Abstract
Land use change is one of the main drivers of species extinction. In Europe, grasslands are under active conflict between conservation efforts and increasing agricultural pressures. Here, we examine the demographic effects of differential land use on the herbaceous perennial Trollius europaeus L. (Ranunculaceae), a bioindicator of species-richness and ecosystem services in wet grasslands of Central Europe. Demographic data were collected in 2006–2009 from nine populations in seven protected sites of northeastern Germany representing four land use types. We constructed stage-based matrix population models to explore the effects of various land management on demographic viability of focal populations. We show that most studied populations are declining (λ < 1), although the estimates of local extinction vary between ≤15 years for grazed and woodland populations, and 20–99 years for mown and abandoned populations. The joint information from our elasticity analyses and life table response experiments revealed that reproduction, growth of small vegetative individuals and survival of reproductive stages are most important for population viability. Our study shows that the current land uses in protected areas where T. europaeus is found is incompatible with its long-term viability. We suggest that, when compatible with in situ practices, grasslands containing this species be mown after maturity in order to enhance seedling recruitment and to reduce competition for juveniles. Prolonged extinction times in abandoned populations offer a buffer to develop conservation schemes there. An improvement of conservation measures is urgently needed to maintain the populations of this important bioindicator and its associated community of moist species-rich fen grasslands.
Similar content being viewed by others
References
Alvarez-Buylla ER, Slatkin M (1993) Finding confidence limits on population growth rates: Monte Carlo test of a simple analytic method. Oikos 68:273–282
Bartz R-P, Bolbrinker P, Funk B, Wollert H (1984) Zum Rückgang der Trollblume (Trollius europaeus L.) im Kreis Teterow im Zeitraum von 1972 bis 1983. Naturschutzarbeit Mecklenburg 27:39–41 (in German)
Bignal EM, McCracken DI (1996) Low intensity farming systems in the conservation of the countryside. J Appl Ecol 33:413–424
Bratteler M, Widmer A (1998) Untersuchungen zur Trollius-Chiastocheta-Interaktion in kleinen, isolierten Pflanzenpopulationen. Bull Geobot Inst ETH 64:69–76 (in German with English abstract)
Bruchmann I, Hobohm C (2010) Halting the loss of biodiversity: endemic vascular plants in grasslands of Europe. In: Schnyder H, Isselstein J, Taube F, Auerswald K, Schellberg J, Wachendorf M, Herrmann A, Gierus M, Wrage N, Hopkins A (eds) Grassland in a changing world. Proceedings of the 23rd General Meeting of the European Grassland Federation. Mecke, Duderstadt, pp 776–778
Brys R, Jacquemyn H, Endels P, de Blust G, Hermy M (2004) The effects of grassland management on plant performance and demography in the perennial herb Primula veris. J Appl Ecol 41:1080–1091
Caswell H (2000) Prospective and retrospective perturbation analysis: their roles in conservation biology. Ecology 81:619–627
Caswell H (2001) Matrix population models: construction, analysis, and interpretation. Sinauer Associates, Sunderland
Chapin FS III, Bloom AJ, Field CB, Waring RH (1987) Plant responses to multiple environmental factors. Bioscience 37:49–57
Chapin FS III, Schulze ED, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21:423–447
Ciosek MT, Krechowski J, Piórek K (2013) Globe flower Trollius europaeus L. in forest and forest edge communities of the northern part of Południowopodlaska Lowland. Forest Res Pap 74:233–243
Colling G, Matthies D (2006) Effects of habitat deterioration on population dynamics and extinction risk of an endangered, long-lived perennial herb (Scorzonera humilis). J Ecol 94:959–972
Council of the European Communities (1992) Council Directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora. Off J Eur Communities Ser L 206:7–50
de Kroon H, Plaisier A, van Groenendael J, Caswell H (1986) Elasticity: the relative contribution of demographic parameters to population growth rate. Ecology 67:1427–1431
de Kroon H, van Groenendael J, Ehrlén J (2000) Elasticities: a review of methods and model limitations. Ecology 81:607–618
Dierschke H, Briemle G (2002) Kulturgrasland: Wiesen, Weiden und verwandte Staudenfluren. Ulmer, Stuttgart (in German)
Dierssen K (1996) Vegetation Nordeuropas. Ulmer, Stuttgart (in German)
Efron B (1982) The jackknife, the bootstrap and other resampling plans. Society for Industrial and Applied Mathematics, Philadelphia
Ehrlén J (1995) Demography of the perennial legume, Lathyrus vernus. II. Herbivory and population dynamics. J Ecol 83:297–308
Ehrlén J, Lehtilä K (2002) How perennial are perennial plants? Oikos 98:308–322
Ehrlén J, van Groenendael J (1998) Direct perturbation analysis for better conservation. Conserv Biol 12:470–474
Ehrlén J, Syrjänen K, Leimu R, García MB, Lehtilä K (2005) Land use and population growth of Primula veris: an experimental demographic approach. J Appl Ecol 42:317–326
Ellenberg H (1996) Vegetation Mitteleuropas mit den Alpen in ökologischer, dynamischer und historischer Sicht. Ulmer, Stuttgart (in German)
Endels P, Jacquemyn H, Brys R, Hermy M (2007) Reinstatement of traditional mowing regimes counteracts population senescence in the rare perennial Primula vulgaris. Appl Veg Sci 10:351–360
European Commission (2013) Eurostat database: land cover overview. http://appsso.eurostat.ec.europa.eu/nui/submitViewTableAction.do. Last accessed on 06 October 2014
Franco M, Silvertown J (2004) A Comparative demography of plants based upon elasticities of vital rates. Ecology 85:531–538
García MB, Picó FX, Ehrlén J (2008) Life span correlates with population dynamics in perennial herbaceous plants. Am J Bot 95:258–262
Gatsuk LE, Smirnova OV, Zaugolnova LI, Zhukoca LA (1980) Age states of plants of various growth forms: a review. J Ecol 68:675–696
Güthler W, Oppermann R (2005) Agrarumweltprogramme und Vertragsnaturschutz weiter entwickeln. Mit der Landwirtschaft zu mehr Natur. Ergebnisse des F+E-Projektes „Angebotsnaturschutz“. Naturschutz und Biologische Vielfalt 13, Bundesamt für Naturschutz (BfN), Bonn-Bad Godesberg (in German)
Hegi G (1965) Illustrierte Flora von Mitteleuropa, band III/3. Carl Hanser, Munich (in German)
Heiland S (1999) Voraussetzungen erfolgreichen Naturschutzes: Individuelle und gesellschaftliche Bedingungen umweltgerechten Verhaltens, ihre Bedeutung für den Naturschutz und die Durchsetzbarkeit seiner Ziele. Schriftenreihe Angewandter Umweltschutz. Ecomed, Landsberg (in German)
Hitchmough JD (2003) Effects of sword height, gap size, and slug grazing on emergence and establishment of Trollius europaeus (Globeflower). Restor Ecol 11:20–28
Horvitz CC, Schemske DW (1995) Spatiotemporal variation in demographic transitions of a tropical understory herb: projection matrix analysis. Ecol Monogr 65:155–192
Isselstein J, Jeangros B, Pavlu V (2005) Agronomic aspects of biodiversity targeted management of temperate grasslands in Europe—a review. Agron Res 3:139–151
Jacquemyn H, Brys R, Jongejans E (2010a) Seed limitation restricts population growth in shaded populations of a perennial woodland orchid. Ecology 91:119–129
Jacquemyn H, Brys R, Jongejans E (2010b) Size-dependent flowering and costs of reproduction affect population dynamics in a tuberous perennial woodland orchid. J Ecol 98:1204–1215
Jacquemyn H, Brys R, Davison R, Tuljapurkar S, Jongejans E (2011) Stochastic LTRE analysis of the effects of herbivory on the population dynamics of a perennial grassland herb. Oikos 121:211–218
Jensen K, Schrautzer J (1999) Consequences of abandonment for a regional fen flora and mechanisms of successional change. Appl Veg Sci 2:79–88
Jongejans E, de Kroon H (2005) Space versus time variation in the population dynamics of three co-occurring perennial herbs. J Ecol 93:681–692
Joyce CB, Wade PM (eds) (1998) European wet grasslands: biodiversity, management and restoration. Wiley, Chichester
Kaye TN, Pyke DA (2003) The effect of stochastic technique on estimates of population viability from transition matrix models. Ecology 84:1464–1476
Kostrakiewicz-Gierałt K (2012) The impact of neighbourhood and gap character on seedling recruitment of Trollius europaeus L. and Iris sibirica L. in Molinetum caerulae meadows. Biodivers Res Conserv 28:37–44
Kotowski W, van Diggelen R (2004) Light as an environmental filter in fen vegetation. J Veg Sci 15:583–594
Lehtilä K, Syrjänen K, Leimu R, García MB, Ehrlén J (2006) Habitat change and demography of Primula veris: identification of management targets. Conserv Biol 20:833–843
Lemke T, Porembski S (2013) Variation in the reproductive performance of the Trollius-Chiastocheta mutualism at the edge of its range in north-east Germany. Oecologia 172:437–447
Lemke T, Janßen A, Porembski S (2015) Multiple limitations to the persistence of Trollius europaeus in a fragmented agricultural landscape in the context of metapopulation theory. Plant Ecol 216:319–330
Lennartsson T, Oostermeijer JGB (2001) Demographic variation and population viability in Gentianella campestris: effects of grassland management and environmental stochasticity. J Ecol 89:451–463
Lindborg R, Ehrlén J (2002) Evaluating the extinction risk of a perennial herb: demographic data versus historical records. Conserv Biol 16:683–690
Lucas RW, Forseth IN, Casper BB (2008) Using rainout shelters to evaluate climate change effects on the demography of Cryptantha flava. J Ecol 96:514–522
Maschinski J, Frye R, Rutman S (1997) Demography and population viability of an endangered plant species before and after protection from trampling. Conserv Biol 11:990–999
Menges ES (2000) Population viability analyses in plants: challenges and opportunities. Trends Ecol Evol 15:51–56
Menges ES, Dolan RW (1998) Demographic viability of populations of Silene regia in midwestern prairies: relationships with fire management, genetic variation, geographic location, population size and isolation. J Ecol 86:63–78
Milberg P (1994) Germination ecology of the polycarpic grassland perennials Primula veris and Trollius europaeus. Ecography 17:3–8
Morris WF, Doak DF (2002) Quantitative conservation biology: theory and practice of population viability analysis. Sinauer Associates, Sunderland
Moser DM, Gygax A, Bäumler B, Wyler N, Palese R (2002) Rote Liste der gefährdeten Arten der Schweiz. Farn- und Blütenpflanzen. BUWAL, Bern (in German)
Neubert MG, Caswell H (2000) Demography and dispersal: calculation and sensitivity analysis of invasion speed for structured populations. Ecology 81:1613–1628
Oesterheld M, Sala OE (1990) Effects of grazing on seedlings establishment: the role of seed and safe-site availability. J Veg Sci 1:353–358
Oostermeijer JGB, Van’t Veer R, Den Nijs JCM (1994) Population structure of the rare, long-lived perennial Gentiana pneumonanthe in relation to vegetation and management in the Netherlands. J Appl Ecol 31:428–438
Oostermeijer JGB, Luijten SH, den Nijs JCM (2003) Integrating demographic and genetic approaches in plant conservation. Biol Conserv 113:389–398
R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Sala OE, Paruelo JM (1997) Ecosystem services in grasslands. In: Daily G (ed) Nature’s services: societal dependence on natural ecosystems. Island Press, Washington, DC, pp 237–252
Silvertown JW, Lovett-Doust J (1993) Introduction into plant population biology. Blackwell, Oxford
Silvertown J, Franco M, Pisanty I, Mendoza A (1993) Comparative plant demography—relative importance of life-cycle components to the finite rate of increase in woody and herbaceous perennials. J Ecol 81:465–476
Silvertown J, Franco M, Menges ES (1996) Interpretation of elasticity matrices as an aid to the management of plant populations for conservation. Conserv Biol 10:591–597
Stammel B, Kiehl K (2004) Do hoof prints actually serve as a regeneration niche for plant species in fens? Phytocoenologia 34:271–286
Stott I, Townley S, Carslake D, Hodgson DJ (2010) On reducibility and ergodicity of population projection matrix models. Methods Ecol Evol 1:242–252
Stott I, Hodgson DJ, Townley S (2012) popdemo: an R package for population demography using projection matrix analysis. Methods Ecol Evol 3:797–802
Stubben C, Milligan B (2007) Estimating and analyzing demographic models using the popbio package in R. J Stat Softw 22:1–23
Tamm A, Kull K, Sammul M (2002) Classifying clonal growth forms based on vegetative mobility and ramet longevity: a whole community analysis. Evol Ecol 15:383–401
Taylor BL, Dizon AE (1999) First policy then science: why a management unit based solely on genetic criteria cannot work. Mol Ecol 8:S11–S16
Tuljapurkar S (1990) Population dynamics in variable environments. Springer, New York
Tuljapurkar S (1997) Stochastic matrix models. In: Tuljapurkar S, Caswell H (eds) Structured population models in marine, terrestrial and freshwater ecosystems. Chapman and Hall, New York, pp 59–82
van der Meer S, Dahlgren JP, Mildén M, Ehrlén J (2014) Differential effects of abandonment on the demography of the grassland perennial Succisa pratensis. Popul Ecol 56:151–160
van Diggelen R, Middleton B, Bakker J, Grootjans A, Wassen M (2006) Fens and floodplains of the temperate zone: present status, threats, conservation and restoration. Appl Veg Sci 9:157–162
Voigtländer U, Henker H (2005) Rote Liste der gefährdeten Höheren Pflanzen Mecklenburg-Vorpommerns. Umweltministerium Mecklenburg-Vorpommern (ed), Schwerin (in German)
Acknowledgments
T. L. thanks S. Porembski and the Department of Botany at the University of Rostock as well as M. Schnittler (University of Greifswald) for logistic support, I. Huismann, K. Nickschick and D. Riebold for help during fieldwork, and R. Kinzelbach (University of Rostock) for the determination of the bug larvae. R. S.-G. acknowledges financial support from the Max Planck Institute for Demographic Research and the Australian Research Council DECRA fellowship DE140100505.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lemke, T., Salguero-Gómez, R. Land use heterogeneity causes variation in demographic viability of a bioindicator of species-richness in protected fen grasslands. Popul Ecol 58, 165–178 (2016). https://doi.org/10.1007/s10144-015-0519-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10144-015-0519-9