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Fragmentation in calcareous grasslands: species specialization matters

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Abstract

Habitat fragmentation resulting from anthropogenic land-use change may negatively affect both biodiversity and ecosystem structure and function. However, susceptibility to fragmentation varies between species and may be influenced by for instance specialization, functional traits and trophic level. We examined how total and specialist species richness, species composition and functional trait composition at two trophic levels (vascular plants and sap-feeding hoppers) vary with habitat fragmentation (patch size and connectivity) in dry calcareous grasslands in southeast Norway. We found that fragmentation affected plant and hopper species composition both totally and of habitat specialists, but with a net species loss only for the specialists, indicating greater susceptibility of specialized species. Reductions in patch size and increasing isolation negatively affected plant specialists with different sets of traits, effectively reducing the number of species with trait combinations suitable to persist in small and isolated patches. Fragmentation influenced trait composition of the total hopper community, but not of habitat specialists. A lesser degree of habitat association could explain why hoppers, despite belonging to a higher tropic level, seemed to be less susceptible to fragmentation than plants. Nonetheless, our study shows that habitat fragmentation affects both species richness, species composition and trait composition of plants and hoppers, indicating that fragmentation leads not only to a loss of species, but also alters dominance hierarchies and the functionality of grassland communities.

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References

  • Adriaens D, Honnay O, Hermy M (2006) No evidence of a plant extinction debt in highly fragmented calcareous grasslands in Belgium. Biol Conserv 133:212–224

    Article  Google Scholar 

  • Barbaro L, van Halder I (2009) Linking bird, carabid beetle and butterfly life-history traits to habitat fragmentation in mosaic landscapes. Ecography 32:321–333. https://doi.org/10.1111/j.1600-0587.2008.05546.x

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01

    Article  Google Scholar 

  • Biedermann R (2002) Leafhoppers (Hemiptera, Auchenorrhyncha) in fragmented habitats. Denisia 4:523–530

    Google Scholar 

  • Biedermann R, Niedringhaus R (2004) Die Zikaden Deutschlands—Bestimmungstafeln fur alle Arten. WABV Frund, Scheessel

    Google Scholar 

  • Brückmann SV, Krauss J, Steffan-Dewenter I (2010) Butterfly and plant specialists suffer from reduced connectivity in fragmented landscapes. J Appl Ecol 47:799–809. https://doi.org/10.1111/j.1365-2664.2010.01828.x

    Article  Google Scholar 

  • Brückmann SV, Krauss J, van Achterberg C, Steffan-Dewenter I (2011) The impact of habitat fragmentation on trophic interactions of the monophagous butterfly Polyommatus coridon. J Insect Conserv 15:707–714. https://doi.org/10.1007/s10841-010-9370-7

    Article  Google Scholar 

  • Bruun HH (2000) Patterns of species richness in dry grassland patches in an agricultural landscape. Ecography 23:641–650. https://doi.org/10.1034/j.1600-0587.2000.230601.x

    Article  Google Scholar 

  • Cagnolo L, Valladares G, Salvo A, Cabido M, Zak M (2009) Habitat fragmentation and species loss across three interacting trophic levels: effects of life-history and food-web traits. Conserv Biol 23:1167–1175

    Article  PubMed  Google Scholar 

  • County Administrator of Oslo and Akershus (2010) Action plan towards invasive species in Oslo and Akershus. Report 2/2010

  • della Giustina W (2002) Migration in Auchenorrhyncha. Denisia 4:513–522

    Google Scholar 

  • Denno RF, Roderick GK (1991) Influence of patch size, vegetation texture, and host plant architecture on the diversity, abundance, and life-history styles of sap-feeding herbivores. In: Bell SS, McCoy ED, Mushinsky HR (eds) Habitat structure: the physical arrangement of objects in space. Chapman and Hall, London, pp 169–196

    Chapter  Google Scholar 

  • Devictor V, Julliard R, Jiguet F (2008) Distribution of specialist and generalist species along spatial gradients of habitat disturbance and fragmentation. Oikos 117:507–514

    Article  Google Scholar 

  • Dupré C, Ehrlén J (2002) Habitat configuration, species traits and plant distributions. J Ecol 90:796–805

    Article  Google Scholar 

  • Endrestøl A (2014) The genus Recilia Edwards, 1922 (Hemiptera, Cicadellidae) confirmed from Northern Europe. Norw J Entomol 61:37–41

    Google Scholar 

  • Eriksson O (1996) Regional dynamics of plants: a review of evidence for remnant, source-sink and metapopulations. Oikos 77:248–258

    Article  Google Scholar 

  • Evju M, Stange E (eds) (2016) Når artenes leveområder splittes opp - eksempler fra øyene i indre Oslofjord. Sluttrapport fra strategisk instituttsatsing (SIS) 2011-2015. NINA Temahefte 65

  • Evju M, Sverdrup-Thygeson A (2016) Spatial configuration matters: a test of the habitat amount hypothesis for plants in calcareous grasslands. Landsc Ecol 31:1891–1902. https://doi.org/10.1007/s10980-016-0405-7

    Article  Google Scholar 

  • Evju M, Blumentrath S, Skarpaas O, Stabbetorp OE, Sverdrup-Thygeson A (2015) Plant species occurrence in a fragmented landscape: the importance of species traits. Biodiv Conserv 24:547–561. https://doi.org/10.1007/s10531-014-0835-y

    Article  Google Scholar 

  • Ewers RM, Didham RK (2006) Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev 81:117–143

    Article  PubMed  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Ann Rev Ecol Evol Syst 34:487–515. https://doi.org/10.1146/annurev.ecolsys.34.011802.132419

    Article  Google Scholar 

  • Fitter AH, Peat HJ (1994) The ecological flora database. J Ecol 82:415–425

    Article  Google Scholar 

  • Gederaas L, Moen TL, Skjelseth S, Larsen L-K (eds) (2012) Non-native species in Norway—with the Norwegian Black List 2012. The Norwegian Biodiversity Information Centre, Trondheim

    Google Scholar 

  • Giladi I, May F, Ristow M, Jeltsch F, Ziv Y (2014) Scale-dependent species-area and species-isolation relationships: a review and a test study from a fragmented semi-arid agro-ecosystem. J Biogeogr 41:1055–1069. https://doi.org/10.1111/jbi.12299

    Article  Google Scholar 

  • Habel JC, Dengler J, Janišová M, Török P, Wellstein C, Wiezik M (2013) European grassland ecosystems: threatened hotspots of biodiversity. Biodiv Conserv 22:2131–2138

    Article  Google Scholar 

  • Haddad NM et al (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1:e1500052. https://doi.org/10.1126/sciadv.1500052

    Article  PubMed  PubMed Central  Google Scholar 

  • Hanski I (1994) A practical model of metapopulation dynamics. J Anim Ecol 63:151–162. https://doi.org/10.2307/5591

    Article  Google Scholar 

  • Henderson RA (2010) Influence of patch size, isolation, and fire history on hopper (Homoptera: Auchenorrhyncha) communities of eight Wisconsin prairie remnants. Wisconsin Department of Natural Resources Research Report 189

  • Henle K, Davies KF, Kleyer M, Margules C, Settele J (2004) Predictors of species sensitivity to fragmentation. Biodiv Conserv 13:207–251

    Article  Google Scholar 

  • Henriksen S, Hilmo O (eds) (2015) Norwegian Red list for species 2015. The Norwegian Biodiversity Information Centre, Trondheim

    Google Scholar 

  • Higgins SI, Lavorel S, Revilla E (2003) Estimating plant migration rates under habitat loss and fragmentation. Oikos 101:354–366. https://doi.org/10.1034/j.1600-0706.2003.12141.x

    Article  Google Scholar 

  • Hooper DU et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35. https://doi.org/10.1890/04-0922

    Article  Google Scholar 

  • Isbell F et al (2011) High plant diversity is needed to maintain ecosystem services. Nature 477:199–202. https://doi.org/10.1038/nature10282

    Article  CAS  PubMed  Google Scholar 

  • Jones NT, Germain RM, Grainger TN, Hall AM, Baldwin L, Gilbert B (2015) Dispersal mode mediates the effect of patch size and patch connectivity on metacommunity diversity. J Ecol 103:935–944. https://doi.org/10.1111/1365-2745.12405

    Article  Google Scholar 

  • Kleyer M et al (2008) The LEDA Traitbase: a database of plant life-history traits of North West Europe. J Ecol 96:1266–1274

    Article  Google Scholar 

  • Kolb A, Diekmann M (2005) Effects of life-history traits on responses of plant species to forest fragmentation. Conserv Biol 19:929–938. https://doi.org/10.1111/j.1523-1739.2005.00065.x

    Article  Google Scholar 

  • Komonen A, Penttilä R, Lindgren M, Hanski I (2000) Forest fragmentation truncates a food chain based on an old-growth forest bracket fungus. Oikos 90:119–126

    Article  Google Scholar 

  • Kormann U, Rosch V, Batary P, Tscharntke T, Orci KM, Samu F, Scherber C (2015) Local and landscape management drive trait-mediated biodiversity of nine taxa on small grassland fragments. Divers Distrib 21:1204–1217. https://doi.org/10.1111/ddi.12324

    Article  Google Scholar 

  • Krauss J et al (2010) Habitat fragmentation causes immediate and time-delayed biodiversity loss at different trophic levels. Ecol Lett 13:597–605. https://doi.org/10.1111/j.1461-0248.2010.01457.x

    Article  PubMed  PubMed Central  Google Scholar 

  • Kruess A, Tscharntke T (1994) Habitat fragmentation, species loss, and biological control. Science 264:1581–1584

    Article  CAS  PubMed  Google Scholar 

  • Kühn I, Durka W, Klotz S (2004) BiolFlor—a new plant-trait database as a tool for plant invasion ecology. Divers Distrib 10:363–365

    Article  Google Scholar 

  • Kuussaari M et al (2009) Extinction debt: a challenge for biodiversity conservation. Trends Ecol Evol 24:564–571

    Article  PubMed  Google Scholar 

  • Lid J, Lid DT (2005) Norsk flora, 7th edn. Det Norske Samlaget, Oslo

    Google Scholar 

  • LIFE (2008) LIFE and Europe’s grasslands: Restoring a forgotten habitat. http://ec.europa.eu/environment/life/publications/lifepublications/lifefocus/documents/grassland.pdf

  • Lindborg R, Helm A, Bommarco R, Heikkinen RK, Kühn I, Pykälä J, Pärtel M (2012) Effect of habitat area and isolation on plant trait distribution in European forests and grasslands. Ecography 35:356–363. https://doi.org/10.1111/j.1600-0587.2011.07286.x

    Article  Google Scholar 

  • Lindgaard A, Henriksen S (eds) (2011) Norwegian red list for ecosystems and habitat types 2011. Norwegian Biodiversity Information Centre, Trondheim

    Google Scholar 

  • MacLean SF (1983) Life cycles and the distribution of psyllids (Homoptera) in arctic and subarctic Alaska. Oikos 40:445–451

    Article  Google Scholar 

  • Martinson HM, Fagan WF (2014) Trophic disruption: a meta-analysis of how habitat fragmentation affects resource comsumption in terrestrial athropod systems. Ecol Lett 17:1178–1189

    Article  PubMed  Google Scholar 

  • Matthews TJ, Cottee-Jones HE, Whittaker RJ (2014) Habitat fragmentation and the species-area relationship: a focus on total species richness obscures the impact of habitat loss on habitat specialists. Divers Distrib 20:1136–1146

    Article  Google Scholar 

  • Maurer K, Durka W, Stöcklin J (2003) Frequency of plant species in remnants of calcareous grassland and their dispersal and persistence characteristics. Basic Appl Ecol 4:307–316

    Article  Google Scholar 

  • Nickel H (2003) The leafhoppers and planthoppers of Germany (Hemiptera, Auchenorrhyncha): Patterns and strategies in a highly diverse group of phytophagous insects. Pensoft, Sofia and Moscow

    Google Scholar 

  • Nickel H, Achtziger R (2005) Do they ever come back? Responses of leafhopper communities to extensification of land use. J Insect Conserv 9:319–333

    Article  Google Scholar 

  • Nickel H, Hildebrandt J (2003) Auchenorrhyncha communities as indicators of disturbance in grasslands (Insecta, Hemiptera)—a case study from the Elbe flood plains (northern Germany). Agr Ecosyst Environ 98:183–199. https://doi.org/10.1016/S0167-8809(03)00080-X

    Article  Google Scholar 

  • Nordén J, Penttilä R, Siitonen J, Tompoo E, Ovaskainen O (2013) Specialist species of wood-inhabiting fungi struggle while generalists thrive in fragmented boreal forests. J Ecol 101:701–712. https://doi.org/10.1111/1365-2745.12085

    Article  Google Scholar 

  • Norwegian Meteorological Institute (2015) eKlima. Data from weather station 18700 Blindern, Oslo, normal period 1961–1990. Available at eklima.met.no

  • Öckinger E, Smith HG (2006) Landscape composition and habitat area affects butterfly species richness in semi-natural grasslands. Oecologia 149:526–534. https://doi.org/10.1007/s00442-006-0464-6

    Article  PubMed  Google Scholar 

  • Öckinger E et al (2010) Life-history traits predict species responses to habitat area and isolation: a cross-continental synthesis. Ecol Lett 13:969–979. https://doi.org/10.1111/j.1461-0248.2010.01487.x

    Article  PubMed  Google Scholar 

  • Oksanen J et al. (2015) vegan: Community ecology package. R package version 2.3-2. http://CRAN.R-project.org/package=vegan

  • Ossiannilsson F (1978) The Auchenorrhyncha (Homoptera) of Fennoscandia and Denmark 1: introduction, infraorder Fulgoromorpha. Scandinavian Science Press, Klampenborg

    Google Scholar 

  • Ossiannilsson F (1981) The Auchenorrhyncha (Homoptera) of Fennoscandia and Denmark 2: the families Cicadidae, Cercopidae, Membracidae, and Cicadellidae (excl. Deltocephalinae). Scandinavian Science Press, Klampenborg

    Google Scholar 

  • Ossiannilsson F (1983) The Auchenorrhyncha (Homoptera) of Fennoscandia and Denmark 3: the family Cicadellidae: Deltocephalinae, catalogue, literature and index. Scandinavian Science Press, Klampenborg

    Google Scholar 

  • Piqueray J, Bisteau E, Cristofoli S, Palm R, Poschlod P, Mahy G (2011) Plant species extinction debt in a temperate biodiversity hotspot: community, species and functional traits approaches. Biol Conserv 144:1619–1629. https://doi.org/10.1016/j.biocon.2011.02.013

    Article  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Rösch V, Tscharntke T, Scherber C, Batáry P (2013) Landscape composition, connectivity and fragment size drive effects of grassland fragmentation on insect communities. J Appl Ecol 50:387–394. https://doi.org/10.1111/1365-2664.12056

    Article  Google Scholar 

  • Rösch V, Tscharntke T, Scherber C, Batáry P (2015) Biodiversity conservation across taxa and landscapes requires many small as well as single large habitat fragments. Oecologia 179:209–222. https://doi.org/10.1007/s00442-015-3315-5

    Article  PubMed  Google Scholar 

  • Rosenzweig ML (1995) Species diversity in space and time. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Roslin T, Várkonyi G, Koponen M, Vikberg V, Nieminen M (2014) Species-area relationships across four trophic levels—decreasing island size truncates food chains. Ecography 37:443–453

    Google Scholar 

  • Saar L, Takkis K, Partel M, Helm A (2012) Which plant traits predict species loss in calcareous grasslands with extinction debt? Divers Distrib 18:808–817. https://doi.org/10.1111/j.1472-4642.2012.00885.x

    Article  Google Scholar 

  • Sang A, Teder T, Helm A, Pärtel M (2010) Indirect evidence for an extinction debt of grassland butterflies half century after habitat loss. Biol Conserv 143:1405–1413

    Article  Google Scholar 

  • Schaffers AP, Raemakers IP, Sýkora KV, ter Braak CJF (2008) Arthropod assemblages are best predicted by plant species composition. Ecology 89:782–794

    Article  PubMed  Google Scholar 

  • Scherber C et al (2010) Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature 468:553–556. https://doi.org/10.1038/nature09492

    Article  CAS  PubMed  Google Scholar 

  • Schnitzler F-R, Hartley S, Lester PJ (2011) Trophic-level responses differ at plant, plot, and fragment levels in urban native forest fragments: a hierarchical analysis. Ecol Entomol 36:241–250

    Article  Google Scholar 

  • Söderman G (2007) Taxonomy, distribution, biology and conservation status of Finnish Auchenorrhyncha (Hemiptera: Fulgoromorpha et Cicadomorpha). Finnish Environ 7:1–101

    Google Scholar 

  • Stewart AJA, Wright AF (1995) A new inexpensive suction apparatus for sampling arthropods in grassland. Ecol Entomol 20:98–102

    Article  Google Scholar 

  • Stork NE, Srivastava DS, Eggleton P, Hodda M, Lawson G, Leakey RRB, Watt AD (2017) Consistency of effects of tropical-forest disturbance on species composition and richness relative to use of indicator taxa. Conserv Biol 31:924–933. https://doi.org/10.1111/cobi.12883

    Article  CAS  PubMed  Google Scholar 

  • Tilman D, May RM, Lehman CL, Nowak MA (1994) Habitat destruction and the extinction debt. Nature 371:65–66

    Article  Google Scholar 

  • Tscharntke T et al (2012) Landscape moderation of biodiversity patterns and processes—eight hypotheses. Biol Rev 87:661–685. https://doi.org/10.1111/j.1469-185X.2011.00216.x

    Article  PubMed  Google Scholar 

  • Vellend M, Baeten L, Myers-Smith IH, Elmendorf SC, Beauséjour R, Brown CD, De Frenne P, Verheyen K, Wipf S (2013) Global metaanalysis reveals no net change in local-scale plant biodiversity over time. Proc Nat Acad Sci USA 110:19456–19459

    Article  CAS  PubMed  Google Scholar 

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

    Book  Google Scholar 

  • Vilà M, Ibáñez I (2011) Plant invasions in the landscape. Landscape Ecol 26:461–472

    Article  Google Scholar 

  • Weiher E, van der Werf A, Thompson K, Roderick M, Garnier E, Eriksson O (1999) Challenging theophrastus: a common core list of plant traits for functional ecology. J Veg Sci 10:609–620

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Smith GM (2007) Analysing ecological data. Springer, New York

    Book  Google Scholar 

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Acknowledgements

This study was carried out under the projects “Survey and monitoring of red-listed species” (ARKO, funded by the Norwegian Environment Agency), and “Management of biodiversity and ecosystem services in spatially structured landscapes” (funded by the Norwegian Research Council, grant 208434/F40). We are grateful to A. Often, O. Skarpaas, O.E. Stabbetorp and J. Wesenberg for field work contributions and H. Nickel for inputs on hopper generalist and specialist classification, and to two anonymous reviewers for valuable inputs on a previous version of the manuscript.

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  1. Norwegian Institute for Nature Research (NINA), Gaustadalléen 21, 0349, Oslo, Norway

    Siri Lie Olsen, Marianne Evju & Anders Endrestøl

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  1. Siri Lie Olsen
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Correspondence to Marianne Evju.

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Communicated by David Hawksworth.

Appendices

Appendix 1: Overview of species

See Tables 4 and 5.

Table 4 Overview of recorded vascular plant species, with abbreviations used in figures, habitat specificity, status as invasive species (Gederaas et al. 2012) and Red list status (Henriksen and Hilmo 2015), number of patches in which the species was recorded, and mean abundance (percentage of sub-plots) in sample plots with occurrence of the species
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Table 5 Overview of recorded hoppers, with abbreviations used in figures, habitat specificity and Red list status (Henriksen and Hilmo 2015), number of patches in which the species was recorded, and mean abundance (no. of specimens) in sample plots with occurrence of the species
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Appendix 2: Ordination results

See Tables 6, 7, 8, 9 and Figures 4, 5, 6, 7.

Table 6 Correlation coefficients (Kendall’s τ) of environmental variables with ordination axes of plant species composition
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Table 7 Constrained ordination results with fraction of variation explained (FVE, in %) of the species/trait composition by the explanatory variables, alone or with conditioning variables, and pseudo-F from permutation tests with 999 permutations
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Table 8 Correlation coefficients (Kendall’s τ) of environmental variables with ordination axes of hopper species composition
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Table 9 Constrained ordination results with fraction of variation explained (FVE, in  %) of the species/trait composition by the explanatory variables, alone or with conditioning variables, and pseudo-F from permutation tests with 999 permutations
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Fig. 4
figure 4

GNMDS ordination plot of plant habitat specialist species composition in 200 sample plots in 20 habitat patches. Only species with a total sub-plot frequency > 40 are shown. Arrows indicate correlations between the ordination and environmental variables, with the length of the arrows proportional to the correlation strength. For species abbreviations, see Table 4

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Fig. 5
figure 5

RDA ordination plot of total plant community weighted mean trait composition as a response to patch size and connectivity in 200 sample plots in 20 habitat patches. See Table 1 for details on traits

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Fig. 6
figure 6

GNMDS ordination plot of hopper habitat specialist species composition in 36 sample plots in 12 habitat patches. Only species with > 10 individuals in the dataset are shown. Arrows indicate correlations between the ordination and environmental variables, with the length of the arrows proportional to the correlation strength. For species abbreviations, see Table 5

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Fig. 7
figure 7

RDA ordination plot of total hopper community weighted mean trait composition as a response to patch size in 36 sample plots in 12 habitat patches. There was no variation in trait composition related to patch connectivity. Some trait names were slightly adjusted to avoid overlap. See Table 1 for details on traits

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Olsen, S.L., Evju, M. & Endrestøl, A. Fragmentation in calcareous grasslands: species specialization matters. Biodivers Conserv 27, 2329–2361 (2018). https://doi.org/10.1007/s10531-018-1540-z

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