Abstract
Massive historical land cover changes in the Central European lowlands have resulted in a forest distribution that now comprises small remnants of ancient forests and more recently established post-agricultural forests. Here, land-use history is considered a key driver of recent herb-layer community changes, where an extinction debt in ancient forest remnants and/or a colonization credit in post-agricultural forests are being paid over time. On a regional scale, these payments should in theory lead toward a convergence in species richness between ancient and post-agricultural forests over time. In this study, we tested this assumption with a resurvey of 117 semi-permanent plots in the well-studied deciduous forests of the Prignitz region (Brandenburg, NE Germany), where we knew that the plant communities of post-agricultural stands exhibit a colonization credit while the extinction debt in ancient stands has largely been paid. We compared changes in the species richness of all herb layer species, forest specialists and ancient forest indicator species between ancient and post-agricultural stands with linear mixed effect models and determined the influence of patch connectivity on the magnitude of species richness changes. Species richness increased overall, but the richness of forest specialists increased significantly more in post-agricultural stands and was positively influenced by higher patch connectivity, indicating a convergence in species richness between the ancient and post-agricultural stands. Furthermore, the richness of ancient forest indicator species only increased significantly in post-agricultural stands. For the first time, we were able to verify a gradual payment of the colonization credit in post-agricultural forest stands using a comparison of actual changes in temporal species richness.
Similar content being viewed by others
References
Baeten L, Bauwens B, De Schrijver A, De Keersmaeker L, Van Calster H, Vandekerkhove K, Roelandt B, Beekman H, Verheyen K (2009) Herb-Layer changes (1954-2000) related to the conversion of coppice-with-standards forest and soil acidification. Appl Veg Sci 12:187–197
Baeten L, Hermy M, Van Daele S, Verheyen K (2010) Unexpected understory community development after 30 years in ancient and post-agricultural forests. J Ecol 98:1447–1453
Bates D, Maechler M, Bolker B, Walker S (2015) lme4: Linear mixed-effect models using Eigen and S4. R package version 1.1-8, http://CRAN.R-project.org/package=lme4
Bernhardt-Römermann M, Baeten L, Craven D, De Frenne P, Hédl R, Lenoir J, Bert D, Brunet J, Chudomelová M, Decocq G, Dierschke H, Dirnböck T, Dörfler I, Heinken T, Hermy M, Hommel P, Jarozewicz B, Keczyński A, Kelly DJ, Kirby K, Kopecký M, Macek M, Máliš F, Mirtl M, Mitchell FJG, Naaf T, Newman M, Peterken G, Petřík P, Schmidt W, Standovár T, Tóth Z, Van Calster H, Verstraeten G, Vladovič J, Vild O, Wulf M, Verheyen K (2015) Drivers of temporal changes in temperate forest plant diversity vary across spatial scales. Glob Change Biol 21:3726–3737
Brunet J, Valtinat K, Lajos Mayr M, Felton A, Lindbladh M, Bruun HH (2011) Understory succession in post-agricultural oak forests: habitat fragmentation affects forest specialists and generalists differently. For Ecol Manag 262:1863–1871
Brunet J, De Frenne P, Holmström E, Lajos Mayr M (2012) Life-history traits explain rapid colonization of young post-agricultural forests by understory herbs. For Ecol Manag 278:55–62
Butaye J, Jacquemyn H, Hermy M (2001) Differential colonization causing non-random forest plant community structure in a fragmented agricultural landscape. Ecography 24:369–380
Cronk Q (2016) Plant extinctions take time. Science 353:446–447
De Frenne P, Baeten L, Graae B, Brunet J, Wulf M, Orczewska A, Kolb A, Jansen I, Jamoneau A, Jacquemyn H, Hermy M, Diekmann M, De Schrijver A, De Sanctis M, Decocq G, Cousins SAO, Verheyen K (2011) Interregional variation in the floristic recovery of post-agricultural forests. J Ecol 99:600–609
De Schrijver A, Vesterdal L, Hansen K, De Frenne P, Augusto L, Achat DL, Staelens J, Baeten L, De Keersmaeker L, De Neve S, Verheyen K (2012) Four decades of post-agricultural forest development have caused major redistributions of soil phosphorous fractions, Oecologia 169: 221–234
Dullinger S, Gattringer A, Thuiller W, Moser D, Zimmermann NE, Guisan A, Willner W, Plutzar C, Leitner M, Mang T, Caccianiga M, Dirnboeck T, Ertl S, Fischer A, Lenoir J, Svenning J, Psomas A, Schmatz DR, Silc U, Vittoz P, Huelber K (2012) Extinction debt of high-mountain plants under twenty-first-century climate change. Nat Clim Chang 2:619–622
DWD (2014) http://www.dwd.de/bvbw/generator/DWDWWW/Content/Oeffentlichkeit/KU/KU2/KU21/klimadaten/german/nieder__8110__akt__html,templateId=raw, property=publicationFile.html/nieder_8110_akt_html.htm>andhttp://www.dwd.de/bvbw/generator/DWDWWW/Content/Oeffentlichkeit/KU/KU2/KU21/klimadaten/german/tmp__8110__akt__html,templateId=raw, property=publicationFile.html/temp_8110_akt_html.html>l. Accessed 27 May 2014
Dzwonko Z, Loster S (1992) Species richness and seed dispersal to secondary woods in southern Poland. J Biogeogr 19:195–204
Etienne D, Ruffaldi P, Dupouey JL, Georges-Leroy M, Ritz F, Dambrine E (2013) Searching for ancient forests: a 2000 year history of land use in northeastern French forests deduced from the pollen composition of closed depressions. Holocene 23:678–691
Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Glob Ecol Biogeogr 16:265–280
Flinn KM, Marks PL (2007) Agricultural legacies in forest environments: tree communities, soil properties, and light availability. Ecol Appl 17:452–463
Flinn KM, Vellend M (2005) Recovery of Forest Plant Communities in Post-Agricultural Landscapes. Front Ecol Environ 3:243–250
IUSS Working Group (2014) World reference base for soil resources 2014. International soil classification system for naming soils and creating legends for soil maps. World Soil Resources Reports No. 106. FAO, Rome
Hanski I (1994) A practical model of metapopulation dynamics. J Anim Ecol 63:151–162
Hanski I (2000) Extinction debt and species credit in boreal forests: modelling the consequences of different approaches to biodiversity conservation. Ann Zool Fennici 37:271–280
Helm A, Hanski I, Partel M (2006) Slow response of plant species richness to habitat loss and fragmentation. Ecol Lett 9:72–77
Heráult B, Honnay O (2005) The relative importance of local, regional and historical factors determining the distribution of plants in fragmented riverine forests: an emergent group approach. J Biogeogr 32:2069–2081
Hermy M, Verheyen K (2007) Legacies of the past in the present-day forest biodiversity: a review of past land-use effects on forest plant species composition and diversity. Ecol Res 22:361–371
Hermy M, Honnay O, Firbank L, Grashof-Bokdam C, Lawesson JE (1999) An ecological comparison between ancient and other forest plant species of Europe, and the implications for forest conservation. Biol Conserv 91:9–22
Honnay O, Degroote B, Hermy M (1998) Ancient-forest plants in Western Belgium: a species list and possible ecological mechanisms. Belgian Bot 130:139–154
IFS (1960) Ergebnisse der standortserkundung im staatlichen forstbetrieb perleberg (Erläuterung zu den Standartskarten). Institut für Forsteinrichtung und Standortserkundung, Schwerin
Jackson ST, Sax DF (2010) Balancing biodiversity in a changing environment: extinction debt, immigration credit and species turnover. Trends Ecol Evol 25:153–160
Jacquemyn H, Butaye J, Hermy M (2001) Forest plant species richness in small, fragmented mixed deciduous forest patches: the role of area, time and dispersal limitation. J Biogeogr 28:801–812
Jacquemyn H, Butaye J, Hermy M (2003) Impacts of restored patch density and distance from natural forests on colonization success. Restor Ecol 11:417–423
Kaplan JO, Krumhardt KM, Zimmermann N (2009) The prehistoric and preindustrial deforestation of Europe. Quat Sci Rev 28:3016–3034
Keith SA, Newton AC, Morecroft MD, Bealey CE, Bullock JM (2009) Taxonomic homogenization of woodland plant communities over 70 years. Proc R Soc B 276:3539–3544
Kokarēviča I, Brumelis G, Kasparinskis R, Rolava A, Nikodemus O, Grods J, Elfert D (2016) Vegetation changes in boreo-nemoral forest stands depending on soil factors and past land use during an 80 year period of no human impact. Can J For Res 46:376–386
Kolk J, Naaf T (2015) Herb-layer extinction debt in highly fragmented temperate deciduous forests—completely paid after 160 years? Biol Conserv 182:164–172
Kuussaari M, Bommarco R, Heikkinen RK, Helm A, Krauss J, Lindborg R, Öckinger E, Pärtel M, Pino J, Rodà F, Stefanescu C, Teder T, Zobel M, Steffan-Dewenter I (2009) Extinction debt: a challenge for biodiversity conservation. TREE 24:564–571
LBGR (2007) Landesamt für bergbau, geologie und rohstoffe (LBGR) Brandenburg bodenübersichtskarte des landes Brandenburg 1: 300,000 (BÜK300). LBGR, Kleinmachnow
Lepš J, Hadincová V (1992) How reliable are our vegetation analysis? J Veg Sci 3:119–124
LGBR (2008) Landesamt für bergbau, geologie und rohstoffe (LBGR) Brandenburg, landkreis prignitz, geologische übersichtskarte 1:100,000. LBGR, Brandenburg
LGBR (2009) Landesamt für bergbau, geologie und rohstoffe (LBGR) Brandenburg, landkreis ostprignitz-ruppin, geologische übersichtskarte 1:100,000. LBGR, Brandenburg
Lindborg R, Eriksson O (2004) Historical landscape connectivity affects present plant species diversity. Ecology 85:1840–1845
Ling KA (2003) Using environmental and growth characteristics of plants to detect long-term changes in response to atmospheric pollution: some examples from British beechwoods. Sci Total Environ 310:203–210
Manly BFJ (2007) Randomization, bootstrap and monte carlo methods in biology, 3rd edn. Chapman & Hall, London
Matlack GR (1994) Plant species migration in a mixed-history forest landscape in eastern North America. Ecology 75:1491–1502
McCollin D, Jackson JI, Bunce RGH, Barr CJ, Stuart R (2000) Hedgerows as habitat for woodland plants. J Environ Manag 60:77–90
Moilanen A, Nieminen M (2002) Simple connectivity measures in spatial ecology. Ecology 83:1131–1145
Naaf T, Kolk J (2015) Colonization credit of post-agricultural forest patches in NE Germany remains 130–230 years after reforestation. Biol Conserv 182:155–163
Naaf T, Kolk J (2016) Initial site conditions and interactions between multiple drivers determine herb-layer changes over five decades in temperate forests. Forest Ecol Manag 366:153–165
Orczewska A (2009) The impact of former agriculture on habitat conditions and distribution patterns of ancient woodland plant species in recent black alder (Alnus glutinosa (L.) Gaertn.) woods in south-western Poland. Forest Ecol Manag 258:794–803
Paltto H, Norden B, Gotmark F, Franc N (2006) At which spatial and temporal scales does landscape context affect local density of red data book and indicator species? Biol Conserv 133:442–454
Perring MP, De Frenne P, Baeten L, Maes SL, Depauw L, Blondeel H, Caron MM, Verheyen K (2016) Global environmental change effects on ecosystems: the importance of land-use legacies. Glob Chang Biol 22:1361–1371
Peterken GF, Game M (1984) Historical factors affecting the number and distribution of vascular plant-species in the woodlands of central Lincolnshire. J Ecol 72:155–182
Petit S, Griffith L, Smart SS, Smith GM, Stuart RC, Wright SM (2004) Effects of area and isolation of woodland patches on herbaceous plant species richness across Great Britain. Landscape Ecol 19:463–471
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2015) nlme: linear and nonlinear mixed effect models. R package version 3.1–122, http://CRAN.R-project.org/package=nlme
R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/
Rogers DA, Rooney TP, Hawbaker TJ, Radeloff VC, Waller DM (2009) Paying the extinction debt in southern wisconsin forest understories. Conserv Biol 23:1497–1506
Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Biodiversity – global biodiversity scenarios for the year 2100. Science 287:1770–1774
Schmidt M, Kriebitzsch WU, Ewald J (2011) Waldartenlisten der Farn- und Blütenpflanzen, Moose und Flechten Deutschlands. BfN-Skripten 299:1–111
Singleton R, Gardescu S, Marks PL, Geber MA (2001) Forest herb colonization of post-agricultural forests in central New York State, USA. J Ecol 89:325–338
Svenning JC, Baktoft KH, Balslev H (2009) Land-use history affects understory plant species distributions in a large temperate-forest complex, Denmark. Plant Ecol 201:221–234
Thomaes A, De Keersmaeker L, Van Calster H, De Schrijver A, Vandekerkhove K, Verstraeten G, Verheyen K (2012) Diverging effects of two contrasting tree species on soil and herb layer development in a chronosequence of post-agricultural forest. Forest Ecol Manag 278:90–100
Tilman D, May RM, Lehman CL, Nowak MA (1994) Habitat destruction and the extinction debt. Nature 371:65–66
Vellend M (2003) Habitat loss inhibits recovery of plant diversity as forests regrow. Ecology 84:1158–1164
Vellend M, Verheyen K, Jacquemyn H, Kolb A, van Calster H, Peterken G, Hermy M (2006) Extinction debt of forest plants persists for more than a century following habitat fragmentation. Ecology 87:542–548
Verheyen K, Guntenspergen G, Biesbrouck B, Hermy M (2003) An integrated analysis oft he effects of past land-use on forest plant species colonization at the landscape scale. J Ecol 91:731–742
Verheyen K, Baeten L, De Frenne P, Bernhardt-Römermann M, Brunet J, Cornelis J, Decocq G, Dierschke H, Eriksson O, Hédl R, Heinken T, Hermy M, Hommel P, Kirby K, Naaf T, Peterken G, Petřík P, Pfadenhauer J, Van Calster H, Walther GR, Wulf M, Verstraeten G (2012) Driving factors behind the eutrophication signal in understorey plant communities of deciduous temperate forests. J Ecol 100:352–365
Vockenhuber EA, Scherber C, Langenbruch C, Meißner M, Seidel D, Tscharntke T (2011) Tree diversity and environmental context predict herb species richness and cover in Germany’s largest connected deciduous forest. Perspect Plant Ecol Evol Syst 13:111–119
Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to climate change. Nature 416:389–395
Williams M (2000) Dark ages and dark areas: global deforestation in the deep past. J Hist Geogr 26:28–46
Wulf M (1997) Plant species as indicators of ancient woodland in northwestern Germany. J Veg Sci 8:635–642
Wulf M (2004) Auswirkungen des Landschaftswandels auf die Verbreitungsmuster von Waldpflanzen - Konsequenzen für den Naturschutz. Dissertationes Botanicae 392, J. Cramer Berlin, Stuttgart, Germany
Wulf M, Kolk J (2014) Plant species richness of very small forests related to patch configuration, quality, heterogeneity and history. J Veg Sci 25:1267–1277
Wulf M, Rujner H (2011) A GIS-based method for the reconstruction of the late eighteenth century forest vegetation in the Prignitz region (NE Germany). Landsc Ecol 26:153–168
Acknowledgements
This research was funded by the German Research Foundation (research grant NA 1067/1-1) and supported by the German Federal Ministry of Food, Agriculture and Consumer Protection (BMELV) and the Ministry for Science, Research and Culture of the State of Brandenburg, Germany (MWFK). We thank the regional forest authorities (Landeskompetenzzentrum Forst Eberswalde, LFE) for providing us the access to their archives from which we obtained the original site investigation record sheets. We further thank U. Jahn for her help in preparing the soil samples.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Daniel Sanchez Mata.
This article belongs to the Topical Collection: Forest and plantation biodiversity.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kolk, J., Naaf, T. & Wulf, M. Paying the colonization credit: converging plant species richness in ancient and post-agricultural forests in NE Germany over five decades. Biodivers Conserv 26, 735–755 (2017). https://doi.org/10.1007/s10531-016-1271-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-016-1271-y