Biological Invasions

, Volume 10, Issue 8, pp 1229–1242 | Cite as

Red shiner invasion and hybridization with blacktail shiner in the upper Coosa River, USA

  • David M. Walters
  • Mike J. Blum
  • Brenda Rashleigh
  • Byron J. Freeman
  • Brady A. Porter
  • Noel M. Burkhead
Original Paper

Abstract

Human disturbance increases the invasibility of lotic ecosystems and the likelihood of hybridization between invasive and native species. We investigated whether disturbance contributed to the invasion of red shiner (Cyprinella lutrensis) and their hybridization with native blacktail shiner (C. venusta stigmatura) in the Upper Coosa River System (UCRS). Historical records indicated that red shiners and hybrids rapidly dispersed in the UCRS via large, mainstem rivers since the mid to late 1990s. We measured the occurrence and abundance of parental species and hybrids near tributary-mainstem confluences and characterized populations at these incipient contact zones by examining variation across morphological traits and molecular markers. Red shiners represented only 1.2% of total catch in tributaries yet introgression was widespread with hybrids accounting for 34% of total catch. Occurrence of red shiners and hybrids was highly correlated with occurrence of blacktail shiners, indicating that streams with native populations are preferentially colonized early in the invasion and that hybridization is a key process in the establishment of red shiners and their genome in new habitats. Tributary invasion was driven by post-F1 hybrids with proportionately greater genomic contributions from blacktail shiner. Occurrence of red shiners and hybrids and the relative abundance of hybrids significantly increased with measures of human disturbance including turbidity, catchment agricultural land use, and low dissolved oxygen concentration. Red shiners are a significant threat to Southeast Cyprinella diversity, given that 41% of these species hybridize with red shiner, that five southeastern drainages are invaded, and that these drainages are increasingly disturbed by urbanization.

Keywords

Land use Turbidity Hybrid swarm Introgression Southeastern fishes Disturbance 

Abbreviations

UCRS

Upper Coosa River System

GMNH

Georgia Museum of Natural History

PCR-RFLP

Polymerase chain reaction restriction fragment length polymorphism

mtDNA

Mitochondrial deoxyribonucleic acid

bp

Base pair

Notes

Acknowledgements

We thank D. Homans for assisting in study design and supervising sample collection, T. Crum, B. Dakin, A. Kuenzi, and C. Tepolt for generating genetic data, C. Straight and M. Reif for compiling and mapping collection data, and K. Oswald for reviewing the manuscript. Although this work was reviewed by US EPA and approved for publication, it may not necessarily reflect official Agency policy. Mention of trade names or commercial products does not constitute endorsement or recommendation for use.

References

  1. Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622CrossRefGoogle Scholar
  2. Boschung HT Jr, Mayden RL (2003) Fishes of Alabama. Smithsonian Books, WashingtonGoogle Scholar
  3. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  4. Burridge CP, Gold JR (2003) Conservation genetic studies of the endangered Cape Fear Shiner, Notropis mekistocholas (Teleostei: Cyprinidae). Conserv Genet 4:219–225CrossRefGoogle Scholar
  5. Candolin U, Salesto T, Evers M (2007) Changed environmental conditions weaken sexual selection in sticklebacks. J Evol Biol 20:233–239PubMedCrossRefGoogle Scholar
  6. Cross FB, Cavin LM (1971) Effects of pollution, especially from feedlots, on fishes in the upper Neosho River basin. Contribution 79. Kansas Water Resources Institute, ManhattanGoogle Scholar
  7. DeVivo JC (1996) Fish assemblages as indicators of water quality within the Apalachiacola-Chattahoochee-Flint (ACF) River basin. Masters Thesis, Institute of Ecology, The University of Georgia, Athens, GAGoogle Scholar
  8. Dimsoski P, Toth GP, Bagley MJ (2000) Microsatellite characterization in central stoneroller Campostoma anomalum (Pisces: Cyprinidae). Mol Ecol 9:2187–2189PubMedCrossRefGoogle Scholar
  9. Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050PubMedCrossRefGoogle Scholar
  10. Falush D, Stephens M, Pritchard JK (2007) Inferences of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578PubMedCrossRefGoogle Scholar
  11. Fuller PL, Nico LG, Wiliams JD (1999) Nonindigenous fishes introduced into inland waters of the United States. American Fisheries Society, Special Publication 27, BethesdaGoogle Scholar
  12. Gido KB, Brown JH (1999) Invasion of North American drainages by alien fish species. Freshw Biol 42:387–399CrossRefGoogle Scholar
  13. Girard P, Angers B (2006) Characterization of microsatellite loci in longnose dace (Rhinichthys cataractae) and interspecific amplification in five other Leusciscinae species. Mol Ecol Notes 6:69–71CrossRefGoogle Scholar
  14. Glantz SA, Slinker BK (1990) Primer of applied regression and analysis of variance. McGraw-Hill, Inc., New YorkGoogle Scholar
  15. Greger PD, Deacon JE (1988) Food partitioning among fishes of the Virgin River. Copeia 1988:314–323CrossRefGoogle Scholar
  16. Hitt NP, Frissell CA, Muhlfeld CC, Allendorf FW (2003) Spread of hybridization between native westslope cutthroat trout, Oncorhynchus clarki lewisi, and nonnative rainbow trout, Oncorhynchus mykiss. Can J Fish Aquat Sci 60:1440–1451CrossRefGoogle Scholar
  17. Hubbs C, Strawn K (1956) Interfertility between two sympatric fishes, Notropis lutrensis and Notropis venustus. Evolution 10:341–344CrossRefGoogle Scholar
  18. Hubbs C, Kuehne RA, Ball JC (1953) The fishes of the upper Guadalupe river, Texas. Texas J Sci 5:216–244Google Scholar
  19. Hurley JF (1986) Summary: development, testing, and application of wildlife-habitat models—the manager’s viewpoint. In: Verner A, Morrison ML, Ralph CJ (eds) Wildlife 2000: modeling habitat relationships of terrestrial vertebrates. University of Wisconsin Press, Madison, pp 151–153Google Scholar
  20. Johnson CE (1999) The relationship of spawning mode to conservation of North American minnows (Cyprinidae). Environ Biol Fishes 55:21–30CrossRefGoogle Scholar
  21. Jongman RHG, Braak CJFt, Tongeren OFRv (1995) Data analysis in community and landscape ecology. Cambridge University Press, CambridgeGoogle Scholar
  22. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204PubMedCrossRefGoogle Scholar
  23. Larimore RW, Bayley PB (1996) The fishes of Champaign County, Illinois, during a century of alterations of a prairie ecosystem. Ill Nat Hist Survey Bull 35:53–183Google Scholar
  24. Marchetti MP, Light T, Moyle PB, Viers JH (2004) Fish invasions in California watersheds: testing hypotheses using landscape patterns. Ecol Appl 14:1507–1525CrossRefGoogle Scholar
  25. Matthews WJ (1985) Distribution of midwestern fishes on multivariate environmental gradients with emphasis on Notropis lutrensis. Am Midl Nat 113:225–237CrossRefGoogle Scholar
  26. Matthews WJ, Hill LG (1977) Tolerance of the red shiner, Notropis lutrensis (Cyprinidae) to environmental parameters. Southwest Nat 22:89–98CrossRefGoogle Scholar
  27. Matthews WJ, Hill LG (1979) Influence of physico-chemical factors on habitat selection by red shiners, Notropis lutrensis (Pisces: Cyprinidae). Copeia 1979:70–81CrossRefGoogle Scholar
  28. Mendelson TC (2003) Sexual isolation evolves faster than hybrid inviability in a diverse and sexually dimorphic genus of fish (Percidae: Etheostoma). Evolution 57:317–327PubMedGoogle Scholar
  29. Minckley WL, Deacon JE (1968) Southwestern fishes and the enigma of “endangered species”. Science 159:1424–1432PubMedCrossRefGoogle Scholar
  30. Montana G, Pritchard JK (2004) Statistical tests for admixture mapping with case–control and cases-only data. Am J Hum Genet 75:771–789PubMedCrossRefGoogle Scholar
  31. Moyle PB (2002) Inland fishes of California. University of California Press, BerkeleyGoogle Scholar
  32. Moyle PB, Light T (1996) Biological invasions of fresh water: empirical rules and assembly theory. Biol Conserv 78:149–161CrossRefGoogle Scholar
  33. Multi-Resolution Land Characteristics Consortium (1992) National Land Cover Dataset (NLCD 1992). Retrieved from http://www.landcover.usgs.gov/natllandcover.php on April 2005
  34. Natural Resource Spatial Analysis Laboratory (2005a) Georgia GAP land cover database. Retrieved from http://www.narsal.ecology.uga.edu/index.html on April 2005
  35. Natural Resource Spatial Analysis Laboratory (2005b) Metro Atlanta land cover methodology: mapping impervious surface area. Retrieved from http://www.narsal.ecology.uga.edu/index.html on April 2005
  36. Page LM, Smith RL (1970) Recent range adjustments and hybridization of Notropis lutrensis and Notropis spilopterus in Illinois. Trans Ill Acad Sci 63:264–272Google Scholar
  37. Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109CrossRefGoogle Scholar
  38. Ruesink JL (2005) Global analysis of factors affecting the outcome of freshwater fish introductions. Conserv Biol 19:1883–1893Google Scholar
  39. Schmidt TR, Bielawski JP, Gold JR (1998) Morphological phylogenetics and evolution of the cytochrome b gene in the cyprinid genus Lythrurus (Actinopterygii: Cypriniformes). Copeia 1998:14–22CrossRefGoogle Scholar
  40. Seehausen O, van Alphen JJM, Witte F (1997) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277:1808–1811CrossRefGoogle Scholar
  41. Taylor CM, Hastings A (2005) Allee effects in biological invasions. Ecol Lett 8:895–908CrossRefGoogle Scholar
  42. U.S. Census Bureau (2007) State and county quickFacts—Georgia. Retrieved from http://www.quickfacts.census.gov/qfd/states/13000.html on May 2007
  43. U.S. Department of Agriculture (2000) 1997 National resource inventory. Percent change in developed land area 1982–1997. Retrieved from http://www.nrcs.usda.gov/technical/land/meta/m5008.html on August 2007
  44. Wallace RK, Ramsey JS (1982) A new cyprinid hybrid, Notropis lutrensis and N. callitaenia, from the Apalachicola draingage in Alabama. Copeia 1982:214–217CrossRefGoogle Scholar
  45. Walters DM, Leigh DS, Bearden AB (2003a) Urbanization, sedimentation, and the homogenization of fish assemblages in the Etowah River Basin, USA. Hydrobiologia 494:5–10CrossRefGoogle Scholar
  46. Walters DM, Leigh DS, Freeman MC, Freeman BJ, Pringle CM (2003b) Geomorphology and fish assemblages in a Piedmont river basin, U.S.A. Freshw Biol 48:1950–1970CrossRefGoogle Scholar
  47. Warren ML Jr, Burr BM, Walsh SJ, Bart HL Jr, Cashner RC, Etnier DA, Freeman BJ, Kuhajda BR, Mayden RL, Robison HW, Ross ST, Starnes WC (2000) Diversity, distribution, and conservation status of the native freshwater fishes of the southern United States. Fisheries 25:7–31CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • David M. Walters
    • 1
  • Mike J. Blum
    • 1
    • 2
  • Brenda Rashleigh
    • 3
  • Byron J. Freeman
    • 4
  • Brady A. Porter
    • 5
  • Noel M. Burkhead
    • 6
  1. 1.U.S. Environmental Protection Agency, National Exposure Research LaboratoryCincinnatiUSA
  2. 2.Department of Ecology and Evolutionary BiologyTulane UniversityNew OrleansUSA
  3. 3.U.S. Environmental Protection Agency, National Exposure Research LaboratoryAthensUSA
  4. 4.Georgia Museum of Natural History and Odum School of EcologyUniversity of GeorgiaAthensUSA
  5. 5.Department of Biological SciencesDuquesne UniversityPittsburghUSA
  6. 6.U.S. Geological Survey, Florida Integrated Science CenterGainesvilleUSA

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