Abstract
The awareness of the importance of deadwood in forest ecosystems has increased in recent decades. Today, dead wood is recognized as a key factor affecting diversity of forest communities. Hole-nesting birds and saproxylic organisms represent an active part of the animal community through the recycle of decaying wood into the forest soils. Three relict beech forests of central Italy were surveyed for both saproxylic beetles and hole-nesting birds, using two different types of interception traps for the former group and point count method for the latter. The variables of dead wood quality were recorded from ten plots, particularly the decaying class and typology of all the wood debris with a diameter ≥ 5 cm. In order to correlate richness and abundance of beetles and birds in a symmetric way, we used co-inertia analysis (CoIA). To correlate in a predictive way the dead wood attributes (dead wood typology and class decay) with birds and beetles assemblages we used partial redundancy analysis (RDA). Our results showed a significant relationship between saproxylic beetle and hole-nesting bird communities. Three dead wood variables (the volume of standing dead trees, stumps and large branches on the ground) appeared to be good predictors of saproxylic beetle richness while the volume of standing dead tree and of dead trees on the ground were the same for hole-nesting birds. These results suggest specific recommendations useful for forest management and planning.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- CoIA:
-
Co-Inertia Analysis
- PCA:
-
Principal Components Analysis
- RDA:
-
Redundancy Analysis
- VIF:
-
Variance Inflation Factor
References
Aitken, K.E.H. and K. Martin. 2007. The importance of excavators in hole-nesting communities: availability and use of natural trees holes in old mixed forest of western Canada. J. Ornithol. 148: 425–434.
Alexander, K.N.A. 2008. Tree biology and saproxylic Coleoptera: issues of definitions and conservation language. Rev. Ecol. (Terre Vie). 63:1–5.
Alinvi, O., J. P. Ball, K. Danell, J. Hjaltén and R.B. Pettersson . 2007. Sampling saproxylic beetle assemblages in dead wood logs: comparing window and eclector traps to traditional bark sieving and a refinement. J. Insect Conserv. 11: 99–112.
Angelstam, P., and G. Mikusiński. 1994. Woodpecker assemblages in natural and managed boreal and hemiboreal forest—a review. Ann. Zool. Fenn. 31:157–172.
Bellamy, P.E., S.A. Hinsley and I. Newton. 1996. Factors influencing bird species numbers in small woods in southeast England. J. Appl. Ecol. 33: 249–262.
Berglund, H. and B.G. Jonsson. 2005. Verifying an extinction debt among lichens and fungi in northern Swedish boreal forests. Conserv. Biol. 19: 338–348.
Bibby, C. J., N. D. Burgess, D. A. Hill and S. H. Mustoe. 2000. Bird Census Techniques, 2nd ed. Academic Press, London.
Blanc, A. and J.R. Walters. 2008. Cavity excavation and enlargement as mechanisms for indirect interactions in an avian community. Ecology 89: 506–514.
Blondel, J., C. Ferry and B. Frochot. 1970. La méthode des indices ponctuels d’abondance (I.P.A.) ou des relevés d’avifaune par “stations d’écoute”. Alauda 38: 55–71.
Bobiec, A., J.M. Gutowski, K. Zub, W.F. Laudenslayer, and P. Pawlaczyk. 2005. The Afterlife of a Tree.WWF Poland, War-szawa-Hajnówka.
Borcard, D., F. Gillett and P. Legendre. 2011. Numerical Ecology with R, Use R. Springer New York Dordrecht London Heidelberg.
Bouchard, P., Y. Bousquet, A.E. Davies, M.A. Alonso-Zarazaga, J.F. Lawrence, C.H.C. Lyal, A.F. Newton, C.A.M. Reid, M. Schmitt, S.A. Ślipiński and A.B.T. Smith. 2011. Family-group names in Coleoptera (Insecta). ZooKeys 88: 1–972.
Bouget, C. and P. Duelli. 2004. The effects of windthrow on forest insect communities: a literature review. Biol. Conserv. 118: 281–299.
Bouget, C., H. Brustel, A. Brin and T. Noblecourt. 2008. Sampling Saproxylic beetles with window flight traps: methodological insights. Rev. Ecol. (Terre Vie). 63: 13–24.
Braak, C. J. F. and A. P. Schaffers. 2004. Co-correspondence analysis: a new ordination method to relate two community compositions. Ecology. 85: 834–846.
Brazaitis, G. and P. Angelstam. 2004. Influence of edges between old deciduous forest and clearcuts on the abundance of passerine hole-nesting birds in Lithuania. Ecol. Bull. 51: 209–217.
Brin, A., H. Brustel and H. Jactel. 2009. Species variables or environmental variables as indicators of forest biodiversity: a case study using saproxylic beetles in Maritime pine plantations. Ann. For. Sci. 66:1–11.
Brunet, J. and G. Isacsson. 2010. A comparison of the saproxylic beetle fauna between lowland and upland beech forests in southern Sweden. Ecol. Bull. 53:131–139.
Brustel, H. 2004. ‘PolytrapTM’ a window flight trap for saproxylic beetles. Proceedings of the 3rd Symposium and Workshop on the Conservation of Saproxylic Beetles. (Riga / Latvia, 7th-11th July, 2004). Latvijas entomologs, (Suppl VI), pp. 128–129.
Carpaneto, G.M., A. Mazziotta, G. Coletti, L. Luiselli and P. Audisio. 2010. Conflict between insect conservation and public safety: the case study of a saproxylic beetle (Osmoderma eremita) in urban parks. J. Insect Conserv. 14: 555–565.
Chiari, S., G.M. Carpaneto, A. Zauli, L. Marini, P. Audisio and T. Ranius. 2012. Habitat of an endangered saproxylic beetle, Osmoderma eremita, in Mediterranean woodlands. Ecoscience. 19: 299–307.
Christensen, M., K. Hahn, E. P. Mountford, P. Ódor, T. Standova, D. Rozenbergar, J. Diaci, S. Wijdeven, P. Meyer, S. Winter and T. Vrska. 2005. Dead wood in European beech (Fagus sylvatica) forest reserves. For. Ecol. Manage. 210: 267–282.
Cramp, S. 1985. Handbook of the Birds of Europe, the Middle East, and North Africa: The Birds of the Western Palearctic, Volume 4. Oxford University Press, Oxford.
Daily, G.C., P.R. Ehrlich and N.M. Haddad. 1993. Double keystone bird in a keystone species complex. PNAS USA. 90: 592–594.
del Hoyo, J., A. Elliott and J. Sargatal. 2013. Handbook of the Birds of the World. Special Volume: New Species and Global Index. Lynx Editions, Barcelona.
Djupström, L.B., J. Weslien and L.M. Schroeder. 2008. Deadwood and saproxylic beetles in set-aside and non set-aside forests in a boreal region. For. Ecol. Manage. 255: 3340–3350.
Drapeau, P., A. Nappi, L. Imbeau and M. Saint-Germain. 2009. Standing deadwood for keystone bird species in the eastern boreal forest: Managing for snag dynamics. The Forestry Chronicle. 85 (2):227–234.
Ewers, R.M. and R.K. Didham. 2006. Confounding factors in detection of species responses to habitat fragmentation. Biol. Reviews 81: 117–142.
Fauna Europaea. 2012. Fauna Europaea version 2.5. Web Service available online at https://doi.org/www.faunaeur.org.
Frelich, L. E. and P. B. Reich. 2003. Perspectives on development of definitions and values related to old-growth forests. Environ. Rev. 11: 9–22.
Fuller, R.J., K.W. Smith and S.A. Hinsley. 2012 Temperate western European woodland as a dynamic habitat for birds: a resource-based view. In: R.J. Fuller (ed.), Birds and Habitat: Relationships in Changing Landscapes. Cambridge University Press, Cambridge, UK. pp. 352–380.
Gaston, K.J. 1994. Rarity. Chapman and Hall, London.
Gibbons, D.W. and R.D. Gregory. 2006. Birds. In: W.J. Sutherland (ed.). Ecological Census Techniques, 2nd ed. Cambridge University Press, Cambridge. pp. 308–350.
Gossner, M. M., S. Getzin, M. Lange, E. Pašalic´, M. Türke, K. Wiegand and W. W. Weisser. 2013. The importance of heterogeneity revisited from a multiscale and multitaxa approach. Biol. Conserv. 166: 212–220.
Graham, M.H. 2003. Confronting multicollinearity in ecological multiple regression. Ecology. 84: 2809–2815.
Grove, S.J. 2002. Saproxylic insect ecology and the sustainable management of Forests. Annu. Rev. Ecol. Syst. 33:1–23.
Henle, K., K.F. Davies, M. Kleyer, C. Margules and J. Settele. 2004. Predictors of species sensitivity to fragmentation. Biodiv. Conserv. 13: 207–251.
Hunter, M.L. 1990. Maintaining Biodiversity in Forest Ecosystems. Cambridge University Press, Cambridge, United Kingdom.
Jacobs, J.M., J.R. Spence and D.W. Langor. 2007. Influence of forest boreal succession and dead wood quality on saproxylic beetles. Agr. Forest. Entomol. 9:3–16.
Johansson, T., J. Hjalten, J. Hilszczanski, J. Stenlid, J.P. Ball, O. Alinvi and K. Danell. 2007. Variable response of different functional groups of saproxylic beetles to substrate manipulation and forest management: implications for conservation strategies. For. Ecol. Manage. 242: 496–510.
Johnsson, K., S.G. Nilsson and M. Tjernberg. 1990. The black woodpecker: a key species in European forest. In: A. Carlsson and G. Aulén (eds.), Conservation and Management of Woodpecker Population. Report 17. Swedish University of Agriculture Science, Department of Wildlife Ecology. pp. 99–102.
Jonsell, M., J. Hansson and L. Wedmo. 2007. Diversity of saproxylic beetles species in logging residues in Sweden: comparison between tree species and diameters. Biol. Conserv. 138: 89–99.
Jonsell, M., J. Weslien and B. Ehnstrӧm. 1998. Substrate requirements of red-listed saproxylic invertebrates in Sweden. Biodivers. Conserv. 7:749–764.
Jonsson, B. G., N. Kruys and T. Ranius. 2005. Ecology of species living on dead wood-Lessons for dead wood management. Silva Fenn. 39: 289–309.
Lachat, T., C. Bouget, R. Bütler and J. Müller. 2013. Deadwood: quantitative and qualitative requirements for the conservation of saproxylic biodiversity. In: D. Kraus and F. Krumm (eds.) 2013. Integrative Approaches as an Opportunity for the Conservation of Forest Biodiversity. European Forest Institute. 284 pp.
Laussace, A., Y. Paillet, H. Jactel and C. Bouget. 2011. Deadwood as a surrogate for forest biodiversity: meta-analysis of correlation between deadwood volume and species richness of saproxylic organisms. Ecol. Indic. 11: 1027–1039.
Legendre, P. and E. Gallagher. 2001. Ecologically meaningful transformations for ordination of species data. Oecologia 129: 271–280.
Lindhe, A. and Å. Lindelöw. 2004. Cut high stumps of spruce, birch, aspen and oak as breeding substrates for saproxylic beetles. For. Ecol. Manage. 203: 1–20.
Martin, K. and J.M. Eadie. 1999. Nest webs: A community-wide approach to the management and conservation of cavity-nesting forest birds. For. Ecol. Manage. 115: 243–257.
Martin, K., K.E.H. Aitken and K. L. Wiebe. 2004. Nest site and nest webs for cavity - nesting community in interior British Columbia, Canada: nest characteristics and niche partitioning. Condor. 106: 5–19.
Martin, T.E. and P. Li. 1992. Life history traits of open- vs. cavity-nesting birds. Ecology 73: 579–592.
Matthysen, E., L. Lens, S.Van Dongen, G.R. Verheyen, L.A.Wauters, F. Adriaensen and A.A. Dhondt. 1995. Diverse effects of forest fragmentation on a number of animal species. Belg. J. Zool. 125: 175–183.
McGeoch, M.A., M. Schroeder, B. Ekbom and S. Larsson. 2007. Saproxylic beetle diversity in a managed boreal forest: importance of stand characteristics and forestry conservation measures. Divers. Distrib. 13: 418–429.
MCPFE. 2003. Improved pan-European indicators for sustainable forest management as adopted by the MCPFE Expert Level Meeting. In: Ministerial Conference on the Protection of Forests in Europe, Vienna, pp. 6.
Mikusiňski, G., M. Gromadzki and P. Chylarecki. 2001. Woodpeckers as indicators of forest bird diversity. Biol.Conserv. 15: 208–217.
Müller, J. and R. Bütler. 2010. A review of habitat thresholds for dead wood: a baseline for management recommendations in European forests. Eur. J. For. Res. 129: 981–992.
Müller, J., J. Brunet, A. Brin, C. Bouget, H. Brustel, H. Bussler, B. Fӧrster, G. Isacsson, F. Kӧhler, T. Lachat, and M.M. Gossner. 2012. Implications from large-scale spatial diversity patterns of saproxylic beetles for the conservation of European beech forests. Insect Conserv. Diver. 6(2): 162–169.
Murphy, E.C. and W.A. Lehnhausen. 1998. Density and foraging ecology of woodpeckers following a stand-replacement fire. J. Wildl. Manag. 62: 1359–1372.
Nappi A., P. Drapeau, J.-F. Giroux and J.-P.L. Savard. 2003. Snag use by foraging Black-backed Woodpeckers in a recently burned eastern boreal forest. Auk. 120: 505–511.
Nappi, A. 2009. Sélection d’habitat et démographie du Pic à dos noir (Picoides arcticus) dans les forêts brûlées de la forêt boréale. Ph.D. thesis, Université du Québec à Montréal. Montréal. 189 pp.
Newton, I. 1998. Population Limitation in Birds. Academic Press, San Diego, California, USA.
Nilsson, S.G. 1984. The evolution of nest-site selection among hole-nesting birds: the importance of nest predation and competition. Orn. Scand. 15: 167–175.
Økland, B., A. Bakke, S. Hagvar and T. Kvamme. 1996. What factors influence the diversity of saproxylic beetles? A multiscale study from a spruce forest in southern Norway. Biodivers. Conserv. 5: 75–100.
Olsson, O., U. Wiktander, A. Malmqvist, S. G. Nilsson. 2001. Variability of patch type preferences in relation to resource availability and breeding success in a bird. Oecologia. 127: 435–443.
Paclík, M. and K. Weidinger. 2007. Microclimate of trees cavities during winter nights: implication for roost site selection in birds. Int. J. Biometeorol. 51: 287–293.
Paillet, Y., L. Berges, J. Hjälten, P. Ódor, C. Avon, M. Bernhardt-Römermann, R.J. Bijlsma, L. De Bruyn, M. Fuhr, U. Graindin, R. Kanka, L. Lundin, S. Luque, T. Magura, S. Matesanz, I. Meszaros, M.T. Sebastia, W. Schmidt, T. Standovar, B. Tothmeresz, A. Uotila, F. Valladares, K. Vellak and R. Virtanen. 2010. Biodiversity differences between managed and unmanaged forests: meta- analysis of species richness in Europe. Conserv. Biol. 24: 101–112.
Pakkala, T., I. Hanski, and E. Tomppo. 2002. Spatial ecology of the three-toed woodpecker in managed forest landscapes. Silva Fenn. 36: 279–288.
Pasinelli, G. 2007. Nest site selection in middle and great spotted woodpeckers Dendrocopos medius & D. major: implications for forest management and conservation. Biodiv. Conserv. 16:1283–1298.
Peterken, G.F. 1996. Natural Woodland. Ecology and Conservation in Northern Temperate Regions. Cambridge University Press, Cambridge.
Piovesan, G., A. Alessandrini, M. Baliva, T. Chiti, E. D’andrea, B. De Cinti, A. Di Filippo, L. Hermanin, M. Lauteri, G. Scarascia Mugnozza, B. Schirone, E. Ziaco and G. Matteucci. 2010. Structural patterns, growth processes, carbon stocks in an Italian network of old-growth beech forests. Italia Forestale e Montana (Italian Journal of Forest and Mountain Environments) 65: 557–590.
Ranius, T. 2002. Influence of stand size and quality of tree hollows on saproxylic beetles in Sweden. Biol.Conserv. 103: 85–91.
Ranius, T. and N. Jansson. 2000. The influence of forest regrowth, original canopy cover and tree size on saproxylic beetles associated with old oaks. Biol.Conserv. 95: 85–94.
Ranius, T., P. Eliasson and P. Johansson. 2008. Large-scale occurrence patterns of red-listed lichens and fungi on old oaks are influenced both by current and historical habitat density. Biodivers. Conserv. 17: 2371–2381.
Rao, C.R. 1995. A review of canonical coordinates and an alternative to correspondence analysis using Hellinger distance. Qüestiió (Cuadernos de Estadística e Investigación Operativa) 19: 23–63.
R-Development Core Team. 2010. R: a language and environment for statistical computing. R Foundation for Statistical Computing.
Remm, J., A. Lohmus and K. Remm. 2006. Tree cavities in riverine forests: what determines their occurrence and use by hole-nesting passerines? For. Ecol. Manage. 221: 267–277.
Rondeux, J. and C. Sanchez. 2010. Review of indicators and field methods for monitoring biodiversity within national forest inventories. Core variable: deadwood. Environ. Monit. Assess. 164: 617–630.
Rose, F. 1992. Temperate forest management, its effect on bryophyte and lichen floras and habitats. In: J.W. Bates and A.M. Farmer (eds.), Bryophytes and Lichens in a Changing Environment. Clarenden Press, Oxford, pp. 223–245.
Schiegg, K. 2000. Effects of deadwood volume and connectivity on saproxylic insect species diversity. Ecoscience 7: 290–298.
Schiegg, K. 2001. Saproxylic insect diversity of beech: limbs are richer than trunk. For. Ecol. Manage. 149: 295–304.
Schuck, A., P. Meyer, N. Menke, M. Lier and M. Lindner. 2004. Forest biodiversity indicator: dead wood - A proposed approach towards operationalising the MCPFE indicator. In: M. Marchetti (ed.), Monitoring and indicators of forest biodiversity in Europe - from ideas to operationality. EFI Proceedings, pp. 49–77.
Siitonen, J. 2001. Forest management, coarse woody debris and saproxylic organisms: Fennoscandian boreal forests as an example. Ecol. Bull. 49:11–41.
Siitonen, J. and B.G. Jonsson. 2012. Other associations with dead wood material. In: J.N. Stokland, J. Siitonen and B.G. Jonsson. (eds.), Biodiversity in dead wood. Cambridge University Press, New York, pp. 58–76.
Siitonen, J., P. Martikainen, P. Punttila and J. Rauh. 2000. Coarse woody debris and stand characteristics in mature managed and old-growth boreal mesic forests in southern Finland. For. Ecol. Manage. 128: 211–225.
Similä, M., J. Kouki and P. Martikainen. 2003. Saproxylic beetles in managed and seminatural Scots pine forests: quality of dead wood matters. For. Ecol. Manage. 174: 365–381.
Speight, M.C.D. 1989. Saproxylic invertebrates and their conservation. Council of Europe, Publications and Documents Division, Strasbourg, France.
Spies, T.A. 2004. Ecological concepts and diversity of old-growth forests. J. Forest. 102: 14–20.
Stokland , J.N., S.M. Tomter, and U. Söderber. 2004. Development of Dead Wood Indicators for Biodiversity Monitoring: Experiences from Scandinavia. In: M. Marchetti (ed.), Monitoring and Indicators of forest biodiversity in Europe - from ideas to operationality, EFI Proceedings. pp.207–226.
Stokland, J. N., J. Siitonen and B.G. Jonsson. 2012. Biodiversity in dead wood. Cambridge University Press, New York.
Stokland, J.N. 2012. The saproxylic food web. In: J.N. Stokland, J. Siitonen and B.G. Jonsson. (eds.), Biodiversity in dead wood. Cambridge University Press, New York, pp. 29–54.
Sutherland, W. 2006. Ecological Census Techniques, 2nd edn. Cambridge University Press, Cambridge.
Thompson, W.L., G.C. White and C. Gowan. 1998. Monitoring vertebrate populations. Academic Press, San Diego, USA.
Tutin, T. G., N. A. Burges, A. O. Chater, J. R. Edmondson, V. H. Heywood, D. M. Moore, D. H. Valentine, S. M. Walters and D. A. Webb. 1964–1993. Flora Europaea. Vols. 1–5 and Vol.1, ed.2., Cambridge University Press.
Virkkala, R. 2006. Why study woodpeckers? The significance of woodpeckers in forest ecosystems. Ann. Zool. Fennici 43: 82–85.
Wenger, K.F. 1984. Forestry handbook. 2nd ed. John Wiley & Sons, New York.
Wesolowski, T. 2007. Lessons from long-term hole nesters studies in a primeval temperate forest. J. Ornithol. 148(2): 395–405.
Wesolowski, T. and P. Rowiński. 2012. The breeding performance of Blue Tits Cyanistes caeruleus in relation to the attributes of natural holes in a primeval forest. Bird Study 59: 437–448.
Wesolowski, T. and P. Rowiński. 2004. Breeding behaviour of Nuthatch Sitta europaea in relation to natural hole attributes in a primeval forest. Bird Study 51:143–155.
Wiebe, K.L. 2001. Microclimate of tree cavity nests: it is important for reproductive success in northen flickers? Auk 118: 412–421.
Zangari, L., M. Ferraguti, L. Luiselli, C. Battisti and M.A. Bologna. 2013. Comparing patterns in abundance and diversity of hole-nesting birds in Mediterranean habitats. Rev. Écol. (Terre Vie) 67: 1–8.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Rights and permissions
This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
About this article
Cite this article
Redolfi De Zan, L., Battisti, C. & Carpaneto, G.M. Bird and beetle assemblages in relict beech forests of central Italy: a multi-taxa approach to assess the importance of dead wood in biodiversity conservation. COMMUNITY ECOLOGY 15, 235–245 (2014). https://doi.org/10.1556/ComEc.15.2014.2.12
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1556/ComEc.15.2014.2.12