Abstract
Land-use change and current game management have favored an increasing population of wild ungulates (especially deer) in many regions of the Northern Hemisphere. Here, we assess the impact of high deer densities (>30 ind km−2) on the highly diverse woody vegetation of Mediterranean ecosystems, where big game have been favored for the last decades. We examine whether prolonged deer browsing (over 30 years) affected plant composition, diversity and dynamics of the original (non-browsed) vegetation. Deer browsing led to an average decrease of 30.4 % in woody plant diversity (species richness), due to a lack of regeneration for the most preferred plant species. Species belonging to early stages of succession (mostly Labiatae and Cistaceae) were non-preferred by deer. Conversely, the most preferred species belonged mainly to late stages of plant succession. Deer impact on Mediterranean shrublands is causing biotic homogenization of plant communities and is threatening vegetation dynamics by forcing it to return to earlier succession stages. Strict deer population control favouring larger trophies but lower offspring numbers together with an adequate habitat management (increasing grass and acorn availability) would be the most efficient measures to reverse this diversity loss. Restoration work seems only appropriate for the most vulnerable species. We highlight the need of sampling deer-free areas with low or null historical browsing to assess the real impact of deer on woody plant diversity and vegetation dynamics.
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References
Alverson WS, Waller DM, Solheim SL (1988) Forests too deer: edge effects in Northern Wisconsin. Conserv Biol 2:348–358
Anderson RC, Katz AJ (1993) Recovery of browse-sensitive tree species following release from white-tailed deer Odocoileus virginianus Zimmerman browsing pressure. Biol Conserv 63:203–208
Anderson RC, Loucks OL (1979) White-tailed deer (Odocoileus virginianus) influence on structure and composition of Tsuga canadensis forests. J Appl Ecol 16:855–861
Baker JE (1997) Trophy hunting as a sustainable use of wildlife resources in Southern and Eastern Africa. J Sustain Tourism 5(4):302–332
Braun-Blanquet J (1951) Planzensoziologie. Springer, Vienne
Bugalho MN, Milne JA (2003) The composition of the diet of red deer (Cervus elaphus) in a Mediterranean environment: a case of nutritional constraint? For Ecol Manag 181:23–29
Busch G (2006) Future European agricultural landscapes: what can we learn from existing quantitative land use scenario studies? Agr Ecosyst Environ 114:121–140
Callaway RM (1995) Positive interactions among plants. Bot Rev 61:306–349
Côté SD, Rooney TP, Tremblay JP, Dussault C, Waller D (2004) Ecological impacts of deer overabundance. Annu Rev Ecol Evol Syst 35:113–147
De Calesta DS (1997) Ecosystem management for deer. In: McShea WJ, Rappole JH, Underwood HB (eds) The science of overabundance: deer ecology and population management. Smithsonian Institute, Washington DC, pp 267–279
Díaz MP, Campos P, Pulido FJ (2008) Importancia de la caza en el desarrollo sustentable y en la conservación de la biodiversidad. In: Carranza J, de Sáez Buruaga M (eds) Manual de la gestión integral de los ecosistemas mediterráneos en los terrenos cinegéticos de Andalucía. Junta de Andalucía, Sevilla, pp 21–32
Dietz DR, Udall RH, Yeager LE (1962) Chemical composition and digestibility by mule deer of selected forage species, Cache La Poudre Range, Colorado. Colorado Game and Fish Dept, Tech Bull 14
Fernández-Olalla M, San Miguel A (2008) La selección de dieta en los fitófagos: conceptos, métodos e índices. Pastos XXXVII 1:5–47
Fernández-Olalla M, Muñoz Igualada J, Martínez-Jauregui M, Rodríguez-Vigal C, San Miguel-Ayanz A (2006) Selección de especies y efecto del ciervo (Cervus elaphus L.) sobre arbustedos y matorrales de los Montes de Toledo, España central. Investigación Agraria. Sistemas y Recursos Forestales 15(3):329–338
Fernández-Ortiz JJ (2007) Propuesta de plan de gestión de los mamíferos fitófagos en el Parque Nacional de Cabañeros. Proyecto Fin de Carrera. Universidad Politécnica de Madrid. Madrid
Festa-Bianchet M (2003) Exploitative wildlife management as a selective pressure for life-history evolution of large mammals. In: Festa-Bianchet M, Apollonio M (eds) Animal behavior and wildlife conservation. Island Press, Washington DC, pp 191–207
Fuller RJ, Gill RMA (2001) Ecological impacts of increasing numbers of deer in British woodland. Forestry 74:193–199
Gershenzon J, Croteau R (1991) Terpenoids. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites. Academic Press, New York, pp 165–219
Ghilarov A (2000) Ecosystem functioning and intrinsic value of biodiversity. Oikos 90:408–412
Gill RMA (1990) Monitoring the status of European and North American Cervids. GEMS Information Series 8, UNEP, Nairobi, p 277
Gill RMA (1992a) A review of damage by mammals in north temperate forests: 1. Deer. Forestry 65:45–169
Gill RMA (1992b) A review of damage by mammals in north temperature forests. 3. Impact on trees and forests. Forestry 65:363–388
Gill RMA, Beardall V (2001) The impact of deer on woodlands: the effects of browsing and seed dispersal on vegetation structure and composition. Forestry 74:209–218
Gordon IJ, Hester AJ, Festa-Bianchet M (2004) The management of wild large herbivores to meet economic, conservation and environmental objectives. J Appl Ecol 41:1021–1031
Gülz P, Kobold U, Michaelis K, Vostrowsky O (1984) The composition of terpene hydrocarbons in the essential oils from leaves of four Cistus species. Zeitschrift für Naturforschung A 39:699–704
Harmer R, Kiewitt A, Morgan G, Gill R (2010) Does the development of bramble (Rubus fruticosus L. agg.) facilitate the growth and establishment of tree seedlings in woodlands by reducing deer browsing damage? Forestry 83:93–102
Horsley SB, Stout SL, Decalesta DS (2003) White-tailed deer impact on the vegetation dynamics of a northern hardwood forest. Ecol Appl 13:98–118
Hrubes D, Ajzen I, Daigle J (2001) Predicting hunting intentions and behavior: an application of the theory of planned behavior. Leisure Sci 23:165–178
Hurtado-Gonzales JL, Bodmer RE (2004) Assessing the sustainability of brocket deer hunting in the Tamshiyacu-Tahuayo Communal Reserve, Northeastern Peru. Biol Conserv 116:1–7
Jaccard P (1912) The distribution of the flora in the alpine zone. New Phytol 11:37–50
Jackson DA (1995) PROTEST: a PROcrustean randomization TEST of community environment concordance. Ecoscience 2(3):297–303
Jacobs J (1974) Quantative measurement of food selection. A modification of the forage ratioand Ivlev′s electivity index. Oecologia 14:413–417
Knoche S, Lupi F (2012) The economic value of publicly accessible deer hunting land. J Wildl Manag 76:462–470
Koleff P, Gaston KJ, Lennon JJ (2003) Measuring beta diversity for presence-absence data. J Anim Ecol 72:367–382
Krebs CJ (1999) Ecological methodology. Addison Wesley, White Plains
Kuiters AT, Mohren GMJ, Van Wieren SE (1996) Ungulates in temperate forest ecosystems. For Ecol Manag 88:1–5
Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A et al (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808
MacDonald D, Crabtree JR, Wiesinger G, Dax T, Stamou N, Fleury P, Lazpita JG, Gibon A (2000) Agricultural abandonment in mountain areas of Europe: environmental consequences and policy response. J Environ Manag 59:47–69
Maestre FT (2004) On the importance of patch attributes, environmental factors and past human impacts as determinants of perennial plant species richness and diversity in Mediterranean semiarid steppes. Diversity Distrib 10:21–29
Marquis DA (1974) The impact of deer browsing on Allegheny hardwood regeneration. USDA For Serv Res Pap NE-308
Martin WE, Gum RL (1978) Economic value of hunting, fishing, and rural outdoor recreation. Wildl Soc Bull 63–67
Martin JL, Stockton SA, Allombert S, Gaston AJ (2010) Top-down and bottom-up consequences of unchecked ungulate browsing on plant and animal diversity in temperate forests: lessons from a deer introduction. Biol Invasions 12:353–371
Martínez M, Rodríguez-Vigal C, Jones OR, Coulson T, San Miguel A (2005) Different hunting strategies select for different weights in red deer. Biol Lett 1:353–356
Martínez-Jáuregui M, Arenas C, Herruzo C (2011) Understanding long-term hunting statistics: the case of Spain (1972–2007). For Syst 20(1):139–150
McInnes PF, Naiman RJ, Pastor J, Cohen Y (1992) Effects of moose browsing on vegetation and litter of the boreal forest, Isle Royale, Michigan, USA. Ecology 73:2059–2075
Milner JM, Bonenfant C, Mysterud A, Gaillard JM, Csányi S, Stenseth NC (2006) Temporal and spatial development of red deer harvesting in Europe: biological and cultural factors. J App Ecol 43:721–734
Miranda M, Díaz L, Sicilia M, Cristóbal I, Cassinello J (2011) Seasonality and edge effect determine herbivory risk according to different plant association models. Plant Biol 13:160–168
Oh HK, Jones MB, Longhurst WM (1968) Comparison of rumen microbial inhibition resulting from various essential oils isolated from relatively unpalatable plant species. Appl Microbiol 16:39–44
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H (2012) vegan: community Ecology Package. R package version 2.0-3
Olden JD (2006) Biotic homogenization: a new research agenda for conservation biogeography. J Biogeogr 33(12):2027–2039
Pastor J, Dewey B, Naiman RJ, McInnes PF, Cohen Y (1993) Moose browsing and soil fertility in the boreal forests of Isle Royale National Park. Ecology 74:467–480
Perea DF, Perea R (2008) Vegetación y Flora de los Montes de Toledo. Ediciones Covarrubias, Toledo
Peres-Neto P, Jackson D (2001) How well do multivariate data sets match? The advantages of a Procrustean superimposition approach over the Mantel test. Oecologia 129:169–178
Pineda FD (2001) Intensification, rural abandonment and nature conservation in Spain. In: Bunce RGH et al (eds) Examples of European agri-environment schemes and livestock systems and their influence on Spanish cultural landscapes. Alterra, Wageningen, pp 23–46
Pinheiro JC, Bates DM (2000) Mixed effects models in S and S-Plus. Statistics and computing. Springer, New York
Pinheiro P, Bates D, DebRoy S, Sarkar D, the R Development Core Team (2012) nlme: linear and nonlinear mixed effects models. R package version 3.1-103
Porter WF (1994) Burgeoning ungulate populations in national parks: is intervention warranted? In: McCullough DR, Barrett RH (eds) Wildlife 2001: populations. Elsevier, New York, pp 304–312
Poyatos R, Lotron J, Llorens P (2003) Land use and land cover change after agricultural abandonment. Mountain Res Dev 23:362–368
Putman RJ (1994) Damage by deer in coppice woodlands: an analysis of factors affecting the severity of damage and options for management. Q J For 88:45–54
Putman RJ, Moore N (1998) Impact of deer in lowland Britain on agriculture, forestry and conservation habitats. Mammal Rev 28:141–164
Rey-Benayas JM, Martins A, Nicolau JM, Schulz JJ (2007) Abandonment of agricultural land: an overview of drivers and consequences. Perspect Agr Vet Sci Nutr Nat Res 2:057. doi:10.1079/PAVSNNR20072057
Rivas-Martínez S (2011) Map of vegetation series, geoseries and geopermaseries from Spain. (Report on potential vegetation map of Spain). Itinera Geobot 18:5–800
Robles C, Garzino S (2000) Infraspecific variability in the essential oil composition of Cistus monspeliensis leaves. Phytochemistry 53:71–75
Rooney TP (2009) High white-tailed deer densities benefit graminoids and contribute to biotic homogenization of forest ground-layer vegetation. Plant Ecol 202:103–111
Rooney TP, Waller DM (2003) Direct and indirect effects of deer in forest ecosystems. For Ecol Manag 181:165–176
San Miguel A, Pérez-Carral C, Roig S (1999) Deer and traditional agrosilvopastoral systems of Mediterranean Spain. A new problem of sustainability for a new concept of land use. Options Méditerranéennes 39:261–264
San Miguel A, Perea R, Fernández-Olalla M (2010) Wild ungulates vs. extensive livestock. Looking back to face the future. Options Meditérranneenes 92:27–34
Savage RE (1931) The relation between the feeding of the herring off the east coast of England and the plankton of the surrounding waters. Fish Investig Minist Agri Food Fish Series 2 12:1–88
Southwood TRE, Henderson PA (2000) Ecological methods. Blackwell Science, Oxford
Stockton SA, Allombert S, Gaston AJ, Martin JL (2005) A natural experiment on the effects of high deer densities on the native flora of coastal temperate rain forests. Biol Conserv 126:118–128
Stromayer KAK, Warren RJ (1997) Are overabundant deer herds in the eastern United States creating alternate stable states in forest plant communities? Wildl Soc Bull 25:227–234
Tilghman NG (1989) Impacts of white-tailed deer on forest regeneration in northwestern Pennsylvania. J Wildl Manag 53:524–532
Torres-Porras J, Carranza J, Pérez-González J (2009) Selective culling of Iberian red deer stags (Cervus elaphus hispanicus) by selective montería in Spain. Eur J Wildl Res 75:117–123
Tremblay JP, Huot J, Potvin F (2006) Divergent nonlinear responses of the boreal forest field layer along an experimental gradient of deer densities. Oecologia 150:78–88
White MA (2012) Long-term effects of deer browsing: composition, structure and productivity in a northeastern Minnesota old-growth forest. For Ecol Manage 269:222–228
Acknowledgments
We would like to thank Irene Moreno for her help in the fieldwork and many land owners for giving us permission to collect the data. Ramón Perea received a grant from the Ministry of Education (MEC-Colaboración) to initiate this research study.
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Communicated by Marcelo F. Tognelli.
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Perea, R., Girardello, M. & San Miguel, A. Big game or big loss? High deer densities are threatening woody plant diversity and vegetation dynamics. Biodivers Conserv 23, 1303–1318 (2014). https://doi.org/10.1007/s10531-014-0666-x
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DOI: https://doi.org/10.1007/s10531-014-0666-x