Research article

Ungulate browsing causes species loss in deciduous forests independent of community dynamics and silvicultural management in Central and Southeastern Europe

E.D. Schulze , O. Bouriaud, J. Wäldchen, N. Eisenhauer, H. Walentowski, C. Seele, E. Heinze, U. Pruschitzki, G. Dănilă, G. Marin, D. Hessenmöller, L. Bouriaud, M. Teodosiu

E.D. Schulze
Max-Planck Institute for Biogeochemistry, PO Box 100164, 07701 Jena, Germany. Email:
O. Bouriaud
Forest Research and Management Institute, Bucharest 128 Bd. Eroilor, Voluntari, Romania
J. Wäldchen
Max-Planck Institute for Biogeochemistry, PO Box 100164, 07701 Jena, Germany
N. Eisenhauer
Institute for Ecology, University of Jena, 07701 Jena, Germany; German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany; Institute for Biology, University of Leipzig, Johannisallee 21, 04103 Leipzig, Germany
H. Walentowski
Bavarian State Inst. of Forestry, Hans-Carl-von-Carlowitz-Platz 1, 85354 Freising, Germany
C. Seele
Max-Planck Institute for Biogeochemistry, PO Box 100164, 07701 Jena, Germany
E. Heinze
Förstereistrasse 34, 01099 Dresden, Germany
U. Pruschitzki
Max-Planck Institute for Biogeochemistry, PO Box 100164, 07701 Jena, Germany
G. Dănilă
University Ştefan del Mare of Suceava, 13 University Street, 720229 Suceava, Romania
G. Marin
Forest Research and Management Institute, Bucharest 128 Bd. Eroilor, Voluntari, Romania
D. Hessenmöller
Max-Planck Institute for Biogeochemistry, PO Box 100164, 07701 Jena, Germany
L. Bouriaud
University Ştefan del Mare of Suceava, 13 University Street, 720229 Suceava, Romania
M. Teodosiu
Forest Research and Management Institute, Bucharest 128 Bd. Eroilor, Voluntari, Romania

Online First: November 27, 2014
Schulze, E., Bouriaud, O., Wäldchen, J., Eisenhauer, N., Walentowski, H., Seele, C., Heinze, E., Pruschitzki, U., Dănilă, G., Marin, G., Hessenmöller, D., Bouriaud, L., Teodosiu, M. 2014. Ungulate browsing causes species loss in deciduous forests independent of community dynamics and silvicultural management in Central and Southeastern Europe. Annals of Forest Research DOI:10.15287/afr.2014.273

Grid-based inventories of 1,924 deciduous forests plots in Germany and 4,775 in Romania were used to investigate tree species composition as affected by browsing and grazing under different forest management (rotation forestry, selectively cut forest, protected forest). At regional scale, the loss of tree species in the dominant layer was between 52 to 67% in Germany and of 10 to 30% in Romania, with largest effects in protected nature reserves in Germany. At plot level, only 50% (Germany) to 54% (Romania) of canopy species were found in the regeneration layer with a height of 1.5 m. Browsing was influenced by the proportion of Fagus in the regenerating trees in Germany, and by stand density, basal area, and management in both regions. Structural equation modeling explained 11 to 26% of the variance in species loss based on the fresh loss of the terminal bud in the winter prior to the inventory work (one season browsing). Browsing (and grazing in Romania) is shown to be a significant cause of species loss across both countries and all management types. Potential cascading effects on other organisms of deciduous forest ecosystems are discussed. We conclude that the present hunting practices that support overabundant ungulate populations constitute a major threat to the biodiversity of deciduous forests in Germany and Romania and to other places with similar ungulate management, and that changes my only be possible by modernizing the legal framework of hunting.

Abs, C., Ewald, J., Walentowski, H. and Winter, S. 2008 Untersuchungen der Schattentoleranz von Baumarten auf der Grundlage der Datenbank bayerischer Naturwaldreservate. Tuexenia 28, 23-40.

Adams S.N., 1975 Sheep and cattle grazing in forests: a review. J. Appl. Ecol. 12, 143-152.
DOI: 10.2307/2401724

Allombert, S., Gaston, A.J. and Martin, J.L. 2005 Anatural experiment on the impact of overabundant deer on songbird populations. Biol. Conserv. 126, 1-13. DOI: 10.1016/ j.biocon.2005.04.001

Ammer, C. 1996. Impact of ungulates on structure and dynamics of natural regeneration of mixed mountain forests in the Bavarian Alps. ForestEcology and Management 88, 43-53.
DOI: 10.1016/S0378-1127(96)03808-X

Arbuckle, J.L. 2010 IBM SPSS Amos 19 User's Guide. – Amos Development Corporation,Crawfordville,FL,USA.

Begon, M., Harper, J.L. and Townsend, C.R. 1990 Ecology: individuals, populations and communities. 2nd edn. Blackwell, 945 pp.

Brousseau P.M., Hébert, C., Cloutier, C., Côté, S.D. 2013 Short-term effects of reduced white-tailed deer density on insectcommunities in a strongly overbrowsed boreal forest ecosystem. Biodivers. Conserv. 22, 77-92. DOI: 10.1007/s10531-012-0400-5

Burschel, P. and Huss J. 2002 Grundriss des Walödbaus. 3rd edn. Ulmer, 487 pp.

Caquet, B., Montpied, P., Dreyer, E., Epron, D. and Collet, C. 2009 Response to canopy opening does not act as a filter to Fagus sylvatica and Acer sp. advance regeneration in a mixed temperate forest. Ann. For. Sci. 67, 20-25.

Carlowitz H.C. von 1713 Sylvicultura oeconomica: Anweisung zur wilden Baum-Zucht. Reprint 2000. Braun Verlag, 414 pp.

Côté, S.D., Rooney, T.P., Tremblay, J.P., Dussault. C. and Waller, D.M. 2004. Ecological impacts of deer overabundance. Ann. Rev. Ecol. Evol. Syst. 35, 113-147. DOI: 10.1146/annurev. ecolsys.35.021103.105725

Crawley, M.J. 1988 Herbivores and plan population dynamics. In Plant Population Ecology. AJ Davy, MJ Hutchings, AR Watkinson (eds). Blackwell, pp. 367-392

Crișan, V. 1994 Jäger? Schlächter Ceauseccu. Verlag Dieter Holzmann,Mainz, 154 pp.

Ellenberg H. 1978 Vegetation Mitteleuropas mit den Alpen in ökologischer Sicht. 2nd. edn. Ulmer, 981 pp.
European Court of Human Rights, 2012. Case of Herrmann vs. Germany. Application 9300/7. JudgementStrasbourg, June 26, 2012. URL:

Gardianul, 27.07.2007.

Gautschi, A. 2010 Der Reichsjägermeister. Edition Nimrod bei JANA, 352 pp.

Gerhardt, P., Arnold, J.M., Hackländer, K. and Hochbichler, E. 2013 Determinants of deer impact in European forests – a systematic literature analysis. Forest Ecol. Manag. 310, 173-186. DOI: 10.1016/j.foreco.2013.08.030

Gill, R.M.A. 2006 The influence of large herbivores on tree recruitment and forest dynamics. In Large herbivore ecology, ecosystems dynamics and conservation. K. Danell, R. Bergström, P Duincan and J. Pastor (eds), Gill, R.M.A. and 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, I.J., Hester, A.J. and Festa Bianchet, M., 2004 Review: The management of wild large herbivores to meet economic, conservation and environmental objectives. J. Appl. Ecol. 41, 1021-1031. DOI: 10.1111/j.0021-8901.2004.00985.x

Grace, J.B. 2006 Structural equation modeling and natural systems. CambridgeUniversityPress.
DOI: 10.1017/CBO9780511617799

Hacker, H. 1998 Schmetterlinge und Sträucher. In Sträucher in Wald und Flur. edn. Bayer. Forstverein, pp. 510-520.

Harper, J.L. 1977 Population Biology of Plants. Academic Press.

Heinze, E., Boch, S., Fischer, M., Hessenmöller, D. et al. 2011 Habitat use of large ungulates in northeastern Germany in relation to forest management. ForestEcol. Manage. 261, 288-296.
DOI: 10.1016/j.foreco.2010.10.022

Hellström, E. and Reunala, A. 1995Forestry conflicts from the 1950s to 1983.Research Report 3. Joensuu, Finland: European Forest Institute.

Hessenmöller, D., Nieschulze, J., von Lüpke, N. and Schulze, E.D., 2011 Identification of forest management types from ground based and remotely sensed variables and the effect of forest management on forest structure and composition. Forstarchiv 82, 171-183.

Hofman, G., Pommer, U. and Jenssen, M. 2008 Wildökologische Lebensraumbewertung für die Bewirtschaftung des widerkäuenden Schalenwildes im nordostdeutschen Tiefland. Eberswalder Forstliche Schriftenreihe, 39, 1-207.

Holt, R.D. 1977 Predation, apparent competition and the structure of prey communities. Theor. Popul. Biol. 12, 197-229. DOI: 10.1016/0040-5809(77)90042-9

Horn, H.S. 1974 The ecology of secondary succession. Annual Review of Ecology and Systematics 5, 25-37 DOI: 10.1146/

Horsley SB, Stout SL, DeCalstea DS 2003 White-tailed deer impact on the vegetation dynamics of a northern hardwood forest. Ecological Applications 13, 98-118. DOI: 10.1890/1051-0761(2003)013[0098:WTDIOT]2.0.CO;2

Jorritsma, I.T. M., Van HeesA. F. M. and Mohren, G. M. J. 1999 Forestdevelopment in relation to ungulate grazing: a modeling approach." Forest Ecology and Management 120, 23-34.
DOI: 10.1016/S0378-1127(98)00540-4

Klötzli, F. 1965 Qualität und Quantität der Rehäsung in Wald- und Grünland-Gesellschaften des nördlichen Schweizer Mittellandes. Thesis ETH Zürich. 187 pp.

Korpel, S. 1995 Die Urwälder der Westkarpaten. Gustav Fischer Verlag,Jena, 310pp

Lang, G. 1994 Quartäre Vegetationsgeshichte Europas Gustav Fischer Verlag,Jena, 462 pp

Lessard, J.P., Reynolds, W.N., Bunn, W.A., Genung, M.A., Cregger, M.A., Felker-Quinn, E., Barrios-Garcia, N., Stevenson, M.L., Lawton, R.M., Brown, C.B., Patrick, M., Rock, J.H., Jenkins, M.A., Bailey, J.K., Schweitzer, J.A. 2012 Equivalence in the strength of deer herbivory an above and below ground communities. Basic and Applied Ecology13, 59-66. DOI: 10.1016/j.baae. 2011.11.001

Linder, P., Elfving, Band Zackrisson, O. 1997 Stand structure and successional trends in virgin boreal forest reserves in Sweden. ForestEcol. Manage. 98, 17–33. DOI: 10.1016/S0378-1127(97)00076-5

Lozano, J. Virgos E., Cabezas-Diáz S. and Mangas, J.G. 2007 Increase of large game species in Mediterranean areas: Is the European wildcat (Felis sylvestris) facing a new threat? Biol. Cons. 138, 321-329. DOI: 10.1016/j.biocon.2007.04.027

Luyssaert, S., Hessenmöller, D., von Lüpke, N., Kaiser, S. and Schulze, E.D. 2011 Quantifying land-use and disturbance intensity in forestry, based on the self-thinning relationship. Ecological Applications 21,3272-3284. DOI: 10.1890/10-2395.1

MADR, 2012. Raport tehnic operativ asupra situatiei din zootehnie la data de 30 iunie 2012 [Operative technical report on zootechnics - June 30, 2012]. URL :

Marin, G., Bouriaud, O., Dumitru, M., Nitu, D. 2009. Development ofRomania's National Forest Inventory. In National Forest Inventories: Pathways for Common Reporting, Tomppo et al. (Eds). Springer,Heidelberg.

Mayer, H. 1984. Wälder Europas. G Fischer Verlag, 691 pp.

Milner, J.M., Bonenfant, C., Mysterud, A., Gaillard, J.M., Csányi, S. and Stenseth, N.C.2006 Temporal and spatial development of red deerharvesting in Europe: biological and cultural factors. J. Appl. Ecol. 43, 721-734. DOI: 10.1111/j.1365-2664.2006.01183.x

Milner, J.M., Nilsen E.B. and Andreassen, H.P. 2007 Demographic side effects of selective hunting in ungulates and carnivores. Conservation Biology 21,35-47. DOI: 10.1111/j.1523-1739.2006.00591.x

Ministerul Mediului și Pădurilor 2011. Starea padurilor, 2010.[Forestreport, 2010]. URL: stareapadurilor2010.pdf

Mitchell, F.J.G. andKirby, K.L. 1990 The impact of large herbivores on the conservation of semi-natural woods in the British uplands. Forestry 63, 333-353. DOI: 10.1093/forestry/63.4.333

Modrý, M., Hubený, D. and Rejsek, K., 2004 Differential response of naturally regenerated European shade tolerant tree species to soil type and light availability. For. Ecol. Manage. 188, 185-195. DOI: 10.1016/j.foreco.2003.07.029

Müller, J., Bußler, H., Brustel, H., et al. 2005 Urwald relic species – Saproxylic beetles indicating structural qualities and habitat tradition. Waldökologie online 2, 106-113.

National Instituteof Statistics2013. Effective de animaleexistente la 1 decembrie 2013 [Existing domestic livestock - December 1, 2013]. URL:

Nationalpark Hainich, 2013 Waldentwicklung im Nationalpark Hainich. Erforschen Bd. 3, 1-166.

Nie, M. 2003 Drivers of natural resource-based political conflict. Policy Sciences 36, 307-341.
DOI: 10.1023/B:OLIC.0000017484.35981.b6

Niemelä, J., Young, J., Alard, D., Askasibar, M. et al. 2005 Identifying, managing and monitoring conflicts between forest biodiversity conservation and other human interests in Europe. Forest Policy Econ.7, 877-890. DOI: 10.1016/j.forpol.2004.04.005

Pépin, D., Renaud, P. C., Boscardin, Y., Goulard, M., Mallet, C., Anglard, F. and Ballon, P., 2006 Relative impact of browsing by red deer on mixed coniferous and broad-leaved seedlings—An enclosure-based experiment. Forest Ecol. Manage., 222, 302-313. DOI: 10.1016/j.foreco. 2005.10.034

Petritan, A.M., von Lüpke, B. and Petritan, I.C. 2009 Influence of light availability on growth, leaf morphology and plant architecture of beech (Fagus sylvatica L.), maple (Acer pseudoplatanus L.) and ash (Fraxinus excelsior L.) saplings. Europ. J. For. Res. 128, 61-74.
DOI: 10.1007/s10342-008-0239-1

R Development Core Team 2010 R: a language and environment for statistical computing.Vienna,Austria: R Foundation for Statistical Computing.

Reimoser, F. and Gossow, H. 1996 Impact of ungulates on forest vegetation and its dependence on the silvicultural system. ForestEcol. Manage. 88, 107-119. DOI: 10.1016/S0378-1127(96)03816-9

Scherber, C., Eisenhauer, N., Weisser, W. W., et al. 2010 Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature 468, 553-556. DOI: 10.1038/ nature09492

Schoonmaker, P., McKee, A., 1988. Species composition and ddiversity during secondary succession of coniferous forests in the Western Cascade Mountains ofOregon.ForestScience 34, 960-979

Schulze, E.D. 2014. Zuwachs und Entmischung der Verjüngung im Laubwald mit und ohne Wildverbiss. AFZ-Der Wald 11/2014, 26-27

Schulze, E.D., Bazzaz, F.A., Nadelhoffer, K.J., Koike T.,Takatsuki, S. 1996. Biodiversity and ecosystem functioning of temperate deciduous broad-leaved forests. SCOPE 55, 71-98.

Schulze, E.D., Hessenmöller, D., Seele, C., Wäldchen, J. and von Lüpke, N. 2010 Die Buche: eine Kultur- und Wirtschaftsgeschichte. Biologie in unserer Zeit 3/2010, 171-183. DOI: 10. 1002/biuz.201010421

Skarpe, C. and Hester, A. 2008 Plant traits, browsing and grazing herbivores, and vegetation dynamics. In The ecology of browsing and grazing. I.J. Gordon & H.H.T. Prins (eds). Ecological studies 195 pp., 217-261. Springer-Verlag, Striepen K. 2000 Einfluß von Wildverbiss auf die Verjüngungsentwicklung von Buchen- und Buchenmischwäldern in Nordrhein-Westfalen. NUA-Seminarberichte 4, 91-107.

Tanentzap, A.J., Bazley, D.R., Koh, S., Timciska, M., Haggith, E.G., Carleton and T.J., Coomes, D.A. 2011 Seeing the forest for the deer: Do reductions in deer-disturbance lead to forest recovery? Biological Conservation 144, 376-382. DOI: 10.1016/j.biocon.2010.09.015

Thoms, C., Gattinger, A., Jacob, M., Thomas, F.M. and Gleixner, G. 2010 Direct and indirect effects of tree diversity drive soil microbial diversity in temperate deciduous forest. Soil Biol. Biochem. 42, 1558-1565. DOI: 10.1016/j.soilbio.2010.05.030

Thüringen Forst 2010 Verbiss- und Schälsituation im Freistaat Thüringen. Internal information.

Tottewitz, F., Stubbe, C., Ahrens, M., Dobias, K., Goretzki, J. and Paustian, K.H. 1996 Die Losungszählung als Methode der Bestandsschätzung von wiederkäuenden Schalenwildarten. Z. Jagdwiss. 42, 111-122.

Tremblay, J.P., Hout, J. and Potvin, F. 2007 Density-related effects of deer browsing on the regeneration dynamics of boreal forests. J. Appl. Ecol. 44, 552-562. DOI: 10.1111/j.1365-2664.2007.01290.x

Van Hees, A. F. M., Kuiters, A. T., & Slim, P. A. 1996 Growth and development of silver birch, pedunculate oak and beech as affected by deer browsing. ForestEcology and Management, 88, 55-63. DOI: 10.1016/S0378-1127(96)03809-1

von Lüpke, B. 2005 Canopy management, plant quality and harvesting regime. In The ecological and silvicultural bases for underplanting beech (Fagus sylvatica L.) belowNorwayspruce shelterwood (Picea abies L. Karst). G. Oleskog, M. Löf, (eds).Frankfurt amMain, Schriften aus des Forstlichen Fakultät der Universität Göttingen, Band 139. J.D. Sauerländer's Verlag.

Walentowski, H., Bussler, H., Bergmeier, E., Blaschke, M. et al., 2010.Sinddie deutschen Buchenwälder adäquat für die Erhaltung der buchenwaldtypischen Flora und Fauna? Eine kritische Bewertung basierend auf der Herkunft der Waldarten des mitteleuropäischen Tief- und Hügellandes. Forstarchiv 81, 195-217.

Wittmann, F., Schöngart, J., Montero, J.C., Motzer, T., Junk, W.J., Piedade, M.T.F., Queiroz, H.L., Worbes, M., 2006. Three species composition and diversity gradients in white-water forests across the Amazon basin. J. Biogeography 33, 1334-1347. DOI: 10.1111/j.1365-2699.2006. 01495.x

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