Skip to main content
Log in

Land use heterogeneity causes variation in demographic viability of a bioindicator of species-richness in protected fen grasslands

  • Original article
  • Published:
Population Ecology

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

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

    Article  Google Scholar 

  • 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)

    Google Scholar 

  • Bignal EM, McCracken DI (1996) Low intensity farming systems in the conservation of the countryside. J Appl Ecol 33:413–424

    Article  Google Scholar 

  • 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)

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Caswell H (2000) Prospective and retrospective perturbation analysis: their roles in conservation biology. Ecology 81:619–627

    Article  Google Scholar 

  • Caswell H (2001) Matrix population models: construction, analysis, and interpretation. Sinauer Associates, Sunderland

    Google Scholar 

  • Chapin FS III, Bloom AJ, Field CB, Waring RH (1987) Plant responses to multiple environmental factors. Bioscience 37:49–57

    Article  Google Scholar 

  • Chapin FS III, Schulze ED, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21:423–447

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • de Kroon H, van Groenendael J, Ehrlén J (2000) Elasticities: a review of methods and model limitations. Ecology 81:607–618

    Article  Google Scholar 

  • Dierschke H, Briemle G (2002) Kulturgrasland: Wiesen, Weiden und verwandte Staudenfluren. Ulmer, Stuttgart (in German)

    Google Scholar 

  • Dierssen K (1996) Vegetation Nordeuropas. Ulmer, Stuttgart (in German)

    Google Scholar 

  • Efron B (1982) The jackknife, the bootstrap and other resampling plans. Society for Industrial and Applied Mathematics, Philadelphia

    Book  Google Scholar 

  • Ehrlén J (1995) Demography of the perennial legume, Lathyrus vernus. II. Herbivory and population dynamics. J Ecol 83:297–308

    Article  Google Scholar 

  • Ehrlén J, Lehtilä K (2002) How perennial are perennial plants? Oikos 98:308–322

    Article  Google Scholar 

  • Ehrlén J, van Groenendael J (1998) Direct perturbation analysis for better conservation. Conserv Biol 12:470–474

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Ellenberg H (1996) Vegetation Mitteleuropas mit den Alpen in ökologischer, dynamischer und historischer Sicht. Ulmer, Stuttgart (in German)

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • García MB, Picó FX, Ehrlén J (2008) Life span correlates with population dynamics in perennial herbaceous plants. Am J Bot 95:258–262

    Article  PubMed  Google Scholar 

  • Gatsuk LE, Smirnova OV, Zaugolnova LI, Zhukoca LA (1980) Age states of plants of various growth forms: a review. J Ecol 68:675–696

    Article  Google Scholar 

  • 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)

    Google Scholar 

  • 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)

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Horvitz CC, Schemske DW (1995) Spatiotemporal variation in demographic transitions of a tropical understory herb: projection matrix analysis. Ecol Monogr 65:155–192

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Jacquemyn H, Brys R, Jongejans E (2010a) Seed limitation restricts population growth in shaded populations of a perennial woodland orchid. Ecology 91:119–129

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Jensen K, Schrautzer J (1999) Consequences of abandonment for a regional fen flora and mechanisms of successional change. Appl Veg Sci 2:79–88

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Joyce CB, Wade PM (eds) (1998) European wet grasslands: biodiversity, management and restoration. Wiley, Chichester

    Google Scholar 

  • Kaye TN, Pyke DA (2003) The effect of stochastic technique on estimates of population viability from transition matrix models. Ecology 84:1464–1476

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Kotowski W, van Diggelen R (2004) Light as an environmental filter in fen vegetation. J Veg Sci 15:583–594

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lindborg R, Ehrlén J (2002) Evaluating the extinction risk of a perennial herb: demographic data versus historical records. Conserv Biol 16:683–690

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Menges ES (2000) Population viability analyses in plants: challenges and opportunities. Trends Ecol Evol 15:51–56

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Milberg P (1994) Germination ecology of the polycarpic grassland perennials Primula veris and Trollius europaeus. Ecography 17:3–8

    Article  Google Scholar 

  • Morris WF, Doak DF (2002) Quantitative conservation biology: theory and practice of population viability analysis. Sinauer Associates, Sunderland

    Google Scholar 

  • 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)

    Google Scholar 

  • Neubert MG, Caswell H (2000) Demography and dispersal: calculation and sensitivity analysis of invasion speed for structured populations. Ecology 81:1613–1628

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Oostermeijer JGB, Luijten SH, den Nijs JCM (2003) Integrating demographic and genetic approaches in plant conservation. Biol Conserv 113:389–398

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Silvertown JW, Lovett-Doust J (1993) Introduction into plant population biology. Blackwell, Oxford

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Stammel B, Kiehl K (2004) Do hoof prints actually serve as a regeneration niche for plant species in fens? Phytocoenologia 34:271–286

    Article  Google Scholar 

  • Stott I, Townley S, Carslake D, Hodgson DJ (2010) On reducibility and ergodicity of population projection matrix models. Methods Ecol Evol 1:242–252

    Google Scholar 

  • Stott I, Hodgson DJ, Townley S (2012) popdemo: an R package for population demography using projection matrix analysis. Methods Ecol Evol 3:797–802

    Article  Google Scholar 

  • Stubben C, Milligan B (2007) Estimating and analyzing demographic models using the popbio package in R. J Stat Softw 22:1–23

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Tuljapurkar S (1990) Population dynamics in variable environments. Springer, New York

    Book  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Voigtländer U, Henker H (2005) Rote Liste der gefährdeten Höheren Pflanzen Mecklenburg-Vorpommerns. Umweltministerium Mecklenburg-Vorpommern (ed), Schwerin (in German)

Download references

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

Authors

Corresponding author

Correspondence to Tristan Lemke.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 1108 kb)

Supplementary material 2 (XLS 258 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10144-015-0519-9

Keywords

Navigation