Skip to main content

Advertisement

Log in

Population viability analysis predicts decreasing genetic diversity in ex situ populations of the Itasenpara bitterling Acheilognathus longipinnis from the Kiso River, Japan

  • Full Paper
  • Published:
Ichthyological Research Aims and scope Submit manuscript

Abstract

To conserve endangered species, the maintenance of ex situ captive populations with sustainable genetic diversity is often required, in combination with population viability analysis (PVA). Since 2010, the threatened Itasenpara bitterling Acheilognathus longipinnis lineages in the Kiso region, Japan, have been maintained in ex situ rearing facilities to allow for conservation efforts. In this study, we obtained microsatellite data from DNA extracted from these captive populations to elucidate their genetic diversity and effective population size. The populations of several initial generations indicated a deviation from Hardy–Weinberg equilibrium, probably due to the limited number of extracted founder individuals analyzed. The effective population size of the captive population tended to increase over the course of generations, although the degree of genetic diversity tended to decrease highlighting the concern for the progression of inbreeding. Our prediction based on the PVA suggests that the maintenance of the captive population under the current conditions could lead to extinction of the Itasenpara bitterling in 50 years. In contrast, simultaneously increasing the carrying capacity and individual exchange among populations appears to enhance the effective management of captive Itasenpara bitterling populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Allendorf FQ, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709

    Article  CAS  PubMed  Google Scholar 

  • Araki H, Schmid C (2010) Is hatchery stocking a help or harm? Evidence, limitations and future directions in ecological and genetic surveys. Aquacult 308:S2–S11

    Article  Google Scholar 

  • Baba K, Nishio M, Yamazaki Y (2016) The environmental factors affecting the growth and survival of Itasenpara bitterling in small-scale water tank. Jpn J Conserv Ecol 21:61–66

    Google Scholar 

  • Belkhir K, Borsa P, Chikhi N, Raufaste N, Bonhomme F (1996–2004) GENETIX 4.05, Logiciel Sous Windows TM Pour la Génétique des Populations. Laboratoire Genome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier, France

  • Brook BW, O’Grady JJ, Chapman AP, Burgman MA, Akçakaya HR, Frankham R (2000) Predictive accuracy of population viability analysis in conservation biology. Nature 404:385–387

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783–796

    Article  CAS  PubMed  Google Scholar 

  • Christie MR, Marine ML, French RA, Waples RS, Blouin MS (2012) Effective size of a wild salmonid population is greatly reduced by hatchery supplementation. Heredity 109:254–260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dawson DA, Burland TM, Douglas A, Le comber SC, Bradshaw M (2003) Isolation of microsatellite loci in the freshwater fish, the bitterling Rhodeus sericeus (Teleostei: Cyprinidae). Mol Ecol Notes 3:199–202

    Article  CAS  Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to Quantitative Genetics, 4th edn. Longman, Horlow, UK

    Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to Conservation Genetics. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Frankham R, Bradshaw CJA, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, red list criteria and population viability analyses. Biol Conserv 170:56–63

    Article  Google Scholar 

  • Futuyma DJ (1998) Evolutionary Biology, 3rd eds. Sinauer Associates, Inc, Massachusetts

  • Gautschi B, Müller JP, Schmid B, Shykoff JA (2003) Effective number of breeders and maintenance of genetic diversity in the captive bearded vulture population. Heredity 91:9–16

    Article  CAS  PubMed  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyze spatial genetic structure at the individual or population levels. Mol Ecol Note 2:618–620

    Article  Google Scholar 

  • Ikeya K, Sagawa S, Ohara K (2012) The efforts of the ex situ conservation of endangered deep body bitterling in Nobi-Plain, Japan. Reintroduction 2:121–128

    Google Scholar 

  • IUCN (2008) Wildlife in a changing world: an analysis of the 2008 IUCN red list of threatened species. https://portals.iucn.org/library/efiles/edocs/RL-2009-001.pdf. Accessed 29 June 2016

  • IUCN (2011) Global re-introduction perspectives: 2011. https://portals.iucn.org/library/efiles/edocs/2011-073.pdf. Accessed 29 June 2016

  • IUCN (2012) The IUCN Red List of Threatened Species. Version 2012.2. http://support.iucnredlist.org/. Accessed 29 June 2016

  • Japan Ministry of the Environment (2003) Threatened wildlife of Japan, red data book, 2nd edn. Japan Wildlife Research Center, Tokyo

    Google Scholar 

  • Kalinowski ST (2005) HP-Rare: A computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • Kawamura K (2005) Low genetic variation and inbreeding depression in small isolated populations of the Japanese rosy bitterling, Rhodeus ocellatus kurumeus. Zool Sci 22:517–524

    Article  CAS  PubMed  Google Scholar 

  • Kitamura J, Nishio M (2010) Reproductive ecology and life history of Itasenpara bitterling Acheilognathus longipinnis in a conservation pond in Himi, Toyama, Japan. Jpn J Ichthyol 57:35–42

    Google Scholar 

  • Kitanishi S, Nishio M, Uehara K, Ogawa R, Yokoyama T, Edo K (2013) Patterns of genetic diversity of mitochondrial DNA within captive populations of the endangered itasenpara bitterling: implications for a reintroduction program Environ Biol Fish 96:567–572

    Google Scholar 

  • Kubota H, Watanabe K, Suguro N, Tabe M, Umezawa K, Watanabe S (2010) Genetic population structure and management units of the endangered Tokyo bitterling, Tanakia tanago (Cyprinidae). Conserv Genet 11:2343–2355

    Article  Google Scholar 

  • Kume M, Onoda Y, Negishi JN, Sagawa S, Nagayama S, Kayaba Y (2012) Feeding damage by exotic species, nutria (Myocastor coypus), to unionid mussels in a floodplain water-body of the Kiso River, Japan. Biol Inland Waters 27:41–47

    Google Scholar 

  • Lacy RC, Pollak JP (2014) Vortex: a stochastic simulation of the extinction process. Version 10.0, Chicago Zoological Society, Brookfield, Illinois

  • Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766

    CAS  PubMed  PubMed Central  Google Scholar 

  • Margan SH, Nurthen RK, Montgomery ME, Woodworth LM, Briscoe DA, Frankham R (1998) Single large or several small? Population fragmentation in the captive management of endangered species. Zoo Biol 17:467–480

    Article  Google Scholar 

  • Montgomery ME, Ballou JD, Nurthen RK, England PR, Briscoe DA, Frankham R (1997) Minimizing kinship in captive breeding programs. Zoo Biol 16:377–389

    Article  Google Scholar 

  • Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787

    Article  CAS  Google Scholar 

  • Nguyen TTT, Sunnucks P (2012) Strong population genetic structure and its management implications in the mud carp Cirrhinus molitorella, an indigenous freshwater species subject to an aquaculture and culture-based fishery. J Fish Biol 80:651–668

    Article  CAS  PubMed  Google Scholar 

  • Nishio M, Soliman T, Yamazaki Y (2012) Occurrence and spawning locations of the Itasenpara bitterling (Acheilognathus longipinnis) in the Moo River, Toyama, Japan. Jpn J Ichthyol 59:147–153

    Google Scholar 

  • Nishio M, Kawamoto T, Kawakami R, Edo K, Yamazaki Y (2015) Life history and reproductive ecology of the endangered Itasenpara bitterling Acheilognathus longipinnis (Cyprinidae) in the Himi region, central Japan. J Fish Biol. doi:10.1111/jfb.12739

    PubMed  Google Scholar 

  • Ogawa R (2008) Acheilognathus longipinnis: a symbol fish of flood plains with natural hydrometeorological environments. Jpn J Ichthyol 55:144–148

    Google Scholar 

  • Ohara K, Takagi M (2007) Survey of genetic variation at three microsatellite loci in captive populations of endangered Japanese minnow Aphyocypris chinensis with implications for reduction of inbreeding. Fish Sci 73:156–160

    Article  CAS  Google Scholar 

  • Peel D, Ovenden JR, Peel SL (2004) NeEstimator; software for estimating effective population size, version 1.3. Queensland Government, Department of Primary Industries and Fisheries, Brisbane

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact test and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical test. Evolution 43:223–225

    Article  Google Scholar 

  • Rømer AE, Nørgaar LS, Mikkelsen DMG, Chriél M, Elmeros M, Madsen AB, Pertoldi C, Jensen TH (2015) Population viability analysis of feral raccoon dog (Nyctereutes procyonoides) in Denmark. Arch Biol Sci Belgrade 67:111–117

    Article  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) ARLEQUIN Ver. 2.000: A Software for Population Genetics Data Analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland

  • Shirai Y, Ikeda S, Tajima S (2009) Isolation and characterization of new microsatellite markers for rose bitterlings, Rhodeus ocellatus. Mol Ecol Res 9:1031–1033

    Article  CAS  Google Scholar 

  • Soulé ME (1987) Viable Populations for Conservation. Cambridge University Press, New York

    Book  Google Scholar 

  • Soulé ME, Wilcox BA (1980) Conservation Biology: An Evolutionary-Ecological Perspective. Sinauer Associates Inc, Massachusetts

    Google Scholar 

  • Sweigart A, Karoly K, Jones A, Willis JH (1999) The distribution of individual inbreeding coefficients and pairwise relatedness in a population of Mimulus guttatus. Heredity 83:625–632

    Article  PubMed  Google Scholar 

  • Thuo DN, Junga JO, Kamau JM, Amimo JO, Kibegwa FM, Githui KE (2015) Population viability analysis of black rhinoceros (Diceros bicornis michaeli) in Lake Nakuru National Park, Kenya. Biodivers Endanger Species 3:1–5

    Google Scholar 

  • Vera M, Sanz N, Hansen MM, Almodóvar A, García-Marín JL (2010) Population and family structure of brown trout, Salmo trutta, in a Mediterranean stream. Mar Freshwater Res 61:676–685

    Article  Google Scholar 

  • Volampeno MSN, Randriatahina GH, Kalle R, Wilson AL, Downs CT (2015) A preliminary population viability analysis of the critically endangered blue-eyed black lemur (Eulemur flavifrons). Afr J Ecol 53:419–427

    Article  Google Scholar 

  • Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756

    Article  PubMed  Google Scholar 

  • Watanabe K, Ichiyanagi H, Abe T, Iwata A (2014) Population viability analysis for the endangered loach Parabotia curtus in the Lake Biwa-Yodo River system, central Japan. Japan J Ichthyol 61:69–83

    Google Scholar 

  • Willoughby JR, Fernandez NB, Lamb MC, Ivy JA, Lacy RC, Dewoody A (2015) The impacts of inbreeding, drift and selection on genetic diversity in captive breeding populations. Mol Ecol 24:98–110

    Article  CAS  PubMed  Google Scholar 

  • Witzenberger KA, Hochkirch A (2011) Ex situ conservation genetics: a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species. Biodivers Conserv 20:1843–1861

    Article  Google Scholar 

  • Woodworth LM, Montgomery ME, Briscoe DA, Frankham R (2002) Rapid genetic deterioration in captive populations: causes and conservation implications. Conserv Genet 3:277–288

    Article  CAS  Google Scholar 

  • Yamazaki Y, Nakamura T, Sasaki M, Nakano S, Nishio M (2014) Decreasing genetic diversity in wild and captive populations of endangered Itasenpara bitterling (Acheilognathus longipinnis) in the Himi region, central Japan, and recommendations for conservation. Conserv Genet 15:921–932

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to the members of the Gifu World Fresh Water Aquarium, Gifu Prefectural Research Institute for Fisheries and Aquatic Environments, and Hekinan Seaside Aquarium for their support in rearing fish and completing experiments. We also thank Shiro Sagawa from the Hyogo Prefectural University and Masaki Nishio on the Board of Education in Himi City, for their invaluable suggestions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yuji Yamazaki.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yamazaki, Y., Ikeya, K., Goto, K. et al. Population viability analysis predicts decreasing genetic diversity in ex situ populations of the Itasenpara bitterling Acheilognathus longipinnis from the Kiso River, Japan. Ichthyol Res 64, 54–63 (2017). https://doi.org/10.1007/s10228-016-0540-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10228-016-0540-9

Keywords

Navigation