Agri-environment schemes do not support Brown Hare populations due to inadequate scheme application
Abstract
The goal of many agri-environment schemes (AES) is to increase biodiversity in agroecosystems. AES effects are often measured on invertebrates and birds; mammals as indicator species are infrequently targets of such researches. Our goal was to evaluate the local-scale effects of the Hungarian Agri-Environmental Measures (AEM) on the European brown hare (Lepus europaeus), which shows decreasing population trends across Europe. We compared hare abundances and their dropping numbers in AEM and control agricultural arable and grassland fields of 17 game management units in two seasons. We also examined the quality of arable fields based on their margin width and vegetation cover. We found that margin quality was higher in AEM than in the control fields. Control grasslands had higher vegetation quality than the AEM grasslands. We found a significant difference in hare counts between AEM and control arable fields in spring but no difference in autumn. The dropping densities did not differ in any season, treatment category or agroecosystem type. We conclude that the AEM program (2009-2014) in Hungary was not effective for the hare, and this might have been caused by the inadequate or weak application of AEM practices. We provide recommendations for future AEM programs to enhance biodiversity.
References
Báldi, A., Batáry, P. & Erdős, S. (2005): Effects of grazing intensity on bird assemblages and populations of Hungarian grasslands. – Agriculture, Ecosystems and Environment 108(3): 251–263. https://doi.org/10.1016/j.agee.2005.02.006
Báldi, A. & Faragó, S. (2007): Long-term changes of farmland game populations in a post-socialist country (Hungary). – Agriculture, Ecosystems and Environment 118(1–4): 307–311. https://doi.org/10.1016/j.agee.2006.05.021
Batáry, P., Dicks, L. V., Kleijn, D. & Sutherland, W. J. (2015): The role of agri-environment schemes in conservation and environmental management. – Conservation Biology 29(4): 1006–1016. https://doi.org/10.1111/cobi.12536
Benton, T. G., Vickery, J. A. & Wilson, J. D. (2003): Farmland biodiversity: Is habitat heterogeneity the key? – Trends in Ecology and Evolution 18(4): 182–188. https://doi.org/10.1016/S0169-5347(03)00011-9
Birkhofer, K., Wolters, V. & Diekötter, T. (2014): Grassy margins along organically managed cereal fields foster trait diversity and taxonomic distinctness of arthropod communities. – Insect Conservation and Diversity 7(3): 274–287. https://doi.org/10.1111/icad.12051
Bray, Y., Devillard, S., Marboutin, E., Mauvy, B. & Péroux, R. (2007): Natal dispersal of European hare in France. – Journal of Zoology 273(4): 426–434. https://doi.org/10.1111/j.1469-7998.2007.00348.x
Broughton, R. K., Shore, R. F., Heard, M. S., Amy, S. R., Meek, W. R., Redhead, J. W., Turk, A. & Pywell, R. F. (2014): Agri-environment scheme enhances small mammal diversity and abundance at the farm-scale. – Agriculture, Ecosystems and Environment 192: 122–129. https://doi.org/10.1016/j.agee.2014.04.009
Canova, L., Gazzola, A., Pollini, L. & Balestrieri, A. (2020): Surveillance and habitat diversity affect European brown hare (Lepus europaeus) density in protected breeding areas. – European Journal of Wildlife Research 66(4). https://doi.org/10.1007/s10344-020-01405-x
Cardarelli, E., Meriggi, A., Brangi, A. & Vidus-Rosin, A. (2011): Effects of arboriculture stands on European hare Lepus europaeus spring habitat use in an agricultural area of northern Italy. – Acta Theriologica 56(3): 229–238. https://doi.org/10.1007/s13364-010-0019-4
Concepción, E. D., Aneva, I., Jay, M., Lukanov, S., Marsden, K., Moreno, G., Oppermann, R., Pardo, A., Piskol, S., Rolo, V., Schraml, A. & Díaz, M. (2020): Optimising biodiversity gain of European agriculture through regional targeting and adaptive management of conservation tools. – Biological Conservation 241: 108384. https://doi.org/10.1016/j.biocon.2019.108384
Csányi, S., Lehoczki, R. & Sonkoly, K. (2011): National game management database of Hungary. – International Journal of Information Systems and Social Change 1(4): 34–43. https://doi.org/10.4018/jissc.2010100103
Dahlin, A. S., Ramezanian, A., Campbell, C. D., Hillier, S. & Öborn, I. (2015): Waste recovered by-products can increase growth of grass-clover mixtures in low fertility soils and alter botanical and mineral nutrient composition. – Annals of Applied Biology 166(1): 105–117. https://doi.org/10.1111/aab.12168
Edwards, P. J., Fletcher, M. R. & Berny, P. (2000): Review of the factors affecting the decline of the European brown hare, Lepus europaeus (Pallas, 1778) and the use of wildlife incident data to evaluate the significance of paraquat. – Agriculture, Ecosystems and Environment 79(2–3): 95–103. https://doi.org/10.1016/S0167-8809(99)00153-X
European Comission (2019): The Common Agricultural Policy; Separating Fact from Fiction. 9 pp.
George, M. R. & Bell, M. E. (2001): Rangeland management series: Using stage of maturity to predict the quality of annual range forage. – Rangeland Management Series, Publication 8019, University of California, 7 pp. https://doi.org/10.3733/ucanr.8019
Hackländer, K., Tataruch, F. & Ruf, T. (2002): The effect of dietary fat content on lactation energetics in the European Hare (Lepus europaeus). – Physiological and Biochemical Zoology: Ecological and Evolutionary Approaches 75(1): 19–28. https://doi.org/10.1086/515863
Haerer, G., Nicolet, J., Bacciarini, L., Gottstein, B. & Giacometti, M. (2001): Todesursachen, Zoonosen und Reproduktion bei Feldhasen in der Schweiz. – Schweizer Archiv für Tierheilkunde 143(4): 193–201. https://doi.org/10.5169/seals-591650
Häring, A., Stolze, M., Zanoli, R., Vairo, D. & Dabbert, S. (2005): Further development of organic farming policy in Europe, with particular emphasis on EU enlargement QLK5-2002-00917. 17 pp.
Hodge, I., Hauck, J. & Bonn, A. (2015): The alignment of agricultural and nature conservation policies in the European Union. – Conservation Biology 29(4): 996–1005. https://doi.org/10.1111/cobi.12531
Hungarian Ministry of Agriculture and Rural Development (2009): Decree No. 61 of 2009 (V. 14.) FVM of the Ministry of Agriculture and Rural Development laying down the conditions of support for agricultural environmental management from the European Agricultural Fund for Rural Development. Hungary.
Hungarian Ministry of Agriculture and Rural Development. (2015): ‘New Hungary’ Rural Development Programme 2007–2013. (May): 1–552.
Huysentruyt, F., Scheppers, T., Verschelde, P., Onkelinx, T. & Casaer, J. (2018): Analysis of the usefulness of transect counts in monitoring local brown hare populations Description of monitoring in 12 test areas and detailed analysis of the results from Bertembos. Brussels, 47 pp.
Jennings, N., Smith, R. K., Hackländer, K., Harris, S. & White, P. C. L. (2006): Variation in demography, condition and dietary quality of hares Lepus europaeus from high-density and low-density populations. – Wildlife Biology 12: 179–189. https://doi.org/10.2981/0909-6396(2006)12
Kaiser, T., Rohner, M. S., Matzdorf, B. & Kiesel, J. (2010): Validation of grassland indicator species selected for result-oriented agri-environmental schemes. – Biodiversity and Conservation 19(5): 1297–1314. https://doi.org/10.1007/s10531-009-9762-8
Kamieniarz, R., Voigt, U., Panek, M., Strauss, E. & Niewegłowski, H. (2013): The effect of landscape structure on the distribution of brown hare Lepus europaeus in farmlands of Germany and Poland. – Acta Theriologica 58(1): 39–46. https://doi.org/10.1007/s13364-012-0091-z
Kleijn, D., Rundlöf, M., Scheper, J., Smith, H. G. & Tscharntke, T. (2011): Does conservation on farmland contribute to halting the biodiversity decline? – Trends in Ecology and Evolution 26(9): 474–481. https://doi.org/10.1016/j.tree.2011.05.009
Kleijn, D. & Sutherland, W. J. (2003): How effective are European agri-environment schemes in conserving and promoting biodiversity? – Journal of Applied Ecology 40(6): 947–969. https://doi.org/10.1111/j.1365-2664.2003.00868.x
Kovács-Hostyánszki, A. & Báldi, A. (2012): Set-aside fields in agri-environment schemes can replace the market-driven abolishment of fallows. – Biological Conservation 152: 196–203. https://doi.org/10.1016/j.biocon.2012.03.039
Kovács Katona, J. (2007): Agri-environmental management and rural development: Hungary after EU accession. – Applied Studies in Agribusiness and Commerce 1(1): 35–40. https://doi.org/10.19041/apstract/2007/1/4
Langhammer, M., Grimm, V., Pütz, S. & Topping, C. J. (2017): A modelling approach to evaluating the effectiveness of Ecological Focus Areas: The case of the European brown hare. – Land Use Policy 61(1307): 63–79. https://doi.org/10.1016/j.landusepol.2016.11.004
Lenth, V. R., Buerkner, P., Herve, M., Love, J., Riebl, H. & Singmann, H. (2020): Package ‘emmeans’: Estimated Marginal Means, aka Least-Squares Means. 84. R package version1.6.2-1
Lioy, S., Braghiroli, S., Dematteis, A., Meneguz, P. G. & Tizzani, P. (2015): Faecal pellet count method: some evaluations of dropping detectability for Capreolus capreolus Linnaeus, 1758 (Mammalia: Cervidae), Cervus elaphus Linnaeus, 1758 (Mammalia: Cervidae) and Lepus europaeus Pallas, 1778 (Mammalia: Leporidae). – Italian Journal of Zoology 82(2): 231–237. https://doi.org/10.1080/11250003.2014.963178
MacDonald, D. W., Tattersall, F. H., Service, K. M., Firbank, L. G. & Feber, R. E. (2007): Mammals, agri-environment schemes and set-aside – What are the putative benefits? – Mammal Review 37(4): 259–277. https://doi.org/10.1111/j.1365-2907.2007.00100.x
Marja, R., Herzon, I., Viik, E., Elts, J., Mänd, M., Tscharntke, T. & Batáry, P. (2014): Environmentally friendly management as an intermediate strategy between organic and conventional agriculture to support biodiversity. – Biological Conservation 178: 146–154. https://doi.org/10.1016/j.biocon.2014.08.005
Marja, R., Kleijn, D., Tscharntke, T., Klein, A. M., Frank, T. & Batáry, P. (2019): Effectiveness of agri-environmental management on pollinators is moderated more by ecological contrast than by landscape structure or land-use intensity. – Ecology Letters 22(9): 1493–1500. https://doi.org/10.1111/ele.13339
Marshall, E. J. P., West, T. M. & Kleijn, D. (2006): Impacts of an agri-environment field margin prescription on the flora and fauna of arable farmland in different landscapes. – Agriculture, Ecosystems and Environment 113(1–4): 36–44. https://doi.org/10.1016/j.agee.2005.08.036
Mayer, M., Ullmann, W., Sunde, P., Fischer, C. & Blaum, N. (2018): Habitat selection by the European hare in arable landscapes: The importance of small-scale habitat structure for conservation. – Ecology and Evolution 8(23): 11619–11633. https://doi.org/10.1002/ece3.4613
Meichtry-Stier, K. S., Jenny, M., Zellweger-Fischer, J. & Birrer, S. (2014): Impact of landscape improvement by agri-environment scheme options on densities of characteristic farmland bird species and brown hare (Lepus europaeus). – Agriculture, Ecosystems and Environment 189: 101–109. https://doi.org/10.1016/j.agee.2014.02.038
Misiorowska, M. & Wasilewski, M. (2008): Spatial organisation and mortality of released hares — Preliminary results. – Annales Zoologici Fennici 45(4): 286–290. https://doi.org/10.5735/086.045.0408
Neumann, F., Schai-Braun, S., Weber, D. & Amrhein, V. (2011): European hares select resting places for providing cover. – Hystrix 22(2): 291–299. https://doi.org/10.4404/Hystrix-22.2-4546
Panek, M. (2018): Habitat factors associated with the decline in brown hare abundance in Poland in the beginning of the 21st century. – Ecological Indicators 85(December 2016): 915–920. https://doi.org/10.1016/j.ecolind.2017.11.036
Pe’er, G., Dicks, L. V., Visconti, P., Arlettaz, R., Báldi, A., Benton, T. G., Collins, S., Dieterich, M., Gregory, R. D., Hartig, F., Henle, K., Hobson, P. R., Kleijn, D., Neumann, R. K., Robijns, T., Schmidt, J., Shwartz, A., Sutherland, W. J., Turbé, A., Wulf, F. & Scott, A. V. (2014): EU agricultural reform fails on biodiversity. – Science 344(6188): 1090–1092. https://doi.org/10.1126/science.1253425
Pelorosso, R., Boccia, L. & Amici, A. (2008): Simulating Brown hare (Lepus europaeus Pallas) dispersion: A tool for wildlife management of wide areas. – Italian Journal of Animal Science 7(3): 335–350. https://doi.org/10.4081/ijas.2008.335
Perry, M. E. & Robertson, A. W. (2012): Cleared and uncleared pellet plots as indices of brown hare density. – New Zealand Journal of Ecology 36(2): 157–163.
Petrovan, S. O., Dixie, J., Yapp, E. & Wheeler, P. M. (2017): Bioenergy crops and farmland biodiversity: benefits and limitations are scale-dependant for a declining mammal, the brown hare. – European Journal of Wildlife Research 63(3). https://doi.org/10.1007/s10344-017-1106-5
Petrovan, S. O., Ward, A. I. & Wheeler, P. M. (2012): Habitat selection guiding agri-environment schemes for a farmland specialist, the brown hare. – Animal Conservation 16(3): 344–352. https://doi.org/10.1111/acv.12002
Piha, M., Tiainen, J., Holopainen, J. & Vepsäläinen, V. (2007): Effects of land-use and landscape characteristics on avian diversity and abundance in a boreal agricultural landscape with organic and conventional farms. – Biological Conservation 140(1–2): 50–61. https://doi.org/10.1016/j.biocon.2007.07.021
Pike, N. (2011): Using false discovery rates for multiple comparisons in ecology and evolution. – Methods in Ecology and Evolution 2(3): 278–282. https://doi.org/10.1111/j.2041-210X.2010.00061.x
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Core Team (2018): Linear and nonlinear mixed effects models. – R package version 3.1-131.1
Prugh, L. R. & Krebs, C. J. (2004): Snowshoe hare pellet-decay rates and aging in different habitats. – Wildlife Society Bulletin 32(2): 386–393. https://doi.org/10.2193/0091-7648(2004)32[386:shpraa]2.0.co;2
QGIS Development Team (2017): QGIS Geographic Information System. – Open Source Geospatial Foundation Project. http://qgis.osgeo.org
R Core Team (2020): R: A language and environment for statistical computing. – R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Reichlin, T., Klansek, E. & Hackländer, K. (2006): Diet selection by hares (Lepus europaeus) in arable land and its implications for habitat management. – European Journal of Wildlife Research 52(2): 109–118. https://doi.org/10.1007/s10344-005-0013-3
Reynolds, J. C., Stoate, C., Brockless, M. H., Aebischer, N. J. & Tapper, S. C. (2010): The consequences of predator control for brown hares (Lepus europaeus) on UK farmland. – European Journal of Wildlife Research 56(4): 541–549. https://doi.org/10.1007/s10344-009-0355-3
Rodríguez-Pastor, R., Luque-Larena, J. J., Lambin, X. & Mougeot, F. (2016): “Living on the edge”: The role of field margins for common vole (Microtus arvalis) populations in recently colonised Mediterranean farmland. – Agriculture, Ecosystems and Environment 231: 206–217. https://doi.org/10.1016/j.agee.2016.06.041
Roedenbeck, I. A. & Voser, P. (2008): Effects of roads on spatial distribution, abundance and mortality of brown hare (Lepus europaeus) in Switzerland. – European Journal of Wildlife Research 54(3): 425–437. https://doi.org/10.1007/s10344-007-0166-3
Sainte Marie, C. de (2014): Rethinking agri-environmental schemes. A result-oriented approach to the management of species-rich grasslands in France. – Journal of Environmental Planning and Management 57(5): 704–719. https://doi.org/10.1080/09640568.2013.763772
Santilli, F. & Galardi, L. (2016): Effect of habitat structure and type of farming on European hare (Lepus europaeus) abundance. – Hystrix 27(2). https://doi.org/10.4404/hystrix-27.2-11974
Schai-Braun, S. C., Reichlin, T. S., Ruf, T., Klansek, E., Tataruch, F., Arnold, W. & Hackländer, K. (2015): The European hare (Lepus europaeus): A picky herbivore searching for plant parts rich in fat. – PLoS ONE 10(7): 1–16. https://doi.org/10.1371/journal.pone.0134278
Schai-Braun, S. C., Ruf, T., Klansek, E., Arnold, W. & Hackländer, K. (2020): Positive effects of set-asides on European hare (Lepus europaeus) populations: Leverets benefit from an enhanced survival rate. – Biological Conservation 244(March). https://doi.org/10.1016/j.biocon.2020.108518
Schai-Braun, S. C., Weber, D. & Hackländer, K. (2013): Spring and autumn habitat preferences of active European hares (Lepus europaeus) in an agricultural area with low hare density. – European Journal of Wildlife Research 59(3): 387–397. https://doi.org/10.1007/s10344-012-0684-5
Schmidt, N. M., Asferg, T. & Forchhammer, M. C. (2004): Long-term patterns in European brown hare population dynamics in Denmark: Effects of agriculture, predation and climate. – BMC Ecology 4: 1–7. https://doi.org/10.1186/1472-6785-4-15
Sliwinski, K., Ronnenberg, K., Jung, K., Strauß, E. & Siebert, U. (2019): Habitat requirements of the European brown hare (Lepus europaeus Pallas, 1778) in an intensively used agriculture region (Lower Saxony, Germany). – BMC Ecology 19(1): 1–11. https://doi.org/10.1186/s12898-019-0247-7
Smith, R. K., Jennings, N. V. & Harris, S. (2005a): A quantitative analysis of the abundance and demography of European hares Lepus europaeus in relation to habitat type, intensity of agriculture and climate. – Mammal Review 35(1): 1–24. https://doi.org/10.1111/j.1365-2907.2005.00057.x
Smith, R. K., Jennings, N. V. & Harris, S. (2005b): A quantitative analysis of the abundance and demography of European hares Lepus europaeus in relation to habitat type, intensity of agriculture and climate. – Mammal Review 35(1): 1–24. https://doi.org/10.1111/j.1365-2907.2005.00057.x
Thompson, W. L., White, G. C. & Gowan, C. (1998): Chapter 10. Mammals. Pp. 301–322. In: Thompson, W. L., White, G. C. & Gowan, C. (eds): Monitoring vertebrate populations. – Elsevier Academic Press, 365 pp.
Vasseur, C., Joannon, A., Aviron, S., Burel, F., Meynard, J. M. & Baudry, J. (2013): The cropping systems mosaic: How does the hidden heterogeneity of agricultural landscapes drive arthropod populations? – Agriculture, Ecosystems and Environment 166(February): 3–14. https://doi.org/10.1016/j.agee.2012.08.013
Vaughan, N., Lucas, E. A., Harris, S. & White, P. C. L. (2003): Habitat associations of European hares Lepus europaeus in England and Wales: Implications for farmland management. – Journal of Applied Ecology 40(1): 163–175. https://doi.org/10.1046/j.1365-2664.2003.00784.x
Venables, W. N. & Ripley, B. D. (2003): Modern applied statistics with S. 4th ed. – Springer, New York, 498 pp.
Vepsäläinen, V., Tiainen, J., Holopainen, J., Piha, M. & Seimola, T. (2010): Improvements in the Finnish Agri-Environment Scheme are needed in order to support rich farmland avifauna. – Annales Zoologici Fennici 47(5): 287–305. https://doi.org/10.5735/086.047.0501
Wong, V. & Hickling, G. J. (1999): Assessment and management of hare impact on high-altitude vegetation. – Science for Conservation. Vol. 116. Department of Conservation, Wellington, 40 pp.
Yi, N. (2019): Negative Binomial and Zero-Inflated Mixed Models. https://github.com/nyiuab/NBZIMM
Zabel, A. & Holm-Müller, K. (2008): Conservation performance payments for carnivore conservation in Sweden. – Conservation Biology 22(2): 247–251. https://doi.org/10.1111/j.1523-1739.2008.00898.x
Zabel, A. & Roe, B. (2009): Optimal design of pro-conservation incentives. – Ecological Economics 69(1): 126–134. https://doi.org/10.1016/j.ecolecon.2009.08.001
Zaccaroni, M., Biliotti, N., Buccianti, A., Calieri, S., Ferretti, M., Genghini, M., Riga, F., Trocchi, V. & Dessì-Fulgheri, F. (2013): Winter locomotor activity patterns of European hares (Lepus europaeus). – Mammalian Biology 78(6): 482–485. https://doi.org/10.1016/j.mambio.2013.07.001
Zellweger-Fischer, J., Kéry, M. & Pasinelli, G. (2011): Population trends of brown hares in Switzerland: The role of land-use and ecological compensation areas. – Biological Conservation 144(5): 1364–1373. https://doi.org/10.1016/j.biocon.2010.11.021
Zuur, A. F., Ieno, E. N., Walker, J. N., Saveliev, A. A. & Smith, G. M. (2009): Mixed effects models and extensions in ecology with R. – Springer-Verlag, New York, 574 pp. https://doi.org/10.1007/978-0-387-87458-6
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