Skip to main content

Advertisement

Log in

Carabus clatratus (Coleoptera: Carabidae): study case of mass rearing and release of a threatened species with new details on its life history

  • ORIGINAL PAPER
  • Published:
Journal of Insect Conservation Aims and scope Submit manuscript

This article has been updated

Abstract

Carabus clatratus is currently known as highly threatened and/or extinct at a European level due to the loss of its habitat, represented by wetlands, to which it is closely linked. In southern Europe, this is much more serious due to the effective adult predation by the alien and invasive crustacean Procambarus clarkii, introduced from the United States of America since the 1980s and now rapidly expanding its range. In an extreme attempt to preserve the Italian native populations of the subspecies C. clatratus antonellii, an effective mass rearing method was developed in 2009. This method, that allowed to record new important data on the biology of the species, is described in detail. Contrary to what is reported in the literature, C. clatratus showed a very high reproductive potential, with an average of 82.8 eggs laid by each female per season. The low prolificacy erroneously attributed to it was wrongly considered a contributing cause of the rarefaction and/or extinction of some of its populations, while the new findings make us focus on other causes. The knowledge of the effective reproductive potential is also important for a better implementation of mass rearings and introduction programs as a function of potential offspring. The duration of the various stages of pre-imaginal development of C. clatratus, from the hatching of the larva to the emergence and appearance of the adults on the ground, is compared with that of another congeneric species living in an extremely unstable habitat (C. stenocephalus susicus) resulting, however, surprisingly even shorter. I hope that other entomologists and conservation biologists will also try their hand at rearing this species (where still present) in an attempt to save it from extinction.

Implications for insect conservation

The new data obtained on the biology and fecundity of C. clatratus, as well as the issues encountered after its release, can be exploited for future initiatives for the species conservation.

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

Similar content being viewed by others

Data availability

Not applicable.

Code availability

Not applicable.

Change history

  • 28 November 2021

    The figures 1 & 2 are replaced with high resolution images.

References

  • Acquistapace P, Cacchiani A, Gherardi F (2006) The impact of the introduced crayfish, Procambarus clarkii, on a lake community in Tuscany. Biol Ambient 20:45–47

    Google Scholar 

  • Anderson R (2005) Northern Ireland priority species: Carabus clatratus—a ground beetle. http://www.habitas.org.uk/priority/species.asp?item=7132. Accessed 17 July 2021

  • Armand J (1975) Notes à propos des élevages de Carabes. Cah Liaison OPIE 16:11–27

    Google Scholar 

  • Armstrong DP, Seddon PJ (2008) Directions in reintroduction biology. Trends Ecol Evol 23:20–25. https://doi.org/10.1016/j.tree.2007.10.003

    Article  PubMed  Google Scholar 

  • Arndt E (1989) Beiträge zur Insektenfauna der DDR: gattung Carabus Linné (Coleoptera; Carabidae). Beitr Entomol 39:63–103

    Google Scholar 

  • Assmann T (2003) Conservation biology. In: Turin H, Penev L, Casale A (eds) The Genus Carabus in Europe. A synthesis. Co-published by Pensoft, Sofia-Moscow & European Invertebrate Survey, Leiden, pp 427–437

    Google Scholar 

  • Baur B, Thommen GH, Coray A (2017) Dynamics of reintroduced populations of Oedipoda caerulescens (Orthoptera, Acrididae) over 21 Years. J Insect Sci 178(1):1–7. https://doi.org/10.1093/jisesa/iew102

    Article  Google Scholar 

  • Bellis J, Bourke D, Williams C, Dalrymple S (2019) Identifying factors associated with the success and failure of terrestrial insect translocations. Biol Conserv 236:29–36. https://doi.org/10.1016/j.biocon.2019.05.008

    Article  Google Scholar 

  • Bomher E, Peiu N, Iconomu L et al (2008) Lista Roşie: a speciilor de floră şi faună sălbatică din zona de graniţă România—Republica Moldova. https://www.yumpu.com/it/document/read/14047287/lista-rosie-management-comun-romania. Accessed 17 July 2021

  • Brandmayr P, Casale A, Puzzo F, Scalercio S (2006) Chronogeonemy analysis: some examples regarding species of the Italian fauna. In: Ruffo S, Stoch F (eds) Ckmap—checklist and distribution of the Italian fauna. Memorie del Museo Civico di Storia Naturale di Verona, 2.Serie, Sezione Scienze della Vita, vol 17, pp 41–45

  • Bucciarelli I (1963) Un interessante reperto faunistico nei dintorni di Milano: il Carabus clathratus antonellii Luigioni. Boll Soc Entomol Ital 93:43–50

    Google Scholar 

  • Burgess AF (1911) Calosoma sycophanta: its life history, behavior, and successful colonization in New England. USDA Bull 101:1–94

    Google Scholar 

  • Burmeister F (1939) Biologie, Ökologie und Verbreitung der europäischen Käfer auf systematischer Grundlage. 1. Band Adephaga, Caraboidea. Goecke and Evers, Krefeld

    Google Scholar 

  • Busato E, Ghittino C, Casale A (2014) Carabus of Subgenus Cathoplius C.G. Thomson, 1875, with description of their life-way, life–cycle and pre-imaginal morphology (Coleoptera, Carabidae). Zootaxa 3866:451–478. https://doi.org/10.11646/zootaxa.3866.4.1

    Article  PubMed  Google Scholar 

  • Cardoso P, Barton PS, Birkhofer K, Chichorro F, Deacon C, Fartmann T, Fukushima CS, Gaigher R, Habel JC, Hallmann CA, Hill MJ, Hochkirch A, Kwak ML, Mammola S, Noriega JA, Orfinger AB, Pedraza F, Pryke JS, Roque FO, Settele J, Simaika JP, Stork NE, Suhling F, Vorster C, Samways MJ (2020) Scientists’ warning to humanity on insect extinctions. Biol Conserv 242:108426. https://doi.org/10.1016/j.biocon.2020.108426

    Article  Google Scholar 

  • Casale A (2018) Estinzioni locali o globali. L’estinzione in entomologia: mito o realtà? Introduzione a una Tavola Rotonda. Atti Accad Naz It Entomol LXVI:143–148

    Google Scholar 

  • Casale A, Busato E (2008) A real time extinction: the case of Carabus clatratus in Italy (Coleoptera Carabidae). In: Penev L, Erwin T, Assmann T (eds) Back to the roots and back to the future? Towards a new synthesis between taxonomic, ecological and biogeographical approaches in carabidology. Pensoft, Sofia, pp 353–362

    Google Scholar 

  • Casale A, Sturani M, Vigna Taglianti A (1982) Coleoptera, Carabidae. I. Introduzione, Paussinae, Carabinae. Fauna d’Italia 18. Calderini, Bologna

    Google Scholar 

  • Casale A, Vigna Taglianti A, Brandmayr P, Colombetta G (2006) Insecta Coleoptera Carabidae (Carabini, Cychrini, Trechini, Abacetini, Stomini, Pterostichini). In: Ruffo S, Stoch F (eds) Ckmap—checklist and distribution of the Italian fauna. Memorie del Museo Civico di Storia Naturale di Verona, 2.Serie, Sezione Scienze della Vita, vol 17, pp 159–163

  • Cavazzuti P, Ghiretti D (2020) Carabus d’Italia. Monografie Entomologiche, vol III. Natura edizioni scientifiche, Bologna

    Google Scholar 

  • Lapouge G (1904) Méthodes d’élevage des larves de Carabes. Bull Soc Sci Nat Ouest Fr 4e trimester, pp 1–15

  • Den Boer PJ (1968) Spreading of risk and stabilization of animal numbers. Acta Biotheor 18:165–194

    Article  Google Scholar 

  • Den Boer PJ, Van Dijk ThS (1996) Life-history patterns among carabid species. Tijdschr Entomol 139:1–16

    Google Scholar 

  • Delmastro GB (1999) Annotazioni sulla storia naturale del gambero della Louisiana Procambarus clarkii (Girard, 1852) in Piemonte centrale e prima segnalazione regionale del gambero americano Orconectes limosus (Rafinesque, 1817) (Crustacea: Decapoda: Astacidea: Cambaridae). Riv Piem St Nat 20:65–92

    Google Scholar 

  • Diamond JM (1996) A-bombs against amphibians. Nature 383:386–387

    Article  CAS  Google Scholar 

  • Drag L, Cizek L (2015) Successful reintroduction of an endangered veteran tree specialis: conservation and genetics of the Great Capricorn beetle (Cerambyx cerdo). Conserv Genet 16:267–276

    Article  Google Scholar 

  • Dumeier AC, Lorenz AW, Kiel E (2018) How to facilitate freshwater macroinvertebrate reintroduction? Limnologica 69:24–27

    Article  Google Scholar 

  • Fabbri R (2007) Modificazioni nella comunità odonatologica nell’oasi di Punte Alberete, Parco del Delta del Po. Riassunti del Convegno: Le libellule in Italia—Ricerche e conservazione. Parco Naturale Valle del Ticino. Cameri 10–11 febbraio 2007, p 12

  • Fradois H (1948) L’élevage des Carabes. Entomologiste 4:1–7

    Google Scholar 

  • Froglia C (2006) Crustacea Malacostraca Decapoda. In: Ruffo S, Stoch F (eds) Ckmap—checklist and distribution of the Italian fauna. Memorie del Museo Civico di Storia Naturale di, Verona, 2.Serie, Sezione Scienze della Vita, vol 17. CD Rom, Magarpatta, pp 113–114

    Google Scholar 

  • Gamradt SC, Kats LB, Anzalone CB (1997) Aggression by non-native crayfish deters breeding in California Newts. Conserv Biol 11:793–796

    Article  Google Scholar 

  • Gherardi F, Baldacchini GN, Barbaresi S, Ercolini P, De Luise G, Mazzoni D, Mori M (1999) The situation in Italy. In: Gherardi F, Holdich DM (eds) Crayfish in Europe as alien species. How to make the best of a bad situation? Crustacean Issues 11, Balkema, Rotterdam, pp 107–128

  • Ghittino C, Busato E, Casale A (2015) Re-establishment of Carabus (Cathoplius) aliai Escalera, 1944 as a separate valid species (Coleoptera, Carabidae). Zookeys 496:61–84. https://doi.org/10.3897/zookeys.496.9428

    Article  Google Scholar 

  • Giglio A, Brandmayr P, Dalpozzo R, Sindona G, Tagarelli A, Talarico F, Zetto Brandmayr T, Ferrero EA (2009) The defensive secretion of Carabus lefebvrei Dejean 1826 pupa (Coleoptera, Carabidae): gland ultrastructure and chemical identification. Microsc Res Tech 72:351–361. https://doi.org/10.1002/jemt.20660

    Article  CAS  PubMed  Google Scholar 

  • Gutiérrez-Yurrita PJ, Sancho G, Bravo MA, Baltanás A, Montes C (1998) Diet of the red swamp crayfish Procambarus clarkii in natural ecosystems of the Doñana National Park temporary fresh-water marsh (Spain). J Crustac Biol 18:120–127

    Article  Google Scholar 

  • Hoffmann KH (1995) Fortpflanzung und Entwicklung. In: Gewecke M (ed) Physiologie der Insekten. Gustav Fischer, Verlag, Stuttgart, pp 69–109

    Google Scholar 

  • Habel JC, Samways MJ, Schmitt T (2019) Mitigating the precipitous decline of terrestrial European insects: requirements for a new strategy. Biodivers Conserv 28:1343–1360

    Article  Google Scholar 

  • Huk T (1998) Ausbreitungsvermögen, Lebenszyklus, Larvalökologie und Habitatwahl von Carabus clatratus (Coleoptera, Carabidae). Angew Carabidol 1:41–50

    Google Scholar 

  • Huk T, Kühne B (1999) Substrate selection by Carabus clatratus (Coleoptera: Carabidae) and its consequences for offspring development. Oecologia 121:348–354

    Article  CAS  PubMed  Google Scholar 

  • Huk T, Kühne B (2000) Egg laying strategy and aspects of larval biology of two Carabus species (Coleoptera, Carabidae). In: Brandmayr P, Lövei G, Zetto Brandmayr T, Casale A, Vigna Taglianti A (eds) Natural history and applied ecology of carabid beetles. Proceedings of the ’IX European Carabidologists’ Meeting, Pensoft, Sofia, pp 161–168

  • Hůrka K (1973) Fortpflanzung und Entwicklung der mitteleuropäischen Carabus– und Procerus-Arten. Stud CSAV 9:1–80

    Google Scholar 

  • INPN—Inventaire national du patrimoine naturel (2021) “Carabus clatratus”. https://inpn.mnhn.fr. Accessed 17 July 2021

  • Kasso M, Balakrishnan M (2013) Ex situ conservation of biodiversity with particular emphasis to Ethiopia. ISRN Biodivers 2013:985037. https://doi.org/10.1155/2013/985037

    Article  Google Scholar 

  • Lövei GL, Sunderland KD (1996) Ecology and behaviour of ground beetles (Coleoptera: Carabidae). Annu Rev Entomol 41:231–256

  • MacArthur R, Wilson OE (1967) The theory of Island biogeography. Princeton University Press, Princeton, p 203

    Google Scholar 

  • Magistretti M (1965) Coleoptera Cicindelidae, Carabidae. Catalogo topografico. Fauna d’Italia, 8. Calderini, Bologna

    Google Scholar 

  • Malausa JC (1977) L’élevage des coléoptères Carabidae: dans la perspective d’une multiplication de masse. Ann Zool Ecol Anim 9:497–505

    Google Scholar 

  • Makarov KV, Sundukov YuN (2016) Distribution and biology of the ground beetle Carabus (Damaster) blaptoides rugipennis (Motschulsky, 1861) on Kunashir Island, Kurile Islands, Russia. Nat Conserv Res 1:44–52. https://doi.org/10.24189/ncr.2016.026

    Article  Google Scholar 

  • National Biodiversity Network (2021) NBN Atlas. https://species.nbnatlas.org/species/NBNSYS0000007132. Accessed 17 July 2021

  • Nelemans MNE (1987) On the life-history of the carabid beetle Nebria brevicollis (F.) (Coleoptera, Carabidae). Neth J Zool 37:26–42

    Article  Google Scholar 

  • Pawłowski J (2004) Carabus clatratus Linnaeus, 1761. Polish Red Data Book of Animals. https://www.iop.krakow.pl/pckz/opis14a3.html?id=38&je=pl. Accessed 17 July 2021

  • Precht H, Christophersen J, Hensel H, Larcher W (1973) Temperature and life. Springer, Berlin

    Book  Google Scholar 

  • Ralls K, Ballou JD (2013) Captive breeding and reintroduction. In: Levin SA (ed) Encyclopedia of biodiversity, 2nd edn. Academic Press, Waltham, MA, pp 662–667. https://doi.org/10.1016/b0-12-226865-2/00041-9

    Chapter  Google Scholar 

  • Raynaud P (1968) Elevage de Carabus (Col. Carabidae). Entomologiste 24:61–65

    Google Scholar 

  • Reznick D, Bryant MJ, Bashey F (2002) r and K-selection revisited: the role of population regulation in life-history evolution. Ecology 83:1509–1520. https://doi.org/10.2307/3071970

    Article  Google Scholar 

  • Robert A (2009) Captive breeding genetics and reintroduction success. Biol Conserv 142(12):2915–2922. https://doi.org/10.1016/j.biocon.2009.07.016

    Article  Google Scholar 

  • Scherney F (1957) Der biologische Wirkungseffekt van Carabiden der Gattung Carabus auf Kartoffelkäferlarven. Verh IV Int Pflanzenschutz-Kongr Hambg 1:1035–1038

    Google Scholar 

  • Skipper L, Calabuig I, Møller J, Wenøe-Breddam D, Skovgaard-Mathorne J (2020) National checklist of all species occurring in Denmark. Version 9.3. Miljøstyrelsen / The Danish Environmental Protection Agency. Checklist dataset https://doi.org/10.15468/bpmaze accessed via GBIF.org on 17 July 2021

    Google Scholar 

  • Sturani M (1962) Osservazioni e ricerche biologiche sul genere Carabus Linnaeus (sensu lato) (Coleoptera Carabidae). Mem Soc Entomol Ital 41:85–202

    Google Scholar 

  • Sturani M (1964) Osservazioni biologiche e morfologiche sul Carabus (Hygrocarabus) variolosus Fabricius (Coleoptera Carabidae). Atti Accad Naz Ital Entomol Rend 11:182–184

    Google Scholar 

  • Sushko G (2019) Key factors affecting the diversity of Sphagnum cover inhabitants with the focus on ground beetle assemblages in Central-Eastern European peat bogs. Community Ecol 20(1):45–52

    Article  Google Scholar 

  • Theodorou K, Couvet D (2014) The efficiency of close inbreeding to reduce genetic adaptation to captivity. Heredity 114(1):38–47

    Article  PubMed  PubMed Central  Google Scholar 

  • Thiele HU (1977) Carabid beetles in their environments—a study on habitat selection by adaptations in physiology and behavior. Springer, Berlin

    Google Scholar 

  • Turin H, Penev L, Casale A (eds) (2003) The Genus Carabus in Europe. A synthesis. Co-published by Pensoft, Sofia-Moscow & European Invertebrate Survey, Leiden

  • Týr V, Dongres V, Kejval Z (2020) Faunistické zprávy ze západních Čech – 14. Coleoptera: mycetophagidae. Západočes Entomol Listy 11:1–2

    Google Scholar 

  • Williams SE, Hoffman EA (2009) Minimizing genetic adaptation in captive breeding programs: a review. Biol Conserv 142:2388–2400

    Article  Google Scholar 

  • Williams CD, Gormally MJ (2010) The effects of blanket bog management on ground beetles (Carabidae) with particular reference to the threatened Carabus clatratus L. Irish Wildlife Manuals 47:1–72. National Parks and Wildlife Service, Department of Environment, Heritage and Local Government, Dublin

Download references

Acknowledgements

I wish to thank my friends and colleagues who, in various ways, have helped me in accomplishing this work: Dr. Valentina Candian (DISAFA, University of Turin) for the statistical processing of rearing data; Prof. Achille Casale (Department of Zoology, University of Sassari); Pierfranco Cavazzuti (Pagno), and Andrea Petrioli (Florence) for the detailed biogeographic indications useful for finding the species in the Chiusi and Montepulciano sites, and for the gift of the first living individuals of Carabus clatratus antonellii, used for the development of the rearing methodology; Dr. Claudio Ghittino (IZSUM, Terni) for his help in the field in collecting the parentals of the individuals used for mass rearing; Dr. Peter John Mazzoglio (DISAFA, University of Turin) for the translation of the text into English; Dr. Dietrich Mossakowski (Institute for Ecology and Evolutionary Biology, University of Bremen) for giving me some living pairs of C. clatratus clatratus; Prof. Rosemarie Tedeschi (DISAFA, University of Turin) for the help in the revision of the manuscript. I would also like to thank the three anonymous reviewers who provided comments and suggestions that greatly improved the manuscript.

Funding

No funding was received for conducting this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Enrico Busato.

Ethics declarations

Conflict of interest

The author has no conflicts of interest to declare that are relevant to the content of this article.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Busato, E. Carabus clatratus (Coleoptera: Carabidae): study case of mass rearing and release of a threatened species with new details on its life history. J Insect Conserv 26, 29–41 (2022). https://doi.org/10.1007/s10841-021-00359-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10841-021-00359-y

Keywords

Navigation