009) Is Groenvlei really fed by groundwater discharged from the Table Mountain Group (TMG) Aquifer? Water SA 35:657

    Article  Google Scholar 

  52. Pressey RL, Cabeza M, Watts ME, Cowling RM, Wilson KA (2007) Conservation planning in a changing world. Trends Ecol Evol 22:583–592

    PubMed  Article  Google 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 211–224

    Google 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:e7318

    PubMed Central  PubMed  Article  Google 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 report

  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 32:305–332

    Article  Google Scholar 

  57. Smith MM, Heemstra PC (1986) Smith’s sea fishes. Springer, Berlin, p 1038

    Google 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 #514

  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 10:20140330

    PubMed Central  PubMed  Article  Google 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 31:263–269

    Article  Google 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 55:1183–1188

    PubMed  Article  Google 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 90:123–158

    Article  Google Scholar 

  63. Vrijenhoek RC (1994) Genetic diversity and fitness in small populations. Conserv Genet 68:37–53

    Article  Google Scholar 

  64. 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 

  65. Whitfield AK (1990) Life-history styles of fishes in South African estuaries. In: Smith JW (ed) Alternative life-history styles of fishes. Springer, Netherlands

    Google Scholar 

  66. Whitfield AK (1994) Fish species diversity in southern African estuarine systems: an evolutionary perspective. Environ Biol Fish 40:37–48

    Article  Google Scholar 

  67. Whitfield AK (2000) Available scientific information on individual southern African estuarine systems. Water Research Commission Report 577/3/00, p 217

  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, Stellenbosch

  69. Winnepenninckx B, Backeljau T, De Wachter R (1993) Extraction of high-molecular-weight DNA from mollusks. Trends Genet 9:407

    CAS  PubMed  Article  Google 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 63:1903–1910

    Article  Google Scholar 

  72. Zavaleta ES, Hobbs RJ, Mooney HA (2001) Viewing invasive species removal in a whole-ecosystem context. Trends Ecol Evol 16:454–459

    Article  Google Scholar 

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Acknowledgments

This study was assisted by funding from the National Research Foundation by an Innovation Honours bursary awarded to NP. This study would not have been possible without the assistance in sample collection by Keith Spencer, CapeNature staff and Corné Erasmus (Department of Agriculture, Fisheries and Forestry, South Africa). All sampling was authorised by sampling permits to collect in protected areas issued to JB by CapeNature (permit number AAA008-0005-0056 dated 22/08/2012) and SANParks (dated 06/09/2012). The authors thank Stellenbosch University for financial assistance through a Discretionary Grant. JB was supported by a postdoctoral research grant from NMMU: Research Capacity Development and SANParks. Johan Huisamen (CapeNature) is thanked for useful discussions around the alien fish in Groenvlei.

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Correspondence to Sophie von der Heyden.

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Phair, N., Barendse, J., Smith, M.K.S. et al. Molecular analyses confirm genetically distinct populations of two indigenous estuarine fish species in an isolated coastal lake: implications for the management of introduced ichthyofauna. Conserv Genet 16, 801–809 (2015). https://doi.org/10.1007/s10592-015-0701-9

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Keywords

  • Groenvlei
  • Introduced ichthyofauna
  • Estuary
  • Atherina breviceps
  • Gilchristella aestuaria
  • Phylogeography
  • South Africa