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.
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
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
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
Amaral M, Kozol A, French T (1997) Conservation status and reintroduction of the endangered American burying beetle. Northeast Nat 4:121–132
Armstrong DP, Seddon PJ (2008) Directions in reintroduction biology. Trends Ecol Evol 23:20–25
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
Bajomi B, Pullin AS, Stewart GB, Takács-Sánta A (2010) Bias and dispersal in the animal reintroduction literature. Oryx 44:358–365
Beebee TJC (2007) Population structure and its implications for conservation of the great silver beetle Hydrophilus piceus in Britain. Freshw Biol 52:2101–2111
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
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
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
Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631
Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660
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
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
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
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
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
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
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
Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge
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
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
Hanski IA, Gilpin ME (1997) Metapopulation biology: ecology, genetics & evolution. Academic Press, London
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
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
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
Jonsson BG, Kruys N, Ranius T (2005) Ecology of species living on dead wood—Lessons for dead wood management. Silva Fenn 39:289–309
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
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
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
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Lindenmayer DB, Laurance WF, Franklin JF (2012) Global decline in large old trees. Science 338:1305
Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237
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
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
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
Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10
Nieto A, Alexander KNA (2010) European red list of saproxylic beetles. Publications Office of the European Union, Luxembourg
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
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
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
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
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
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Ranius T (2006) Measuring the dispersal of saproxylic insects: a key characteristic for their conservation. Popul Ecol 48:177–188
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138
Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Res 8:103–106
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
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
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
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
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
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
Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Res 8:753–756
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
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
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-014-0656-2