Skip to main content

Advertisement

Log in

Successful reintroduction of an endangered veteran tree specialist: conservation and genetics of the Great Capricorn beetle (Cerambyx cerdo)

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Habitat fragmentation is one of the main threats to biodiversity. Reintroductions or translocations may mitigate its effects by allowing species with limited dispersal ability to exploit otherwise inaccessible habitat patches. Despite the fact that reintroductions are among the most effective conservation measures, they are rarely used for invertebrates. In this study we investigate the potential of reintroductions as a conservation measure for beetles, and present the first genetic results for an endangered veteran tree specialist. After translocation of 10 adults in 1987, a population of the Great Capricorn beetle reappeared in Hluboká nad Vltavou (Czech Republic) in 1990s. Using population genetic analyses of 79 individuals based on nine microsatellite loci and 82 individuals based on the mitochondrial COI gene we assessed the origin of this population, and compared its genetic variation, population structure and demography to the alleged source population (southern Moravia) and to the closest autochthonous population (Třeboňsko). Although the reintroduced and the closest autochthonous populations are geographically close (24 km), their mutual genetic distance was much higher than that between each of them and the geographically distant (>150 km) potential source population in southern Moravia. The genetic diversity of the reintroduced population was the lowest from the three studied populations and represented a subset of the alleged source population suggesting its establishment due to a translocation from southern Moravia. Despite the lower genetic variation at the reintroduced site, our results suggest that reintroductions could serve as a highly effective measure in biodiversity conservation and in some cases it may be the only chance to prevent extirpation of many endangered 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
Fig. 4

Similar content being viewed by others

References

  • Ahrens D, Fabrizi S, Šipek P, Lago P (2013) Integrative analysis of DNA phylogeography and morphology of the European rose chafer (Cetonia aurata) to infer species taxonomy and patterns of postglacial colonisation in Europe. Mol Phylogenet Evol 39:83–94

    Article  Google Scholar 

  • Albert J, Platek M, Cizek L (2012) Vertical stratification and microhabitat selection by the Great Capricorn Beetle (Cerambyx cerdo) (Coleoptera: Cerambycidae) in open-grown, veteran oaks. Eur J Entomol 109:553–559

    Article  Google Scholar 

  • Alexander KNA (1998) The links between forest history and biodiversity: the invertebrate fauna of ancient pasture-woodlands in Britain and its conservation. In: Kirby KJ, Watkins C (eds) The ecological history of European forests. CAB International, Wallingford, pp 73–80

    Google Scholar 

  • Amaral M, Kozol A, French T (1997) Conservation status and reintroduction of the endangered American burying beetle. Northeast Nat 4:121–132

    Article  Google Scholar 

  • Armstrong DP, Seddon PJ (2008) Directions in reintroduction biology. Trends Ecol Evol 23:20–25

    Article  PubMed  Google Scholar 

  • Audisio P, Brustel H, Carpaneto GM, Coletti G, Mancini E, Trizzino M, Antonini G, De Biase A (2009) Data on molecular taxonomy and genetic diversification of the European Hermit beetles, a species-complex of endangered insects (Coleoptera: Scarabaeidae, Cetoniinae, Osmoderma). J Zool Sys Evol Res 47:88–95

    Article  Google Scholar 

  • Bajomi B, Pullin AS, Stewart GB, Takács-Sánta A (2010) Bias and dispersal in the animal reintroduction literature. Oryx 44:358–365

    Article  Google Scholar 

  • Beebee TJC (2007) Population structure and its implications for conservation of the great silver beetle Hydrophilus piceus in Britain. Freshw Biol 52:2101–2111

    Article  CAS  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2004) GENETIX 4.05, logiciel sous Windows TM pour la genetique des populations. Laboratoire Genome, Populations, Interactions, CNRS UMR 5000, Universite de Montpellier II, Montpellier. http://www.genetix.univ-montp2.fr/genetix/intro.htm. Accessed 22 Jan 2014

  • Berg A, Ehnstrom B, Gustavsson L, Hallingback T, Jonsell M, Weslien J (1994) Threatened plant, animal, and fungus species in Swedish forests: distribution and habitat association. Conserv Biol 8:718–731

    Article  Google Scholar 

  • Buse J, Schröder T, Assmann B (2007) Modelling habitat and spatial distribution of an endangered longhorn beetle—A case study for saproxylic insect conservation. Biol Conserv 137:372–381

    Article  Google Scholar 

  • Buse J, Ranius T, Assmann B (2008) An endangered longhorn beetle associated with old oaks and its possible role as an ecosystem engineer. Conserv Biol 22:329–337

    Article  CAS  PubMed  Google Scholar 

  • Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    Article  CAS  PubMed  Google Scholar 

  • Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660

    Article  CAS  PubMed  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed Central  CAS  PubMed  Google Scholar 

  • Council of the European Communities (1992) Council Directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora. The Member States, OJ L 206

  • David G, Giffard B, Pioul D, Jactel H (2013) Dispersal capacity of Monochamus galloprovincialis, the European vector of the pine wood nematode, on flight mills. J Appl Entomol (in press)

  • Do C, Waples RS, Pell D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NEESTIMATOR v2: re-implementation of software for the estimation of contemporary effective population size (N e ) from genetic data. Mol Ecol Res 14:209–214

    Article  CAS  Google Scholar 

  • Drag L, Hauck D, Pokluda P, Zimmermann K, Cizek L (2011) Demography and dispersal ability of a threatened saproxylic beetle: A mark-recapture study of the Rosalia Longicorn (Rosalia alpina). PLoS ONE. doi:10.1371/journal.pone.0021345

    PubMed Central  PubMed  Google Scholar 

  • Drag L, Kosnar J, Cizek L (2013) Development and characterization of ten polymorphic microsatellite loci for the Great Capricorn beetle (Cerambyx cerdo) (Coleoptera: Cerambycidae). Conserv Genet Res 5:907–909

    Article  Google Scholar 

  • Earl DA, vonHoldt BM (2012) Structure Harvester: a website and program for visualizing Structure output and implementing the Evanno method. Conserv Genet Res 4:359–361

    Article  Google Scholar 

  • Ehnström B, Axelsson R (2002) Insektsgnag i bark och ved. [Insect Galleries in Bark and Wood.] ArtDatabanken SLU, Uppsala, Sweden [in Swedish]

  • Ellwanger G (2009) Conservation status of saproxylic beetles listed in Annexes II and IV of the Habitats Directive at a national (Germany) and biogeographical level. In: Buse J, Alexander KNA, Ranius T, Assmann T (ed) Saproxlic beetles: their role and diversity in european woodland and tree habitats. Proceedings of the 5th symposium and workshop on the conservation of saproxylic beetles. Lüneberg, Germany, pp 107–118

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

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Gibbs JP, Marquez C, Sterling EJ (2008) The Role of Endangered Species Reintroduction in Ecosystem Restoration: Tortoise-Cactus Interactions on Española Island, Galápagos. Restor Ecol 16:88–93

    Article  Google Scholar 

  • Goudet J (2002) Fstat, a Program to estimate and test gene diversities and fixation indices, version 2.9.3.2. http://www.unil.ch/popgen/softwares/fstat.htm. Accessed 22 Jan 2014

  • Hanski IA (2005) Landscape fragmentation, biodiversity loss and the societal response. The longterm consequences of our use of natural resources may be surprising and unpleasant. EMBO Rep 6:388–392

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hanski IA, Gilpin ME (1997) Metapopulation biology: ecology, genetics & evolution. Academic Press, London

    Google Scholar 

  • Hauck D, Cizek L (2006) Inventarizace stromů potenciálně vhodných pro páchníka hnědého (Osmoderma eremita) a tesaříka obrovského (Cerambyx cerdo) v Hluboké nad Vltavou v roce 2006. [Inventory of Trees Suitable for the Hermit Beetle (Osmoderma eremita) and the Great Capricorn Beetle (Cerambyx cerdo) in Hluboka nad Vltavou in 2006.] Report for AOPK, Prague, Czech Republic [in Czech]

  • Hayward MW (2011) Using the IUCN Red List to determine effective conservation strategies. Biodivers Conserv 20:2563–2573

    Article  Google Scholar 

  • IUCN (2013) IUCN red list of threatened species. www.iucnredlist.org. Accessed 22 Jan 2014

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

    Article  CAS  PubMed  Google Scholar 

  • Jonsson M, Johannesen J, Seitz A (2003) Comparative genetic structure of the threatened tenebrionid beetle Oplocephala haemorrhoidalis and its common relative Bolitophagus reticulates. J Insect Conserv 7:111–124

    Article  Google Scholar 

  • Jonsson BG, Kruys N, Ranius T (2005) Ecology of species living on dead wood—Lessons for dead wood management. Silva Fenn 39:289–309

    Article  Google Scholar 

  • Kajtoch L, Mazur M, Kubisz D, Mazur MA, Babik W (2014) Low effective population sizes and limited connectivity in xerothermic beetles: implications for the conservation of an endangered habitat. Anim Conserv. doi:10.1111/acv.12110

    Google Scholar 

  • Karlsson M (2012) Qualities and supply of suitable dead wood for Ceruchus chrysomelinus and its dispersal pattern in a translocated population. Master’s thesis, Swedish University of Agricultural Sciences, Uppsala, Sweden

  • Kletečka Z, Klečka J (2003) Distribution of Cerambyx cerdo L. (Coleoptera, Cerambycidae) in South Bohemia. Acta Musei Bohemiae Meridionalis in České Budějovice 43:71–78

    Google Scholar 

  • Knisley CB, Hill JM, Scherer AM (2005) Translocation of threatened tiger beetle Cicindela dorsalis dorsalis (Coleoptera: Cicindelidae), to Sandy Hook, New Jersey. Ann Entomol Soc Am 98:552–557

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lindenmayer DB, Laurance WF, Franklin JF (2012) Global decline in large old trees. Science 338:1305

    Article  CAS  PubMed  Google Scholar 

  • Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237

    Article  Google Scholar 

  • Martín J, Cabezas J, Buyolo T, Patón D (2005) The relatonship between Cerambyx spp. damage and subsequent Biscogniauxia mediterranum infection on Quercus suber forest. Forest Ecol Manag 216:166–174

    Article  Google Scholar 

  • Miklín J, Čížek (2014) Erasing a European biodiversity hot-spot: open woodlands, veteran trees and mature forests succumb to forestry intensification, logging, and succession in a UNESCO Biosphere Reserve. J Nat Conserv 22:35–41

    Article  Google Scholar 

  • Müller J, Bussler H, Kneib T (2008) Saproxylic beetle assemblages related to silvicultural management intensity and stand structures in a beech forest in Southern Germany. J Insect Conserv 12:107–124

    Article  Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Article  Google Scholar 

  • Nieto A, Alexander KNA (2010) European red list of saproxylic beetles. Publications Office of the European Union, Luxembourg

    Google Scholar 

  • Nothnagle PJ (2002) Population augmentation of the Puritan tiger beetle, Cicindela puritana, through transplantation of larvae to Massachusetts. Unpublished report to the US fish and wildlife service Silvio O. Conte national fish and wildlife refuge, Turners Falls, Massachusetts

  • Oleksa A, Chybicki IJ, Gawroński R, Svensson GP, Burczyk J (2013) Isolation by distance in saproxylic beetles may increase with niche specialization. J Insect Conserv 17:219–233

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Peel D, Waples RS, Macbeth GM, Do C, Ovenden JR (2013) Accounting for missing data in the estimation of contemporary genetic effective population size (Ne). Mol Ecol Res 13:243–253

    Article  CAS  Google Scholar 

  • Perrotti L, Prospero ML, Spevak EM (2001) The effort to save the endangered American burying beetle on a shoe-string budget: making conservation resources go farther with invertebrates. AZAA Conf Proc 2001:189–194

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ranius T (2006) Measuring the dispersal of saproxylic insects: a key characteristic for their conservation. Popul Ecol 48:177–188

    Article  Google Scholar 

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

    Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Sebek P, Altman J, Platek M, Cizek L (2013) Is active management the key to the conservation of saproxylic biodiversity? Pollarding promotes the formation of tree hollows. PLoS ONE DOI:10.1371/journal.pone.0060456

  • Seddon PJ, Armstrong DP, Maloney R (2007) Developing the science of reintroduction biology. Conserv Biol 21:303–312

    Article  PubMed  Google Scholar 

  • Sherley GH, Stringer IAN, Parrish GR (2010) Summary of native bat, reptile, amphibian and terrestrial invertebrate translocations in New Zealand. Science for conservation 303, Department of Conservation, Wellington

  • Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved PCR primers. Ann Entomol Soc Am 87:651–701

    Article  CAS  Google Scholar 

  • Sláma MEF (1998) Tesaříkovití—Cerambycidae České Republiky a Slovenské Republiky. [Longhorn Beetles – Cerambycidae of the Czech Republic and Slovak Republic.] By the author, Krhanice, Czech Republic [in Czech]

  • Smith MT, Bancroft J, Li G, Gao R, Teale S (2001) Dispersal of Anoplophora glabripennis (Cerambycidae). Environ Entomol 30:1036–1040

    Article  Google Scholar 

  • Solano E, Mancini E, Ciucci P, Mason F, Audisio P, Antonini G (2013) The EU protected taxon Morimus funereus Mulsant, 1862 (Coleoptera: Cerambycidae) and its western Palaearctic allies: systematics and conservation outcomes. Conserv Genet 14:683–694

    Article  Google Scholar 

  • Starzyk JR (2004) Cerambyx cerdo (Linnaeus, 1758), Kozioróg dębosz. [Cerambyx cerdo (Linnaeus, 1758), the great capricorn beetle.]. In: Głowacinski Z, Nowacki J (ed) Polska czerwona ksiega zwierzat. Bezkregowce. [Polish Red Data Book of Animals. Invertebrates.] IOP PAN Kraków, AR Poznan, Poland, pp 148–149 [in Polish]

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data III. Cladogram estimation. Genetics 132:619–633

    PubMed Central  CAS  PubMed  Google Scholar 

  • Torres-Vila LM, Sánchez-González Á, Merino-Martínez J, Ponce-Escudero F, Conejo-Rodríguez Y, Martín-Vertedor D, Ferrero-García JJ (2013) Mark–recapture of Cerambyx welensii in dehesa woodlands: dispersal behaviour, population density, and mass trapping efficiency with low trap densities. Entomol Exp Appl 149:273–281

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary N e using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–266

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank to M. Plátek, M. Borovanská for assistance with obtaining samples or molecular analyses, and M. Mende and S. Segar for manuscript review and language correction. The study and its authors were supported by the Agency for Nature Conservation and Landscape Protection of the Czech Republic, Czech Science Foundation (P504/12/1952), and the Project Biodiversity of Forest Ecosystems (CZ.1.07/2.3.00/20.0064) co-financed by the European Social Fund and the state budget of the Czech Republic.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. Drag.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 347 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Drag, L., Cizek, L. Successful reintroduction of an endangered veteran tree specialist: conservation and genetics of the Great Capricorn beetle (Cerambyx cerdo). Conserv Genet 16, 267–276 (2015). https://doi.org/10.1007/s10592-014-0656-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-014-0656-2

Keywords

Navigation