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Robustness of plant–insect herbivore interaction networks to climate change in a fragmented temperate forest landscape

Published online by Cambridge University Press:  10 February 2017

K.W. Bähner ,
K.A. Zweig ,
I.R. Leal  and
R. Wirth
K.W. Bähner
Affiliation:
Plant Ecology and Systematics, University of Kaiserslautern, P.O. Box 3049, 67663 Kaiserslautern, Germany
K.A. Zweig
Affiliation:
Graph Theory & Complex Network Analysis, University of Kaiserslautern, P.O. Box 3049, 67663 Kaiserslautern, Germany
I.R. Leal
Affiliation:
Departamento de Botânica, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego, s/n, 50670-901, Cidade Universitária, Recife, PE, Brazil
R. Wirth*
Affiliation:
Plant Ecology and Systematics, University of Kaiserslautern, P.O. Box 3049, 67663 Kaiserslautern, Germany
*
*Author for correspondence Phone: +49 631 205 4401 Fax: +49 631 205 2998 E-mail: [email protected]
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Abstract

Forest fragmentation and climate change are among the most severe and pervasive forms of human impact. Yet, their combined effects on plant–insect herbivore interaction networks, essential components of forest ecosystems with respect to biodiversity and functioning, are still poorly investigated, particularly in temperate forests. We addressed this issue by analysing plant-insect herbivore networks (PIHNs) from understories of three managed beech forest habitats: small forest fragments (2.2–145 ha), forest edges and forest interior areas within three continuous control forests (1050–5600 ha) in an old hyper-fragmented forest landscape in SW Germany. We assessed the impact of forest fragmentation, particularly edge effects, on PIHNs and the resulting differences in robustness against climate change by habitat-wise comparison of network topology and biologically realistic extinction cascades of networks following scores of vulnerability to climate change for the food plant species involved. Both the topological network metrics (complexity, nestedness, trophic niche redundancy) and robustness to climate change strongly increased in forest edges and fragments as opposed to the managed forest interior. The nature of the changes indicates that human impacts modify network structure mainly via host plant availability to insect herbivores. Improved robustness of PIHNs in forest edges/small fragments to climate-driven extinction cascades was attributable to an overall higher thermotolerance across plant communities, along with positive effects of network structure. The impoverishment of PIHNs in managed forest interiors and the suggested loss of insect diversity from climate-induced co-extinction highlight the need for further research efforts focusing on adequate silvicultural and conservation approaches.

Keywords

ecosystem stabilityedge effectsextinction cascadesfood web resilienceglobal changephytophagous insects
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 107 , Issue 5 , October 2017 , pp. 563 - 572
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Copyright
Copyright © Cambridge University Press 2017 

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References

Albrecht, J., Berens, D.G., Blüthgen, N., Jaroszewicz, B., Selva, N. & Farwig, N. (2013) Logging and forest edges reduce redundancy in plant–frugivore networks in an old-growth European forest. Journal of Ecology 101, 990–999.CrossRefGoogle Scholar
Bale, J.S., Masters, G.J., Hodkinson, I.D., Awmack, C., Bezemer, T.M., Brown, V.K., Butterfield, J., Buse, A., Coulson, J.C., Farrar, J., Good, J.E.G., Harrington, R., Hartley, S., Jones, T.H., Lindroth, R.L., Press, M.C., Symrnioudis, I., Watt, A.D. & Whittaker, J.B. (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biology 8, 1–16.CrossRefGoogle Scholar
Bascompte, J., Jordano, P., Melián, C.J. & Olesen, J.M. (2003) The nested assembly of plant-animal mutualistic networks. Proceedings of the National Academy of Sciences of the United States of America 100, 9383–9387.CrossRefGoogle ScholarPubMed
Blüthgen, N. (2010) Why network analysis is often disconnected from community ecology: a critique and an ecologist's guide. Basic and Applied Ecology 11, 185–195.CrossRefGoogle Scholar
Blüthgen, N., Menzel, F. & Blüthgen, N. (2006) Measuring specialization in species interaction networks. BMC Ecology 6, 1–12.CrossRefGoogle ScholarPubMed
Blüthgen, N., Fründ, J., Vázquez, D.P. & Menzel, F. (2008) What do interaction network metrics tell us about specialization and biological traits? Ecology 89, 3387–3399.CrossRefGoogle ScholarPubMed
Brunet, J., Fritz, Ö. & Richnau, G. (2010) Biodiversity in European beech forests–a review with recommendations for sustainable forest management. Ecological Bulletins 53, 77–94.Google Scholar
Burgos, E., Ceva, H., Perazzo, R.P.J., Devoto, M., Medan, D., Zimmermann, M. & Delbue, A.M. (2007) Why nestedness in mutualistic networks? Journal of Theoretical Biology 249, 307–313.CrossRefGoogle ScholarPubMed
Coch, T. (1995) Waldrandpflege: Grundlagen und Konzepte. Praktischer Naturschutz. Radebeul, Neumann Verlag.Google Scholar
Deutscher Wetterdienst (2013) Mean annual climate data. Available online at http://www.dwd.de Google Scholar
Dormann, C.F., Gruber, B. & Fründ, J. (2008) Introducing the bipartite package: analysing ecological networks. R News 8, 8–11.Google Scholar
Dormann, C.F., Fründ, J., Blüthgen, N. & Gruber, B. (2009) Indices, graphs and null models: analyzing bipartite ecological networks. The Open Ecology Journal 2, 7–24.CrossRefGoogle Scholar
Ellenberg, H., Leuschner, C. (1996) Vegetation Mitteleuropas mit den Alpen. Berlin, UTB.Google Scholar
Emmerson, M., Bezemer, M., Hunter, M.D. & Jones, T.H. (2005) Global change alters the stability of food webs. Global Change Biology 11, 490–501.CrossRefGoogle Scholar
Fahrig, L. (2003) Effects of habitat fragmentation on biodiversity. Review of Ecology, Evolution, and Systematics 34, 487–515.CrossRefGoogle Scholar
Fortuna, M.A. & Bascompte, J. (2006) Habitat loss and the structure of plant-animal mutualistic networks. Ecology Letters 9, 281–286.CrossRefGoogle ScholarPubMed
Frey, W. & Lösch, R. (2010) Geobotanik: Pflanze und Vegetation in Raum und Zeit. Heidelberg, Spektrum Akademischer Verlag.Google Scholar
Gehlhausen, S., Schwartz, M. & Augspurger, C. (2000) Vegetation and microclimatic edge effects in two mixed-mesophytic forest fragments. Plant Ecology 147, 21–35.CrossRefGoogle Scholar
Haddad, N.M., Crutsinger, G.M., Gross, K., Haarstad, J. & Tilman, D. (2011) Plant diversity and the stability of foodwebs. Ecology Letters 14, 42–46.CrossRefGoogle ScholarPubMed
Heleno, R., Devoto, M. & Pocock, M. (2012) Connectance of species interaction networks and conservation value: is it any good to be well connected? Ecological Indicators 14, 7–10.CrossRefGoogle Scholar
Hermy, M., Honnay, O., Firbank, L., Grashof-Bokdam, C. & Lawesson, J.E. (1999) An ecological comparison between ancient and other forest plant species of Europe, and the implications for forest conservation. Biological Conservation 91, 9–22.CrossRefGoogle Scholar
Honnay, O., Verheyen, K. & Hermy, M. (2002) Permeability of ancient forest edges for weedy plant species invasion. Forest Ecology and Management 161, 109–122.CrossRefGoogle Scholar
Kaiser-Bunbury, C.N., Muff, S., Memmott, J., Müller, C.B. & Caflisch, A. (2010) The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. Ecology Letters 13, 442–452.CrossRefGoogle Scholar
Kaneryd, L., Borrvall, C., Berg, S., Curtsdotter, A., Eklöf, A., Hauzy, C., Jonsson, T., Münger, P., Setzer, M., Säterberg, T. & Ebenman, B. (2012) Species-rich ecosystems are vulnerable to cascading extinctions in an increasingly variable world. Ecology and Evolution 2, 858–874.CrossRefGoogle Scholar
Klanderud, K. (2005) Climate change effects on species interactions in an alpine plant community. Journal of Ecology 93, 127–137.CrossRefGoogle Scholar
Kramer, K., Degen, B., Buschbom, J., Hickler, T., Thuiller, W., Sykes, M.T. & de Winter, W. (2010) Modelling exploration of the future of European beech (Fagus sylvatica L.) under climate change—range, abundance, genetic diversity and adaptive response. Forest Ecology and Management 259, 2213–2222.CrossRefGoogle Scholar
Laliberté, E. & Tylianakis, J.M. (2010) Deforestation homogenizes tropical parasitoid–host networks. Ecology 91, 1740–1747.CrossRefGoogle ScholarPubMed
Laliberté, E., Wells, J.A., DeClerck, F., Metcalfe, D.J., Catterall, C.P., Queiroz, C., Aubin, I., Bonser, S.P., Ding, Y., Fraterrigo, J.M., McNamara, S., Morgan, J.W., Merlos, D.S., Vesk, P.A. & Mayfield, M.M. (2010) Land-use intensification reduces functional redundancy and response diversity in plant communities. Ecology Letters 13, 76–86.CrossRefGoogle ScholarPubMed
Lindner, M., Maroschek, M., Netherer, S., Kremer, A., Barbati, A., Garcia-Gonzalo, J., Seidl, R., Delzon, S., Corona, P., Kolström, M., Lexer, M.J. & Marchetti, M. (2010) Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. Forest Ecology and Management 259, 698–709.CrossRefGoogle Scholar
Melian, C.J. & Bascompte, J. (2002) Food web structure and habitat loss. Ecology Letters 5, 37–46.CrossRefGoogle Scholar
Memmott, J., Waser, N.M. & Price, M.V. (2004) Tolerance of pollination networks to species extinctions. Proceedings of the Royal Society B: Biological Sciences 271, 2605–2611.CrossRefGoogle ScholarPubMed
Menke, S., Böhning-Gaese, K. & Schleuning, M. (2012) Plant-frugivore networks are less specialized and more robust at forest-farmland edges than in the interior of a tropical forest. Oikos 121, 1553–1566.CrossRefGoogle Scholar
Morris, R.J. (2010) Anthropogenic impacts on tropical forest biodiversity: a network structure and ecosystem functioning perspective. Philosophical Transactions of the Royal Society B: Biological Sciences 365, 3709–3718.CrossRefGoogle ScholarPubMed
MUF (2002) Bundeswaldinventur 2. Germany, Ministry of Environment and Forestry.Google Scholar
Nakagawa, S. & Schielzeth, H. (2013) A general and simple method for optaining R2 from generalized linear mixed-effect models. Methods in Ecology and Evolution 4, 133–142.CrossRefGoogle Scholar
Netherer, S. & Schopf, A. (2010) Potential effects of climate change on insect herbivores in European forests – General aspects and the pine processionary moth as specific example. Forest Ecology and Management 259, 831–838.CrossRefGoogle Scholar
Olesen, J.M., Bascompte, J., Dupont, Y.L. & Jordano, P. (2007) The modularity of pollination networks. Proceedings of the National Academy of Sciences of the United States of America 10, 19891–19896.CrossRefGoogle Scholar
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & the R Core Team (2017) nlme: linear and nonlinear mixed effects models. R package version 3.1–122, https://CRAN.R-project.org/package=nlme.Google Scholar
Pompe, S., Hanspach, J., Badeck, F.W., Klotz, S., Bruelheide, H. & Kühn, I. (2010) Investigating habitat-specific plant species pools under climate change. Basic and Applied Ecology 11, 603–611.CrossRefGoogle Scholar
Pompe, S., Berger, S., Bergmann, J., Badeck, F., Lübbert, J., Klotz, S., Rehse, A., Söhlke, G., Sattler, S., Walther, G.-R. & Kühn, I. (2011) Modellierung der Auswirkungen des Klimawandels auf die Flora und Vegetation in Deutschland. Bonn, BfN.Google Scholar
Price, P.W. (2002) Resource-driven terrestrial interaction webs. Ecological Research 17, 241–247.CrossRefGoogle Scholar
R Core Team (2013) R: a language and environment for statistical computing. R package version 3.0.2.Google Scholar
Reid, H. (2006) Climate change and biodiversity in Europe. Conservation and Society 4, 84–101.Google Scholar
Rzanny, M. & Voigt, W. (2012) Complexity of multitrophic interactions in a grassland ecosystem depends on plant species diversity. Journal of Animal Ecology 81, 614–627.CrossRefGoogle Scholar
Santos, B.A., Peres, C.A., Oliveira, M.A., Grillo, A.S., Alves-Costa, C.P. & Tabarelli, M. (2008) Drastic erosion in functional attributes of tree assemblages in Atlantic forest fragments of northeastern Brazil. Biological Conservation 141, 249–260.CrossRefGoogle Scholar
Schweiger, O., Settele, J., Kudrna, O., Klotz, S. & Kühn, I. (2008) Climate change can cause spatial mismatch of trophically interacting species. Ecology 89, 3472–3479.CrossRefGoogle ScholarPubMed
Segura, A., Castaño-Santamaría, A., Laiolo, P. & Obeso, J.R. (2014) Divergent responses of flagship, keystone and resource-limited bio-indicators to forest structure. Ecological Research 29, 925–936.CrossRefGoogle Scholar
Sprick, P. & Floren, A. (2008) Species richness and historical relations in arboreal phytophagous beetles a study based on fogging samples from primeval forests of Poland, Romania and Slovenia (Coleoptera: Chrysomelidae, Curculionoidea). pp. 225–259 in Floren, A. & Schmidl, J. (Eds) Canopy Arthropod Research in Europe. Basic and Applied Studies from the High Frontier. Nürnberg, Bioform Entomology.Google Scholar
Thomas, C.D., Cameron, A., Green, R.E., Bakkenes, M., Beaumont, L.J., Collingham, Y.C., Erasmus, B.F.N., de Siqueira, M.F., Grainger, A., Hannah, L., Hughes, L., Huntley, B., van Jaarsveld, A.S., Midgley, G.F., Miles, L., Ortega-Huerta, M.A., Townsend Peterson, A., Phillips, O.L. & Williams, S.E. (2004) Extinction risk from climate change. Nature 427, 145–148.CrossRefGoogle ScholarPubMed
Traill, L.W., Lim, M.L.M., Sodhi, N.S. & Bradshaw, C.J.A. (2010) Mechanisms driving change: altered species interactions and ecosystem function through global warming. Journal of Animal Ecology 79, 937–947.CrossRefGoogle ScholarPubMed
Tylianakis, J.M., Tscharntke, T. & Lewis, O.T. (2007) Habitat modification alters the structure of tropical host–parasitoid food webs. Nature 445, 202–205.CrossRefGoogle ScholarPubMed
Tylianakis, J.M., Didham, R.K., Bascompte, J. & Wardle, D.A. (2008) Global change and species interactions in terrestrial ecosystems. Ecology Letters 11, 1351–1363.CrossRefGoogle ScholarPubMed
Valladares, G., Cagnolo, L. & Salvo, A. (2012) Forest fragmentation leads to food web contraction. Oikos 121, 299–305.CrossRefGoogle Scholar
van Halder, I., Barbaro, L. & Jactel, H. (2011) Conserving butterflies in fragmented plantation forests: are edge and interior habitats equally important? Journal of Insect Conservation 15, 591–601.CrossRefGoogle Scholar
Weiner, C.N., Werner, M., Linsenmair, K.E. & Blüthgen, N. (2011) Land use intensity in grasslands: changes in biodiversity, species composition and specialisation in flower visitor networks. Basic and Applied Ecology 12, 292–299.CrossRefGoogle Scholar
Wirth, R., Meyer, S.T., Leal, I.R. & Tabarelli, M. (2008) Plant herbivore interactions at the forest edge. pp. 423–448 in Lüttge, U., Beyschlag, W. & Murata, J. (Eds) Progress in Botany. Berlin, Heidelberg, Springer.CrossRefGoogle Scholar
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