Abstract
Wood-pastures are socio-ecological systems covering vast areas in Europe. Although used for grazing and production of various forest goods, wood-pastures harbour a rich biodiversity and are usually considered as High Nature Value Farmlands. However, socio-economic pressures are driving the transformation of these valuable landscapes from multi-functional, heterogeneous habitats to homogeneous areas through either intensification or land abandonment. We investigated how changes in management intensity influence the taxonomic diversity, functional diversity and functional composition of birds in these landscapes using generalized linear models. In contrast to taxonomic diversity, functional diversity decreased significantly towards shrub-dominated and less heterogeneous areas related to the abandonment of grazing and/or understory management practices. Grassland and generalist species, and associated guilds such as granivores, ground-nesters and ground-foragers are almost absent less managed areas. On the other hand, shrub-dominated areas favour forest species, particularly understory/canopy foragers and arboreal nesters, although the forest guild is still well-represented in actively managed, heterogeneous areas. Our results indicate the abandonment of wood-pasture management affects the prevalence of grassland and generalist species, leading to functional diversity loss and potentially reduced ecosystem functioning. We suggest non-intensive, active management is needed to maintain habitat heterogeneity and canopy openness, enhancing trait diversity in wood-pastures.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
All data generated or analysed during this study is included in Supplementary Information files (Online Resources 1 and 2).
References
Bergmeier E, Roellig M (2014) Diversity, threats and conservation of European wood-pastures. In: Plieninger T, Hartel T (eds) European wood-pastures in transition: a social-ecological approach. Routledge, London, pp 19–38. https://doi.org/10.4324/9780203797082
Berrahmouni N, Escuté X, Regato P, Stein C (2007) Beyond cork: a wealth of resources for people and nature. Lessons from the Mediterranean. WWF Mediterranean, Rome
Bibby CJ, Burgess ND, Hill DA, Mustoe SH (2005) Bird census techniques. Elsevier Academic Press, London. https://doi.org/10.1016/c2009-0-03531-4
Bugalho MN, Plieninger T, Aronson J, Ellatifi M (2009) Open woodlands: A diversity of uses (and overuses). In: Aronson J, Pereira JS, Pausas JG (eds) Cork Oak woodlands on the edge. Ecology, adaptive management, and restoration, Society for Ecological Restoration International. Island Press, Washington D.C., pp 33–47. https://doi.org/10.1111/j.1526-100x.2010.00701.x
Bugalho MN, Caldeira MC, Pereira JS, Aronson J, Pausas JG (2011) Mediterranean Cork Oak Savannas require human use to sustain biodiversity and ecosystem services. Front Ecol Environ 9(5):278–286. https://doi.org/10.1890/100084
Butler SJ, Boccaccio L, Gregory RD, Voříšek P, Norris K (2010) Quantifying the impact of land-use change to European farmland bird populations. Agric Ecosyst Environ 137:348–357. https://doi.org/10.1016/j.agee.2010.03.005
Castro H, Freitas H (2009) Aboveground biomass and productivity in the Montado: from herbaceous to shrub dominated communities. J Arid Environ 73:506–511. https://doi.org/10.1016/j.jaridenv.2008.12.009
Ceia RS, Ramos JA (2016) Birds as predators of cork and holm oak pests. Agrofor Syst 90(1):159–176. https://doi.org/10.1007/s10457-014-9749-7
Clavero M, Brotons L (2010) Functional homogenization of bird communities along habitat gradients: accounting for niche multidimensionality. Glob Ecol Biogeogr 19(5):684–696. https://doi.org/10.1111/j.1466-8238.2010.00544.x
Correia RA, Franco AMA, Palmeirim JM (2015) Role of the Mediterranean Sea in differentiating European and North African woodland bird assemblages. Community Ecol 16:106–114
Crowder DW, Northfield TD, Strand MR, Snyder WE (2010) Organic agriculture promotes evenness and natural pest control. Nature 466:109–112. https://doi.org/10.1038/nature09183
de Bello F, Lavorel S, Díaz S et al (2010) Towards an assessment of multiple ecosystem processes and services via functional traits. Biodivers Conserv 19:2873–2893. https://doi.org/10.1007/s10531-010-9850-9
Devictor V, Mouillot D, Meynard C, Jiguet F, Thuiller W, Mouquet N (2010) Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: the need for integrative conservation strategies in a changing world. Ecol Lett 13:1030–1040. https://doi.org/10.1111/j.1461-0248.2010.01493.x
Díaz S, Purvis A, Cornelissen JHC, Mace GM, Donoghue MJ, Ewers RM, Jordano P, Pearse WD (2013) Functional traits, the phylogeny of function, and ecosystem service vulnerability. Ecol Evol 3:2958–2975. https://doi.org/10.1002/ece3.601
Dormann CF, Elith J, Bacher S, Buchmann C et al (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36(1):27–46. https://doi.org/10.1111/j.1600-0587.2012.07348.x
Estel S, Kuemmerle T, Alcántara C, Levers C, Prishchepov A, Hostert P (2015) Mapping farmland abandonment and recultivation across Europe using MODIS NDVI time series. Remote Sens Environ 163:312–325. https://doi.org/10.1016/j.rse.2015.03.028
Flynn DF, Gogol-Prokurat M, Nogeire T, Molinari N, Richers BT, Lin BB, DeClerck F (2009) Loss of functional diversity under land use intensification across multiple taxa. Ecol Lett 12(1):22–33. https://doi.org/10.1111/j.1461-0248.2008.01255.x
Gagic V, Bartomeus I, Jonsson T, Taylor A, Winqvist C, Fischer C, Slade EM, Steffan-Dewenter I, Emmerson M, Potts SG, Tscharntke T, Weisser W, Bommarco R (2015) Functional identity and diversity of animals predict ecosystem functioning better than species-based indices. Proc R Soc Lond B Biol Sci 282(1801):20142620. https://doi.org/10.1098/rspb.2014.2620
Godinho C, Rabaça JE (2011) Birds like it Corky: the influence of habitat features and management of ‘montados’ in breeding bird communities. Agrofor Syst 82:183–195. https://doi.org/10.1007/s10457-010-9345-4
Godinho S, Guiomar N, Machado R et al (2016) Assessment of environment, land management, and spatial variables on recent changes in montado land cover in southern Portugal. Agrofor Syst 90(1):177–192. https://doi.org/10.1007/s10457-014-9757-7
Graves AR, Burgess PJ, Palma JHN, Herzog F, Moreno G, Bertomeu M, Dupraz C, Liagre F, Keesman K, van der Werf W, de Nooy AK, van den Briel JP (2007) Development and application of bio-economic modelling to compare silvoarable, arable, and forestry systems in three European countries. Ecol Eng 29:434–449. https://doi.org/10.1016/j.ecoleng.2006.09.018
Hartel T, Plieninger T (2014) The social and ecological dimensions of wood-pastures. In: Plieninger T, Hartel T (eds) European wood-pastures in transition: a social-ecological approach. Routledge, London, pp 3–18. https://doi.org/10.4324/9780203797082
Hartel T, Plieninger T, Varga A (2015) Wood-pastures in Europe In: Kirby KJ, Watkinsi C (eds.), Europe's changing woods and forests: from wildwood to managed landscapes, Chapter 5, vol 432, CABI, Wallingford, pp 63–76
Hevia V, Martin-Lopez B, Palomo S, Garcia-Llorente M, de Bello F, Gonzalez JA (2016) Trait-based approaches to analyse links between the drivers of change and ecosystem services: synthesizing existing evidence and future challenges. Ecol Evol 7:831–844. https://doi.org/10.1002/ece3.2692
Hillebrand H, Bennett DM, Cadotte MW (2008) Consequences of dominance: a review of evenness effects on local and regional ecosystem processes. Ecology 89:1510–1520. https://doi.org/10.1890/07-1053.1
Hooper DU, Chapin FS, Ewel JJ, Hector A 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
Horák J, Pavlíček J, Kout J, Halda JP (2018) Winners and losers in the wilderness: response of biodiversity to the abandonment of ancient forest pastures. Biodivers Conserv 27:3019–3029. https://doi.org/10.1007/s10531-018-1585-z
Jakobsson S, Wood H, Ekroos J, Lindborg R (2018) Contrasting multi-taxa functional diversity patterns along vegetation structure gradients of wooded pastures. In: Jakobsson S (ed.), Wooded or treeless pastures?: linking policy, farmers' decisions and biodiversity. Dissertation, Stockholm University
Laliberté E, Legendre P, Shipley B (2014) FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1:0–12. https://cran.rproject.org/web/packages/FD/FD.pdf
Landis DA (2017) Designing agricultural landscapes for biodiversity-based ecosystem services. Basic Appl Ecol 18:1–12. https://doi.org/10.1016/j.baae.2016.07.005
Leal AI, Rainho A, Martins RC et al (2016) Modelling future scenarios to improve woodland landscapes for birds in the Mediterranean. J Nat Conserv 30:103–112. https://doi.org/10.1016/j.jnc.2016.02.001
Leal AI, Acácio M, Meyer CFJ et al (2019) Grazing improves habitat suitability for many ground foraging birds in Mediterranean wooded grasslands. Agric Ecosyst Environ 270–271:1–8. https://doi.org/10.1016/j.agee.2018.10.012
Lepš J, de Bello F, Lavorel S, Berman S (2006) Quantifying and interpreting functional diversity of natural communities: practical considerations matter. Preslia 78:481–501
Levers C, Schneider M, Prishchepov AV, Estel S, Kuemmerle T (2018) Spatial variation in determinants of agricultural land abandonment in Europe. Sci Total Environ 644:95–111. https://doi.org/10.1016/j.scitotenv.2018.06.326
Luck GW, Lavorel S, McIntyre S, Lumb K (2012) Improving the application of vertebrate trait-based frameworks to the study of ecosystem services. J Anim Ecol 81:1065–1076. https://doi.org/10.1111/j.1365-2656.2012.01974.x
Mag Z, Ódor P (2015) The effect of stand-level habitat characteristics on breeding bird assemblages in Hungarian temperate mixed forests. Community Ecol 16:156–166. https://doi.org/10.1556/168.2015.16.2.3
Martin TG, Possingham HP (2005) Predicting the impact of livestock grazing on birds using foraging height data. J Appl Ecol 42:400–408. https://doi.org/10.1111/j.1365-2664.2005.01012.x
Moreno G, Aviron S, Berg S et al (2018) Agroforestry systems of high nature and cultural value in Europe: provision of commercial goods and other ecosystem services. Agrofor Syst 92:877–891. https://doi.org/10.1007/s10457-017-0126-1
Mouillot D, Graham NAJ, Villéger S, Mason NWH, Bellwood DR (2013) A functional approach reveals community responses to disturbances. Trends Ecol Evol 28:167–177. https://doi.org/10.1016/j.tree.2012.10.004
Mönkkönen M, Juutinen A, Mazziotta A, Miettinen K, Podkopaev D, Reunanen P, Salminen H, Tikkanen OP (2014) Spatially dynamic forest management to sustain biodiversity and economic returns. J Environ Manag 134:80–89. https://doi.org/10.1016/j.jenvman.2013.12.021
Nikolov SC, Demerdzhiev DA, Popgeorgiev GS, Plachiyski DG (2011) Bird community patterns in sub-Mediterranean pastures: the effects of shrub cover and grazing intensity. Anim Biodivers Conserv 34(1):11–21
Oksanen O, Blanchet FG, Kindt R, Legendre P, McGlinn D (2016) Vegan: Community Ecology Package. R Package Version 2.3-0. https://github.com/vegandevs/vegan.
Oksuz DP, Aguiar CA, Tápia S et al (2020) Increasing biodiversity in wood-pastures by protecting small shrubby patches. For Ecol Manag 464:118041. https://doi.org/10.1016/j.foreco.2020.118041
Oldén A, Komonen A, Tervonen K, Halme P (2017) Grazing and abandonment determine different tree dynamics in wood-pastures. Ambio 46(2):227–236. https://doi.org/10.1007/s13280-016-0821-6
Pinto-Correia T, Ribeiro S (2012) HNV in 35 countries in Europe: Portugal. In: Oppermann R, Beaufoy G, Jones G (eds) High Nature Value Farming in Europe. 35 European countries-experiences and perspectives. Verlag Regionalkultur, Heidelberg, pp 336–345. https://doi.org/10.1659/mrd.mm126
Pons J, Pausas JG (2007) Acorn dispersal estimated by radio-tracking. Oecologia 153(4):903–911. https://doi.org/10.1007/s00442-007-0788-x
Plieninger T, Hartel T, Martín-lópez B, Beaufoy G, Bergmeier E, Kirby K, Montero MJ, Moreno G, Oteros-Rozas E, Uytvanck JV (2015) Wood-pastures of Europe: Geographic coverage, social-ecological values, conservation management, and policy implications. Biol Conserv 190:70–79. https://doi.org/10.1016/j.biocon.2015.05.014
Queiroz C, Beilin R, Folke C, Lindborg R (2014) Farmland abandonment: threat or opportunity for biodiversity conservation? A global review. Front Ecol Environ 12:288–296. https://doi.org/10.1890/120348
R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
Reino L, Porto M, Morgado R et al (2010) Effects of changed grazing regimes and habitat fragmentation on Mediterranean grassland birds. Agric Ecosyst Environ 138:27–34. https://doi.org/10.1016/j.agee.2010.03.013
Rey Benayas JM, Martins A, Nicolau JM, Schulz JJ (2007) Abandonment of agricultural land: an overview of drivers and consequences. CAB Rev Perspect Agric Vet Sci Nutr Nat Resour. https://doi.org/10.1079/PAVSNNR20072057
Rey Benayas JM, Galván I, Carrascal LM (2010) Differential effects of vegetation restoration in Mediterranean abandoned cropland by secondary succession and pine plantations on bird assemblages. For Ecol Manag 260(1):87–95. https://doi.org/10.1016/j.foreco.2010.04.004
Roellig M, Sutcliffe LME, Sammul M, von Wehrden H, Newig J, Fischer J (2016) Reviving wood-pastures for biodiversity and people: a case study from western Estonia. Ambio 45:185–195. https://doi.org/10.1007/s13280-015-0719-8
Rotenberry JT, Wiens JA (1980) Habitat structure, patchiness, and avian communities in North American steppe vegetation: a multivariate analysis. Ecology 61:1228–1250. https://doi.org/10.2307/1936840
Santana J, Porto M, Gordinho L, Reino L, Beja P (2012) Long-term responses of Mediterranean birds to forest fuel management. J Appl Ecol 49:632–643. https://doi.org/10.1111/j.1365-2664.2012.02141.x
Sekercioglu CH (2006) Ecological significance of bird populations. Handbook of the Birds of the World 11, Lynx Edicions, Spain, pp 15–51
Sirami C, Brotons L, Martin JL (2007) Vegetation and songbird response to land abandonment: from landscape to census plot. Divers Distrib 13(1):42–52. https://doi.org/10.1111/j.1472-4642.2006.00297.x
Sirami C, Seymour C, Midgley G, Barnard P (2009) The impact of shrub encroachment on savanna bird diversity from local to regional scale. Divers Distrib 15:948–957. https://doi.org/10.1111/j.1472-4642.2009.00612.x
Spitzer L, Konvička M, Beneš J, Tropek R, Tuf IH, Tufová J (2008) Does closure of traditionally managed open woodlands threaten epigeic invertebrates? Effects of coppicing and high deer densities. Biol Conserv 141:827–837. https://doi.org/10.1016/j.biocon.2008.01.005
Tews J, Brose U, Grimm V, Tielborger K, Wichmann MC, Schwager M, Jeltsch F (2004) Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. J Biogeogr 31:79–92. https://doi.org/10.1046/j.0305-0270.2003.00994.x
Torralba M, Fagerholm N, Burgess PJ, Moreno G, Plieninger T (2016) Do European agroforestry systems enhance biodiversity and ecosystem services? A meta-analysis. Agric Ecosyst Environ 230:150–161. https://doi.org/10.1016/j.agee.2016.06.002
Vanhooydonck B, Herrel A, Gabela A, Podos J (2009) Wing shape variation in the medium ground finch (Geospiza fortis): an ecomorphological approach. Biol J Linn Soc Lond 98:129–138. https://doi.org/10.1111/j.1095-8312.2009.01269.x
Vickery JA, Arlettaz R (2012) The importance of habitat heterogeneity at multiple scales for birds in European agricultural landscapes. In: Fuller RJ (ed) Birds and habitat: relationships in changing landscapes. Cambridge University Press, Cambridge, pp 177–204. https://doi.org/10.1017/cbo9781139021654.009
Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89(8):2290–2301. https://doi.org/10.1890/07-1206.1
Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer, New York. https://doi.org/10.1111/j.1541-0420.2011.01616.x
Wood SA, Karp DS, DeClerck F, Kremen C, Naeem S, Palm CA (2015) Functional traits in agriculture: agrobiodiversity and ecosystem services. Trends Ecol Evol 30:531–539. https://doi.org/10.1016/j.tree.2015.06.013
Zhang D (2018) R-squared and related measures. Documentation for the R package ‘rsq’. Version 1.1. https://cran.r-project.org/web/packages/rsq/rsq.pdf
Acknowledgements
We are thankful to Aldina Franco for her insightful contributions during fieldwork design and to several landowners and managers who kindly allowed us to work on their land.
Funding
This work was supported by Fundação para a Ciência e a Tecnologia (FCT), through doctoral and post-doctoral grants: DPO (PD/BD/106044/2015) and RAC (SFRH/BD/66150/2009, SFRH/BPD/118635/2016).
Author information
Authors and Affiliations
Contributions
Duygu P. Oksuz: Conceptualization, Data Curation, Formal analysis, Investigation, Methodology, Writing-original draft, Writing-review & editing. Jorge M. Palmeirim: Conceptualization, Methodology, Supervision, Funding acquisition, Writing-review & editing. Ricardo A. Correia: Conceptualization, Data Curation, Investigation, Methodology, Funding acquisition, Supervision, Writing-review & editing.
Corresponding author
Ethics declarations
Conflicts of interest
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Oksuz, D.P., Palmeirim, J.M. & Correia, R.A. Bird taxonomic and functional responses to land abandonment in wood-pastures. Agroforest Syst 95, 1167–1176 (2021). https://doi.org/10.1007/s10457-021-00649-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10457-021-00649-z