Skip to main content
Log in

The value of semi-natural grasslands for the conservation of carabid beetles in long-term managed forested landscapes

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

Abstract

Species rich semi-natural grasslands are disappearing across Europe, affecting invertebrate diversity negatively. In NW Spain, the recent abandonment of traditional farming practices and the gradual decrease in grazing pressures are reducing the number and extent of montane grasslands. In this context, we investigated the composition of carabid beetle (Coleoptera, Carabidae) assemblages that inhabit semi-natural grasslands situated in long-term managed oak and beech forested landscapes. According to their spatial arrangement, the studied grasslands were classified into: (1) interior or gap grasslands (small and completely surrounded by continuous forest) and (2) exterior grasslands (large and connected to a variety of habitat types). Our results indicate that, within each forested landscape, the gap and exterior grasslands harboured particular carabid assemblages (i.e. exclusive or abundantly collected species), which were also distinct from the surrounding forest carabid fauna. Dissimilarities between gap and exterior grasslands in each landscape suggest great carabid diversity at the regional scale. We also detected species-specific responses as several carabids were mainly associated with gap or exterior grasslands. Consequently, in highly modified forested landscapes, semi-natural grassland remnants may constitute great value for the protection of the carabid fauna. Specifically, we recommend conservation strategies that preserve variety in grassland features and maintain proper management activities to prevent the loss of specialised species and a decrease in regional carabid diversity.

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Batáry P, Báldi A, Szél G, Podlussány A, Rozner I, Erdös S (2007) Responses of grassland specialist and generalist beetles to management and landscape complexity. Divers Distrib 13:196–202

    Article  Google Scholar 

  • Baur B, Cremene C, Groza G, Rakosy L, Schileyko AA, Baur A, Stoll P, Erhardt A (2006) Effects of abandonment of subalpine hay meadows on plant and invertebrate diversity in Transilvania, Romania. Biol Conserv 132:261–273

    Article  Google Scholar 

  • Blanco E, Casado MA, Costa M, Escribano R, García M, Génova M, Gómez A, Gómez F, Moreno JC, Morla C, Regato P, Sáinz H (1997) Los bosques ibéricos. Una interpretación geobotánica. Editorial Planeta, Barcelona

    Google Scholar 

  • Brose U (2003) Bottom-up control of carabid beetle communities in early successional wetlands: mediated by vegetation structure or plant diversity? Oecologia 135:407–413

    PubMed  CAS  Google Scholar 

  • Campos AM (2003) Estudio de los Carabidae (Coleoptera) de Galicia. PhD Thesis, University of Santiago de Compostela, Spain

  • Cole LJ, Pollock ML, Robertson D, Holland JP, McCracken DI (2006) Carabid (Coleoptera) assemblages in the Scottish uplands: the influence of sheep grazing on ecological structure. Entomol Fenn 17:229–240

    Google Scholar 

  • Collinge SK, Palmer TM (2002) The influences of patch shape and boundary contrast on insect response to fragmentation in California grasslands. Landsc Ecol 17:647–656

    Article  Google Scholar 

  • Colwell RK, Coddington JA (1995) Estimating terrestrial biodiversity through extrapolation. In: Hawksworth DL (ed) Biodiversity: measurement and estimation. Chapman & Hall, London, pp 101–118

    Google Scholar 

  • Davies KF, Margules CR (1998) Effects of habitat fragmentation on carabid beetles: experimental evidence. J Anim Ecol 67:460–471

    Article  Google Scholar 

  • De Vries HH (1994) Size of habitat and presence of ground beetle species. In: Desender K et al (eds) Carabid beetles: ecology and evolution. Kluwer, The Netherlands, pp 253–259

    Google Scholar 

  • De Vries W, Vel E, Reinds GJ, Deelstra H, Klap JM, Leeters EEJM, Hendriks CMA, Kerkvoorden M, Landmann G, Herkendell J, Haussmann T, Erisman JW (2003) Intensive monitoring of forest ecosystems in Europe 1. Objectives, set-up and evaluation strategy. For Ecol Manage 174:77–95

    Article  Google Scholar 

  • Del Río S, Penas A (2006) Potential distribution of semi-deciduous forests in Castile and Leon (Spain) in relation to climatic variations. Plant Ecol 185:269–282

    Article  Google Scholar 

  • Dennis P, Aspinall RJ, Gordon IJ (2002) Spatial distribution of upland beetles in relation to landform, vegetation and grazing management. Basic Appl Ecol 3:183–193

    Article  Google Scholar 

  • Di Stefano J (2004) A confidence interval approach to data analysis. For Ecol Manage 187:173–183

    Article  Google Scholar 

  • Fadda S, Henry F, Orgeas J, Ponel P, Buisson E, Dutoit T (2008) Consequences of the cessation of 3000 years of grazing on dry Mediterranean grassland ground-active beetle assemblages. C R Biol 331:532–546

    Article  PubMed  Google Scholar 

  • Forman RTT, Godron M (1986) Landscape ecology. Wiley, New York

    Google Scholar 

  • García LV (2004) Escaping the Bonferroni iron claw in ecological studies. Oikos 105:657–663

    Article  Google Scholar 

  • García D, Quevedo M, Obeso JR, Abajo A (2005) Fragmentation patterns and protection of montane forest in the Cantabrian range (NW Spain). For Ecol Manage 208:29–43

    Article  Google Scholar 

  • García-Ruiz JM, Lasanta T, Ruiz-Flano P, Ortigosa L, White S, González C, Martí C (1996) Land-use changes and sustainable development in mountain areas: a case study in the Spanish Pyrenees. Landsc Ecol 11:267–277

    Article  Google Scholar 

  • Gómez-Limón J, De Lucío Fernández JV (1999) Changes in use and landscape preferences on the agricultural-livestock landscapes of the central Iberian Peninsula (Madrid, Spain). Landsc Urban Plan 44:165–175

    Article  Google Scholar 

  • Grandchamp A-C, Bergamini A, Stofer S, Niemelä J, Duelli P, Scheidegger C (2005) The influence of grassland management on ground beetles (Carabidae, Coleoptera) in Swiss montane meadows. Agric Ecosyst Environ 110:307–317

    Article  Google Scholar 

  • Gutiérrez D, Menéndez R, Méndez M (2004) Habitat-based conservation priorities for carabid beetles within the Picos de Europa National Park, northern Spain. Biol Conserv 115:379–393

    Article  Google Scholar 

  • Halme E, Niemelä J (1993) Carabid beetles in fragments of coniferous forest. Ann Zool Fenn 30:17–30

    Google Scholar 

  • Haysom KA, McCracken DI, Foster GN, Sotherton NW (2004) Developing grassland conservation headlands: response of carabid assemblage to different cutting regimes in a silage field edge. Agric Ecosyst Environ 102:263–277

    Article  Google Scholar 

  • Heliölä J, Koivula M, Niemelä J (2001) Distribution of carabid beetles (Coleoptera, Carabidae) across a boreal forest-clearcut ecotone. Conserv Biol 15:370–377

    Article  Google Scholar 

  • Hodgson JG, Montserrat-Martí G, Tallowin J, Thompson K, Díaz S, Cabido M, Grime JP, Wilson PJ, Band SR, Bogard A, Cabido R, Cáceres D, Castro-Díez P, Ferrer C, Maestro-Martínez M, Pérez-Rontomé MC, Charles M, Cornelissen JHC, Dabber S, Pérez-Harguindeguy N, Krimly T, Sijtsma FJ, Strijker D, Vendramini F, Guerrero-Campo J, Hynd A, Jones G, Romo-Díez A, De Torres Espuny L, Villar-Salvador P, Zak MR (2005) How much will it cost to save grassland diversity? Biol Conserv 122:263–273

    Article  Google Scholar 

  • Irmler U, Hoernes U (2003) Assignment and evaluation of ground beetle (Coleoptera: Carabidae) assemblages to sites on different scales in a grassland landscape. Biodivers Conserv 12:1405–1419

    Article  Google Scholar 

  • Jeannel R (1941–1942) Coléoptères Carabiques. Faune de France, vols 39 and 40. Lechevalier, Paris

  • Jongman RHG, Ter Braak CJF, Van Tongeren OFR (1995) Data analysis in community and landscape ecology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Kinnunen H, Järveläinen K, Pakkala T, Tiainen J (1996) The effect of isolation on the occurrence of farmland carabids in a fragmented landscape. Ann Zool Fenn 33:165–171

    Google Scholar 

  • Koivula M, Vermeulen HJW (2005) Highways and forest fragmentation—effects on carabid beetles (Coleoptera, Carabidae). Landsc Ecol 20:911–926

    Article  Google Scholar 

  • Koivula M, Kukkonen J, Niemelä J (2002) Boreal carabid-beetle (Coleoptera, Carabidae) assemblages along the clear-cut originated succession gradient. Biodivers Conserv 11:1269–1288

    Article  Google Scholar 

  • Koricheva J, Mulder CPH, Schmid B, Joshi J, Huss-Danell K (2000) Numerical responses of different trophic groups of invertebrates to manipulations of plant diversity in grasslands. Oecologia 125:271–282

    Article  Google Scholar 

  • Kotze DJ, O’Hara RB (2003) Species decline—but why? Explanations of carabid beetle (Coleoptera, Carabidae) declines in Europe. Oecologia 135:138–148

    PubMed  Google Scholar 

  • Lindner M, Maroschek M, Netherer S, Kremer A, Barbati A, García-Gonzalo J, Seidl R, Delzon S, Corona P, Kolström M, Lexer MJ, Marchetti M (2010) Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. For Ecol Manage 259:698–709

    Article  Google Scholar 

  • Lindroth CH (1974) Handbooks for the identification of British insects. Coleoptera, Carabidae. Royal Entomological Society, London

    Google Scholar 

  • Luff ML (1996) Use of Carabids as environmental indicators in grasslands and cereals. Ann Zool Fenn 33:185–195

    Google Scholar 

  • Luis-Calabuig E, Tárrega R, Calvo L, Marcos E, Valbuena L (2000) History of landscape changes in Northwest Spain according to land use and management. In: Trabaud L (ed) Life and environment in the Mediterranean. Wit Press, UK, pp 43–86

    Google Scholar 

  • Magura T, Ködöböcz V (2007) Carabid assemblages in fragmented sandy grasslands. Agric Ecosyst Environ 119:396–400

    Article  Google Scholar 

  • Magura T, Ködöböcz V, Tóthmérész B (2001) Effects of habitat fragmentation on carabids in forest patches. J Biogeogr 28:129–138

    Article  Google Scholar 

  • Minns A, Finn J, Hector A, Caldeira M, Joshi J, Palmborg C, Schmid B, Scherer-Lorenzen M, Spehn E, Troumbis A, the BIODEPTH project (2001) The functioning of European grassland ecosystems: potential benefits of biodiversity to agriculture. Agriculture 30(3):179–185

    Google Scholar 

  • Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403–405

    Article  Google Scholar 

  • Muñoz Sobrino C, Ramil-Rego P, Gómez-Orellana L, Ferreiro da Costa J, Díaz Varela RA (2009) Climatic and human effects on the post-glacial dynamics of Fagus sylvatica L. in NW Iberia. Plant Ecol 203:317–340

    Article  Google Scholar 

  • Nakagawa S (2004) A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15:1044–1045

    Article  Google Scholar 

  • Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605

    Article  PubMed  Google Scholar 

  • Niemelä J (2001) Carabid beetles (Coleoptera: Carabidae) and habitat fragmentation: a review. Eur J Entomol 98:127–132

    Google Scholar 

  • Niemelä J, Haila Y, Punttila P (1996) The importance of small-scale heterogeneity in boreal forests: variation in diversity in forest-floor invertebrates across the succession gradient. Ecography 19:352–368

    Google Scholar 

  • O’Hara RB, Kotze DJ (2010) Do not log-transform count data. Methods Ecol Evol 1:118–122

    Article  Google Scholar 

  • Öckinger E, Eriksson AK, Smith HG (2006) Effects of grassland abandonment, restoration and management on butterflies and vascular plants. Biol Conserv 133:291–300

    Article  Google Scholar 

  • Oksanen J, Kindt R, O’Hara B (2005) Community ecology package. R Package Version 1.6-9, VEGAN Package

  • Olea PP, Mateo-Tomás P (2009) The role of traditional farming practices in ecosystem conservation: the case of transhumance and vultures. Biol Conserv 142:1844–1853

    Article  Google Scholar 

  • Ortuño VM, Marcos JM (2003) Los Caraboidea (Insecta: Coleoptera) de la comunidad autónoma del País Vasco, Tomo I. Servicio Central de Publicaciones del Gobierno Vasco, Spain

    Google Scholar 

  • Pärtel M, Bruun HH, Sammul M (2005) Biodiversity in temperate European grasslands: origin and conservation. In: Lillak R, Viiralt R, Linke A, Geherman V (eds) Integrating efficient grassland farming and biodiversity. Estonian Grassland Society, Estonia, pp 1–14

    Google Scholar 

  • Peco B, De Pablos I, Traba J, Levassor C (2005) The effect of grazing abandonment on species composition and functional traits: the case of dehesa grasslands. Basic Appl Ecol 6:175–183

    Article  Google Scholar 

  • Peláez MC (2004) Estudio faunístico, ecológico y biogeográfico de los Carabidae (Coleoptera) del macizo del Sueve (Asturias, España). PhD Thesis, University of León, Spain

  • Penas A, García ME, Herrero L (1995) Series de vegetación. Atlas del medio natural de la provincia de León. Instituto Tecnológico Geominero de España y Diputación de León, León

    Google Scholar 

  • Plieninger T (2006) Habitat loss, fragmentation and alteration—quantifying the impact of land-use changes on a Spanish dehesa landscape by use of aerial photography and GIS. Landsc Ecol 21:91–105

    Article  Google Scholar 

  • Polus E, Vandewoestijne S, Choutt J, Baguette M (2007) Tracking the effects of one century of habitat loss and fragmentation on calcareous grassland butterfly communities. Biodivers Conserv 16:3423–3436

    Article  Google Scholar 

  • Poschlod P, Wallis De Vries MF (2002) The historical and socioeconomic perspective of calcareous grasslands–lessons from the distant and recent past. Biol Conserv 104:361–376

    Article  Google Scholar 

  • Pöyry J, Lindgren S, Salminen J, Kuussaari M (2005) Responses of butterfly and moth species to restored cattle grazing in semi-natural grasslands. Biol Conserv 122:465–478

    Article  Google Scholar 

  • Purtauf T, Dauber J, Wolters V (2004) Carabid communities in the spatio-temporal mosaic of a rural landscape. Landsc Urban Plan 67:185–193

    Article  Google Scholar 

  • R Development Core Team (2005) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org

  • Raworth DA, Choi M-Y (2001) Determining numbers of active carabid beetles per unit area from pitfall-trap data. Entomol Exp Appl 98:95–108

    Article  Google Scholar 

  • Ribera I, Dolédec S, Downie IS, Foster GN (2001) Effect of land disturbance and stress on species traits of ground beetle assemblages. Ecology 82:1112–1129

    Article  Google Scholar 

  • Rodríguez Pascual M (2004) La trashumancia: cultura, cañadas y viajes. Edilesa, León

    Google Scholar 

  • Rozas V (2003) Regeneration patterns, dendroecology, and forest-use history in an old-growth beech-oak lowland forest in Northern Spain. For Ecol Manage 182:175–194

    Article  Google Scholar 

  • Ruiz M, Ruiz JP (1986) Ecological history of transhumance in Spain. Biol Conserv 37:73–86

    Article  Google Scholar 

  • Sánchez de Dios R, Benito-Garzón M, Sainz-Ollero H (2009) Present and future extension of the Iberian submediterranean territories as determined from the distribution of marcescent oaks. Plant Ecol 204:189–205

    Article  Google Scholar 

  • Serrano J (2003) Catálogo de los Carabidae (Coleoptera) de la Península Ibérica. Monografías de la Sociedad Entomológica Aragonesa, vol 9. Zaragoza, Spain

    Google Scholar 

  • Söderström B, Svensson B, Vessby K, Glimskär A (2001) Plants, insects and birds in semi-natural pastures in relation to local habitat and landscape factors. Biodivers Conserv 10:1839–1863

    Article  Google Scholar 

  • Stoate C, Boatman ND, Borralho RJ, Rio Carvalho C, De Snoo GR, Eden P (2001) Ecological impacts of arable intensification in Europe. J Environ Manage 63:337–365

    Article  PubMed  CAS  Google Scholar 

  • Taboada A, Kotze DJ, Salgado JM (2004) Carabid beetle occurrence at the edges of oak and beech forests in NW Spain. Eur J Entomol 101:555–563

    Google Scholar 

  • Taboada A, Kotze DJ, Salgado JM, Tárrega R (2006a) The influence of habitat type on the distribution of carabid beetles in traditionally managed “dehesa” ecosystems in NW Spain. Entomol Fenn 17:284–295

    Google Scholar 

  • Taboada A, Kotze DJ, Tárrega R, Salgado JM (2006b) Traditional forest management: do carabid beetles respond to human-created vegetation structures in an oak mosaic landscape? For Ecol Manage 237:436–449

    Article  Google Scholar 

  • Taboada A, Kotze DJ, Tárrega R, Salgado JM (2008) Carabids of differently aged reforested pinewoods and a natural pine forest in a historically modified landscape. Basic Appl Ecol 9:161–171

    Article  Google Scholar 

  • Tárrega R, Calvo L, Taboada A, García-Tejero S, Marcos E (2009) Abandonment and management in Spanish dehesa systems: effects on soil features and plant species richness and composition. For Ecol Manage 257:731–738

    Article  Google Scholar 

  • Thiele H-U (1977) Carabid beetles in their environments. Springer, New York

    Google Scholar 

  • Thomas CFG, Brown NJ, Kendall DA (2006) Carabid movement and vegetation density: Implications for interpreting pitfall trap data from split-field trials. Agric Ecosyst Environ 113:51–61

    Article  Google Scholar 

  • Trautner J, Geigenmüller K (1987) Tiger beetles, ground beetles: illustrated key to the Cicindelidae and Carabidae of Europe. Margraf, Germany

    Google Scholar 

  • Tscharntke T, Steffan-Dewenter I, Kruess A, Thies C (2002) Contribution of small habitat fragments to conservation of insect communities of grassland-cropland landscapes. Ecol Appl 12:354–363

    Google Scholar 

  • Vanbergen AJ, Woodcock BA, Watt AD, Niemelä J (2005) Effect of land-use heterogeneity on carabid communities at the landscape scale. Ecography 28:3–16

    Article  Google Scholar 

  • Vázquez MG (1990) Estudio faunístico, biogeográfico y ecológico de los Caraboidea (Coleoptera) entre las cuencas de los ríos Bernesga, Torío y Porma (León, España). PhD Thesis, University of León, Spain

  • Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York

    Google Scholar 

  • Walker KJ, Stevens PA, Stevens DP, Mountford JO, Manchester SJ, Pywell RF (2004) The restoration and re-creation of species-rich lowland grassland on land formerly managed for intensive agriculture in the UK. Biol Conserv 119:1–18

    Article  Google Scholar 

  • Wallis De Vries MF, Poschlod P, Willems JH (2002) Challenges for the conservation of calcareous grasslands in northwestern Europe: integrating the requirements of flora and fauna. Biol Conserv 104:265–273

    Article  Google Scholar 

  • White GC, Bennetts RE (1996) Analysis of frequency count data using the negative binomial distribution. Ecology 77:2549–2557

    Article  Google Scholar 

  • Woodcock BA, Pywell RF (2010) Effects of vegetation structure and floristic diversity on detritivore, herbivore and predatory invertebrates within calcareous grasslands. Biodivers Conserv 19:81–95

    Article  Google Scholar 

  • Woodcock BA, Pywell RF, Roy DB, Rose RJ, Bell D (2005) Grazing management of calcareous grasslands and its implications for the conservation of beetle communities. Biol Conserv 125:193–202

    Article  Google Scholar 

  • Zschokke S, Dolt C, Rusterholz H-P, Oggier P, Braschler B, Thommen GH, Lüdin E, Erhardt A, Baur B (2000) Short-term responses of plants and invertebrates to experimental small-scale grassland fragmentation. Oecologia 125:559–572

    Article  Google Scholar 

Download references

Acknowledgments

We thank H. Robles for his collaboration and R.B. O’Hara for statistical advice. Landscape measurements were carried out with SIGPAC, http://sigpac.mapa.es/fega/visor and SITCyL, http://www.sitcyl.jcyl.es/smap/index.jsp. We thank the Servicio Territorial de Medio Ambiente de la Junta de Castilla y León who granted access to the grasslands and several forest guards for collaboration. The study was supported by Ministerio de Ciencia y Tecnología (project reference REN2003-05432/GLO). A. Taboada was financed by Junta de Castilla y León, Spain and CIMO, Finland.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Angela Taboada.

Appendix

Appendix

See Table 6.

Table 6 Carabid beetles collected at gap and exterior grasslands in the oak and beech forested landscapes

Rights and permissions

Reprints and permissions

About this article

Cite this article

Taboada, A., Kotze, D.J., Salgado, J.M. et al. The value of semi-natural grasslands for the conservation of carabid beetles in long-term managed forested landscapes. J Insect Conserv 15, 573–590 (2011). https://doi.org/10.1007/s10841-010-9359-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10841-010-9359-2

Keywords

Navigation