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Securing genetic integrity in freshwater pearl mussel propagation and captive breeding

  • 1.

    Geist, J. Integrative freshwater ecology and biodiversity conservation. Ecol. Indic. 11, 1507–1516 (2011).

    Article 

    Google Scholar 

  • 2.

    Lopes-Lima, M. et al. Conservation status of freshwater mussels in Europe: State of the art and future challenges. Biol. Rev. 92, 572–607 (2017).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 3.

    Geist, J. Strategies for the conservation of endangered freshwater pearl mussels (Margaritifera margaritifera L.): A synthesis of conservation genetics and ecology. Hydrobiologia 644, 69–88 (2010).

    Article 

    Google Scholar 

  • 4.

    Taeubert, J. E. & Geist, J. The relationship between the freshwater pearl mussel (Margaritifera margaritifera) and its hosts. Biol. Bull. 44, 67–73 (2017).

    Article 

    Google Scholar 

  • 5.

    Salonen, J. K. et al. Atlantic salmon (Salmo salar) and brown trout (Salmo trutta) differ in their suitability as a host for the endangered freshwater pearl mussel (Margaritifera margaritifera) in northern Fennoscandian rivers. Freshw. Biol. 62, 1346–1358 (2017).

    Article 

    Google Scholar 

  • 6.

    Geist, J. & Auerswald, K. Physicochemical stream bed characteristics and recruitment of the freshwater pearl mussel (Margaritifera margaritifera). Freshw. Biol. 52, 2299–2316 (2007).

    Article 

    Google Scholar 

  • 7.

    Stoeckl, K., Denic, M. & Geist, J. Conservation status of two endangered freshwater mussel species in Bavaria, Germany: Habitat quality, threats, and implications for conservation management. Aquat. Conserv. 30, 647–661 (2020).

    Article 

    Google Scholar 

  • 8.

    Auerswald, K. & Geist, J. Extent and cause of siltation in a headwater stream bed: Catchment and soil erosion is less important than internal stream processes. Land Degrad. Dev. 29, 737–748. https://doi.org/10.1002/ldr.2779 (2018).

    Article 

    Google Scholar 

  • 9.

    Bauer, G. Threats to the freshwater pearl mussel Margaritifera margaritifera L. in central Europe. Biol. Conserv. 45, 239–253 (1988).

    Article 

    Google Scholar 

  • 10.

    Boon, P. J. et al. Developing a standard approach for monitoring freshwater pearl mussel (Margaritifera margaritifera) populations in European rivers. Aquat. Conserv. 29, 1365–1379 (2019).

    Article 

    Google Scholar 

  • 11.

    Hruska, J. Nahrungsansprüche der Flußperlmuschel und deren halbnatürliche Aufzucht in der Tschechischen Republik (Dietary requirements and semi-natural rearing of freshwater pearl mussel in the Czech Republic). Heldia 4, 69–79 (1999).

    Google Scholar 

  • 12.

    Preston, S. J., Keys, A. & Roberts, D. Culturing freshwater pearl mussel Margaritifera margaritifera: A breakthrough in the conservation of an endangered species. Aquat. Conserv. 17, 539–549. https://doi.org/10.1002/aqc.799 (2007).

    Article 

    Google Scholar 

  • 13.

    Thomas, G. R., Taylor, J. & de Leaniz, C. G. Captive breeding of the endangered freshwater pearl mussel, Margaritifera margaritifera. Endanger. Species Res. 12, 1–9 (2010).

    Article 

    Google Scholar 

  • 14.

    Gum, B., Lange, M. & Geist, J. A critical reflection on the success of rearing and culturing juvenile freshwater mussels with a focus on the endangered freshwater pearl mussel (Margaritifera margaritifera L.). Aquat. Conserv. 21, 743–751 (2011).

    Article 

    Google Scholar 

  • 15.

    Geist, J., Rottmann, O., Schröder, W. & Kühn, R. Development of microsatellite markers for the endangered freshwater pearl mussel Margaritifera margaritifera L. (Bivalvia: Unionoidea). Mol. Ecol. Resour. 3, 444–446 (2003).

    CAS 
    Article 

    Google Scholar 

  • 16.

    Geist, J. & Kühn, R. Genetic diversity and differentiation of central European freshwater pearl mussel (Margaritifera margaritifera L.) populations: Implications for conservation and management. Mol. Ecol. 14, 425–439 (2005).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 17.

    Geist, J. & Kuehn, R. Host-parasite interactions in oligotrophic stream ecosystems: The roles of life history strategy and ecological niche. Mol. Ecol. 17, 997–1008 (2008).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 18.

    Marchordom, A., Araujo, R., Erpenbeck, D. & Ramos, M. A. Phylogeography and conservation genetics of the endangered European Margaritiferidae (Bivalvia: Unionoidea). Biol. J. Linn. Soc. Lond. 78, 235–252 (2003).

    Article 

    Google Scholar 

  • 19.

    Stoeckle, et al. Strong genetic differentiation and low genetic diversity of the freshwater pearl mussel (Margaritifera margaritifera L.) in the southwestern European distribution range. Conserv. Genet. 18, 147–157 (2017).

    Article 

    Google Scholar 

  • 20.

    Karlsson, S., Larsen, B. M. & Hindar, K. Host-dependent genetic variation in freshwater pearl mussel (Margaritifera margaritifera L.). Hydrobiologia 735, 179–190 (2014).

    Article 

    Google Scholar 

  • 21.

    Geist, J., Söderberg, H., Karlberg, A. & Kuehn, R. Drainage-independent genetic structure and high genetic diversity of endangered freshwater pearl mussels (Margaritifera margaritifera) in northern Europe. Conserv. Genet. 11, 1339–1350 (2010).

    Article 

    Google Scholar 

  • 22.

    Geist, et al. Genetic structure of Irish freshwater pearl mussels (Margaritifera margaritifera and Margaritifera durrovensis): Validity of subspecies, roles of host fish, and conservation implications. Aquat. Conserv. 28, 923–933 (2018).

    Article 

    Google Scholar 

  • 23.

    Zanatta, et al. High genetic diversity and low differentiation in North American Margaritifera margaritifera (Bivalvia: Unionida: Margaritiferidae). Biol. J. Linn. Soc. Lond. 123, 850–863 (2018).

    Article 

    Google Scholar 

  • 24.

    Taeubert, J. E., Denic, M., Gum, B., Lange, M. & Geist, J. Suitability of different salmonid strains as hosts for the endangered freshwater pearl mussel (Margaritifera margaritifera). Aquat. Conserv. 20, 728–734 (2010).

    Article 

    Google Scholar 

  • 25.

    Marwaha, et al. Host (Salmo trutta) age influences resistance to infestation by freshwater pearl mussel (Margaritifera margaritifera) glochidia. Parasitol. Res. 118, 1519–1532 (2019).

    PubMed 
    Article 

    Google Scholar 

  • 26.

    Taeubert, J. E., Gum, B. & Geist, J. Variable development and excystment of freshwater pearl mussel (Margaritifera margaritifera L.) at constant temperature. Limnologica 43, 319–322 (2013).

    Article 

    Google Scholar 

  • 27.

    Taeubert, J. E. & Geist, J. Critical swimming speed of brown trout (Salmo trutta) infested with freshwater pearl mussel (Margaritifera margaritifera) glochidia and implications for artificial breeding of an endangered mussel species. Parasitol. Res. 112, 1607–1613 (2013).

    PubMed 
    Article 

    Google Scholar 

  • 28.

    Marwaha, J., Jensen, K. H., Jakobsen, P. J. & Geist, J. Duration of the parasitic phase determines subsequent performance in juvenile freshwater pearl mussels (Margaritifera margaritifera). Ecol. Evol. 7, 1375–1383 (2017).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 29.

    Eybe, T., Thielen, F., Bohn, T. & Sures, B. Influence of the excystment time on the breeding success of juvenile freshwater pearl mussels (Margaritifera margaritifera). Aquat. Conserv. 25, 21–30 (2015).

    Article 

    Google Scholar 

  • 30.

    Denic, M., Taeubert, J. E. & Geist, J. Trophic relationships between the larvae of two freshwater mussels and their fish hosts. Invertebr. Biol. 134, 129–135 (2015).

    Article 

    Google Scholar 

  • 31.

    Denic, M. et al. Influence of stock origin and environmental conditions on the survival and growth of juvenile freshwater pearl mussels (Margaritifera margaritifera) in a cross-exposure experiment. Limnologica 50, 67–74 (2015).

    CAS 
    Article 

    Google Scholar 

  • 32.

    Hyvärinen, H. S. H., Chowdhury, M. M. R. & Taskinen, J. Pulsed flow-through cultivation of Margaritifera margaritifera: Effects of water source and food quantity on the survival and growth of juveniles. Hydrobiologia. 3219–3229 (2021).

  • 33.

    Hyvärinen, H., Saarinen-Valta, M., Mäenpää, E. & Taskinen, J. Effect of substrate particle size on burrowing of the juvenile freshwater pearl mussel Margaritifera margaritifera. Hydrobiologia https://doi.org/10.1007/s10750-021-04522-z (2021).

    Article 

    Google Scholar 

  • 34.

    Taskinen, J. et al. Effect of pH, iron and aluminum on survival of early life history stages of the endangered freshwater pearl mussel, Margaritifera margaritifera. Toxicol. Environ. Chem. 93, 1764–1777 (2011).

    CAS 
    Article 

    Google Scholar 

  • 35.

    Lavictoire, L., Moorkens, E., Ramsay, A. & Sweeting, R. Effects of substrate size and cleaning regime on growth and survival of captive-bred juvenile freshwater pearl mussels, Margaritifera margaritifera (Linnaeus, 1758). Hydrobiologia 766, 89–102 (2016).

    Article 

    Google Scholar 

  • 36.

    Eybe, T., Thielen, F., Bohn, T. & Sures, B. The first millimetre: Rearing juvenile freshwater pearl mussels (Margaritifera margaritifera L.) in plastic boxes. Aquat. Conserv. 23, 964–975 (2013).

    Article 

    Google Scholar 

  • 37.

    Strayer, D. L., Geist, J., Haag, W. R., Jackson, J. K. & Newbold, J. D. Essay: Making the most of recent advances in freshwater mussel propagation and restoration. Conserv. Sci. Pract. 1, e53. https://doi.org/10.1111/csp2.53 (2019).

    Article 

    Google Scholar 

  • 38.

    Patterson, M. A. et al. Freshwater Mussel Propagation for Restoration (Cambridge University Press, 2018).

    Book 

    Google Scholar 

  • 39.

    Gstöttenmayr, D., Scheder, C. & Gumpinger, C. Conservation de la mulette perlière d’eau douce en Autriche: un système d’élevage contrôlé en progrès. Penn ar Bed 222, 45–49 (2015).

    Google Scholar 

  • 40.

    Gumpinger, C., Pichler-Scheder, C. & Huemer, D. Das oberösterreichische Artenschutzprojekt „Vision Flussperlmuschel“. Österreichs Fischerei 69, 259–273 (2016).

    Google Scholar 

  • 41.

    Rice, W. R. Analyzing tables of statistical tests. Evolution 43, 223–225 (1989).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 42.

    DeWoody, J. A. et al. Universal method for producing ROXlabeled size standards suitable for automated genotyping. Biotechniques 37, 348–352. https://doi.org/10.2144/04373BM02 (2004).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 43.

    Goudet, J. Fstat (Version 1.2): A computer program to calculate F-statistics. J. Hered. 86, 485–486 (1995).

  • 44.

    Rousset, F. Genepop’007: A complete reimplementation of the Genepop software for Windows and Linux. Mol. Ecol. Resour. 8, 103–106 (2008).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 45.

    Haldane, J. B. S. An exact test for randomness of mating. J. Genet. 52, 631–635. https://doi.org/10.1007/BF02981502 (1954).

    Article 

    Google Scholar 

  • 46.

    Weir, B. S. & Cockerham, C. C. Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370 (1984).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 47.

    Guo, S. W. & Thompson, E. A. Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48, 361–372 (1992).

    CAS 
    PubMed 
    MATH 
    Article 
    PubMed Central 

    Google Scholar 

  • 48.

    Raymond, M. & Rousset, F. An exact test for population differentiation. Evolution 49, 1280–1283 (1995).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 49.

    Kamvar, Z. N., Tabima, J. F. & Grünwald, N. J. Poppr: An R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2, e281. https://doi.org/10.7717/peerj.281 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 50.

    Jombart, T. Adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405 (2008).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 51.

    Ciofi, C., Beaumont, M. A., Swingland, I. R. & Bruford, M. W. Genetic divergence and units for conservation in the Komodo dragon Varanus komodoensis. Proc. Royal Soc. B 266, 2269–2274 (1999).

    Article 

    Google Scholar 

  • 52.

    Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 53.

    Kopelman, N. M., Mayzel, J., Jakobsson, M., Rosenberg, N. A. & Mayrose, I. CLUMPAK: A program for identifying clustering modes and packaging population structure inferences across K. Mol. Ecol. Resour. 15, 1179–1191 (2015).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 54.

    Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software structure: A simulation study. Mol. Ecol. 14, 2611–2620 (2005).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 55.

    Jakobsson, M. & Rosenberg, N. A. CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806 (2007).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 56.

    Rosenberg, N. A. DISTRUCT: A program for the graphical display of population structure. Mol. Ecol. Notes 4, 137–138 (2004).

    Article 

    Google Scholar 

  • 57.

    Kalinowski, S. T. The computer program STRUCTURE does not reliably identify the main genetic clusters within species: Simulations and implications for human population structure. Heredity 106, 625–632 (2011).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 58.

    Puechmaille, S. J. The program structure does not reliably recover the correct population structure when sampling is uneven: Subsampling and new estimators alleviate the problem. Mol. Ecol. Resour. 16, 608–627 (2016).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 59.

    Jombart, T., Devillard, S. & Balloux, F. Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. BMC Genet. 11, 94 (2010).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 60.

    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL: https://www.R-project.org/ (2019).

  • 61.

    Trushenski, J. T., Whelan, G. E. & Bowker, J. D. Why keep hatcheries? Weighing the economic cost and value of fish production for public use and public trust purposes. Fisheries 43, 285–293 (2018).

    Google Scholar 

  • 62.

    Wacker, S., Larsen, B. M., Jakobsen, P. & Karlsson, S. High levels of multiple paternity in a spermcast mating freshwater mussel. Ecol. Evol. 8, 8126–8134 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 63.

    Wacker, S., Larsen, B. M., Jakobsen, P. & Karlsson, S. Multiple paternity promotes genetic diversity in captive breeding of a freshwater mussel. Glob. Ecol. Conserv. 17, e00564. https://doi.org/10.1016/j.gecco.2019.e00564 (2019).

    Article 

    Google Scholar 

  • 64.

    Garrison, N. L., Johnson, P. D. & Whelan, N. V. Conservation genomics reveals low genetic diversity and multiple parentage in the threatened freshwater mussel, Margaritifera hembeli. Conserv. Genet. https://doi.org/10.1007/s10592-020-01329-8 (2021).

    Article 

    Google Scholar 

  • 65.

    Bauer, G. Reproductive strategy of the freshwater pearl mussel Margaritifera margaritifera. J. Anim. Ecol. 56, 691–704 (1987).

    Article 

    Google Scholar 

  • 66.

    McMurray, S. E. & Roe, K. J. Perspectives on the controlled propagation, augmentation, and reintroduction of freshwater mussels (Mollusca: Bivalvia: Unionoida). Freshw. Mollusk Biol. Conserv. 20, 1–12 (2017).

    Article 

    Google Scholar 

  • 67.

    Geist, J. Seven steps towards improving freshwater conservation. Aquat. Conserv. 25, 447–453 (2015).

    Article 

    Google Scholar 


  • Source: Ecology - nature.com

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