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Extinction debt in a common grassland species: immediate and delayed responses of plant and population fitness

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Abstract

Changes in landscape structure and environmental conditions due to habitat fragmentation can have significant effects on plant populations. Decreasing genetic diversity and changing population structure can reduce plant fitness and influence the long-term persistence of populations. Dry calcareous grasslands in Estonia have witnessed a large decline in area within the last 80 years, but due to extinction debt, the species richness in these grasslands has not yet responded to this decline. In these calcareous grasslands, we studied genetic diversity, phenotypic performance and population characteristics of a common habitat-specialist grass, Briza media. A decrease in genetic diversity was associated with a decrease in plant reproductive output. In addition, we found that some fitness components of B. media showed a delayed response to landscape changes. Specifically, plant height and germination success were related to historical rather than to current landscape parameters, indicating a time-lagged response of plant performance to habitat fragmentation. Dependence on historical landscape structure may thus result in a future decline in population fitness even if habitat loss and fragmentation no longer continue. The documented effect of current environmental conditions, however, shows that fitness-related traits are already slowly adapting to the changing conditions. Our results indicate that even common habitat-specialist species can be susceptible to landscape changes and be threatened by decreased population performance in the future.

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References

  • Aavik T, Jõgar Ü, Liira J, Tulva I, Zobel M (2008) Plant diversity in a calcareous wooded meadow—The significance of management continuity. J Veg Sci 19:475–484

    Article  Google Scholar 

  • Adriaens D, Honnay O, Hermy M (2006) No evidence of a plant extinction debt in highly fragmented calcareous grasslands in Belgium. Biol Conserv 133:212–224

    Article  Google Scholar 

  • Adriaens D, Jacquemyn H, Honnay O, Hermy M (2009) Conservation of remnant populations of Colchicum autumnale—The relative importance of local habitat quality and habitat fragmentation. Acta Oecol 35:69–82

    Article  Google Scholar 

  • Aguilar R, Quesada M, Ashworth L, Herrerias-Diego Y, Lobo J (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol Ecol 17:5177–5188

    Article  PubMed  Google Scholar 

  • Aizen MA, Harder LD (2007) Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88:271–281

    Article  PubMed  Google Scholar 

  • Balmford A, Bennun L, ten Brink B, Cooper D, Côté IM, Crane P, Dobson A, Dudley N, Dutton I, Green RE, Gregory RD, Harrison J, Kennedy ET, Kremen C, Leader-Williams N, Lovejoy TE, Mace G, May R, Mayaux P, Morling P, Phillips J, Redford K, Ricketts TH, Rodríguez JP, Sanjayan M, Schei PJ, van Jaarsveld AS, Walther BA (2005) The convention on biological diversity’s 2010 target. Science 307:212–213

    Article  PubMed  CAS  Google Scholar 

  • Brückmann SV, Krauss J, Steffan-Dewenter I (2010) Butterfly and plant specialists suffer from reduced connectivity in fragmented landscapes. J Appl Ecol 47:799–809

    Article  Google Scholar 

  • Bruun HH, Fritzbøger B (2002) The past impact of livestock husbandry on dispersal of plant seeds in the landscape of Denmark. Ambio 31:425–431

    PubMed  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Ceulemans T, Merckx R, Hens M, Honnay O (2011) A trait-based analysis of the role of phosphorus versus nitrogen enrichment in plant species loss across North-west European grasslands. J Appl Ecol 48:1155–1163

    Article  CAS  Google Scholar 

  • Cheptou P-O, Carrue O, Rouifed S, Cantarel A (2008) Rapid evolution of seed dispersal in an urban environment in the weed Crepis sancta. Proc Natl Acad Sci 105:3796–3799

    Article  PubMed  CAS  Google Scholar 

  • Cousins SAO, Ohlson H, Eriksson O (2007) Effects of historical and present fragmentation on plant species diversity in semi-natural grasslands in Swedish rural landscapes. Landscape Ecol 22:723–730

    Article  Google Scholar 

  • de Vere N, Jongejans E, Plowman A, Williams E (2009) Population size and habitat quality affect genetic diversity and fitness in the clonal herb Cirsium dissectum. Oecologia 159:59–68

    Article  PubMed  Google Scholar 

  • Dirzo R, Raven PH (2003) Global state of biodiversity and loss. Annu Rev Environ Resour 28:137–167

    Article  Google Scholar 

  • Dixon JM (2002) Briza media L. J Ecol 90:737–752

    Article  Google Scholar 

  • Ewers RM, Didham RK (2006) Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev 81:117–142

    Article  PubMed  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515

    Article  Google Scholar 

  • Fischer M, Stöcklin J (1997) Local extinctions of plants in remnants of extensively used calcareous grasslands 1950–1985. Conserv Biol 11:727–737

    Article  Google Scholar 

  • Fischer SF, Poschlod P, Burkhard B (1996) Experimental studies on the dispersal of plants and animals on sheep in calcareous grasslands. J Appl Ecol 33:1206–1222

    Article  Google Scholar 

  • Frankham R, Ballou J, Briscoe D (2009) Introduction to conservation genetics, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Helm A, Hanski I, Pärtel M (2006) Slow response of plant species richness to habitat loss and fragmentation. Ecol Lett 9:72–77

    PubMed  Google Scholar 

  • Helm A, Oja T, Saar L, Takkis K, Talve T, Pärtel M (2009) Human influence lowers plant genetic diversity in communities with extinction debt. J Ecol 97:1329–1336

    Article  Google Scholar 

  • Jacquemyn H, Brys R, Hermy M (2002) Patch occupancy, population size and reproductive success of a forest herb (Primula elatior) in a fragmented landscape. Oecologia 130:617–625

    Article  Google Scholar 

  • Jänes-Kapp K, Randma E, Soosaar M (eds) (2007) Saaremaa 2. Ajalugu, majandus, kultuur. Koolibri, Tallinn, Estonia

  • Kolb A, Dahlgren JP, Ehrlén J (2010) Population size affects vital rates but not population growth rate of a perennial plant. Ecology 91:3210–3217

    Article  PubMed  Google Scholar 

  • Krauss J, Bommarco R, Guardiola M, Heikkinen RK, Helm A, Kuussaari M, Lindborg R, Öckinger E, Pärtel M, Pino J, Pöyry J, Raatikainen KM, Sang A, Stefanescu C, Teder T, Zobel M, Steffan-Dewenter I (2010) Habitat fragmentation causes immediate and time-delayed biodiversity loss at different trophic levels. Ecol Lett 13:597–605

    Article  PubMed  Google Scholar 

  • 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. Trends Ecol Evol 24:564–571

    Article  PubMed  Google Scholar 

  • Laasimer L (1965) Eesti NSV taimkate. Valgus, Tallinn

    Google Scholar 

  • Legendre P (2008) Studying beta diversity: ecological variation partitioning by multiple regression and canonical analysis. J Plant Ecol 1:3–8

    Article  Google Scholar 

  • Leimu R, Mutikainen P, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size, fitness and genetic variation? J Ecol 94:942–952

    Article  Google Scholar 

  • Lienert J (2004) Habitat fragmentation effects on fitness of plant populations—a review. J Nat Conserv 12:53–72

    Article  Google Scholar 

  • Lienert J, Fischer M, Schneller J, Diemer M (2002) Isozyme variability of the wetland specialist Swetia perennis (Gentianaceae) in relation to habitat size, isolation, and plant fitness. Am J Bot 89:801–811

    Article  PubMed  CAS  Google Scholar 

  • Lindborg R, Helm A, Bommarco R, Heikkinen RK, Kühn I, Pykälä J, Pärtel M (2012) Effect of habitat area and isolation on plant trait distribution in European forests and grasslands. Ecography 35:356–363

    Article  Google Scholar 

  • Luijten SH, Dierick A, Gerard J, Oostermeijer B, Raijmann LEL, Den Nijs HCM (2000) Population size, genetic variation, and reproductive success in a rapidly declining, self-incompatible perennial (Arnica montana) in The Netherlands. Conserv Biol 14:1776–1787

    Article  Google Scholar 

  • Luque S, Saura S, Fortin M-J (2012) Landscape connectivity analysis for conservation: insights from combining new methods with ecological and genetic data. Landscape Ecol 27:153–157

    Article  Google Scholar 

  • Moilanen A, Nieminen M (2002) Simple connectivity measures in spatial ecology. Ecology 83:1131–1145

    Article  Google Scholar 

  • Murray BG (1974) Breeding systems and floral biology in the genus Briza. Heredity 33:285–292

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2011) vegan: community ecology package. R package version 2.0-1

  • Oostermeijer JGB, Luijten SH, Křenová ZV, Den Nijs HCM (1998) Relationships between population and habitat characteristics and reproduction of the rare Gentiana pneumonanthe L. Conserv Biol 12:1042–1053

    Article  Google Scholar 

  • Ouborg NJ, Vergeer P, Mix C (2006) The rough edges of the conservation genetics paradigm for plants. J Ecol 94:1233–1248

    Article  Google Scholar 

  • Pärtel M, Kalamees R, Zobel M, Rosén E (1999) Alvar grasslands in Estonia: variation in species composition and community structure. J Veg Sci 10:561–570

    Article  Google Scholar 

  • Pärtel M, Bruun HH, Sammul M (2005) Biodiversity in temperate European grasslands: origin and conservation. In: Lillak R, Viiralt R, Linke A, Geherman V (eds) Integrating efficient grassland farming and biodiversity. Estonian Grassland Society, Tartu, pp 1–14

    Google Scholar 

  • Pärtel M, Helm A, Reitalu T, Liira J, Zobel M (2007) Grassland diversity related to the Late Iron Age human population density. J Ecol 95:574–582

    Article  Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

  • Poschlod P, WallisDeVries MF (2002) The historical and socioeconomic perspective of calcareous grasslands—lessons from the distant and recent past. Biol Conserv 104:361–376

    Article  Google Scholar 

  • Poska A, Saarse L (2002) Vegetation development and introduction of agriculture to Saaremaa Island, Estonia: the human response to shore displacement. Holocene 12:555–568

    Article  Google Scholar 

  • Prentice HC, Lönn M, Rosquist G, Ihse M, Kindström M (2006) Gene diversity in a fragmented population of Briza media: grassland continuity in a landscape context. J Ecol 94:87–97

    Article  CAS  Google Scholar 

  • Rangel TF, Diniz-Filho JAF, Bini LM (2010) SAM: a comprehensive application for spatial analysis in macroecology. Ecography 33:46–50

    Article  Google Scholar 

  • Reitalu T, Johansson LJ, Sykes MT, Hall K, Prentice H (2010) History matters: village distances, grazing and grassland species diversity. J Appl Ecol 47:1216–1224

    Article  Google Scholar 

  • Rico Y, Boehmer HJ, Wagner HH (2012) Determinants of actual functional connectivity for calcareous grassland communities linked by rotational sheep grazing. Landscape Ecol 27:199–209

    Article  Google Scholar 

  • Saar L, Takkis K, Pärtel M, Helm A (2012) Which plant traits predict species loss in calcareous grasslands with extinction debt? Divers Distrib 18:808–817

    Article  Google Scholar 

  • Tammekann A (1929) Outlines of the distribution of population in Estonia. Tartu Ülikooli ja Loodusuurijate Seltsi Aruanded XXXV: 372–379

  • R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. www.R-project.org

  • Thompson K, Jones A (1999) Human population density and prediction of local plant extinction in Britain. Conserv Biol 13:185–189

    Article  Google Scholar 

  • Van Geert A, Van Rossum F, Triest L (2008) Genetic diversity in adult and seedling populations of Primula vulgaris in a fragmented agricultural landscape. Conserv Genet 9:845–853

    Article  Google Scholar 

  • Vranckx G, Jacquemyn H, Muys B, Honnay O (2012) Meta-analysis of susceptibility of woody plants to loss of genetic diversity through habitat fragmentation. Conserv Biol 26:228–237

    Article  PubMed  Google Scholar 

  • WallisDeVries MF, Poschlod P, Willems JH (2002) Challenges for the conservation of calcareous grasslands in northwestern Europe: integrating the requirements of flora and fauna. Biol Conserv 104:265–273

    Article  Google Scholar 

  • Weber A, Kolb A (2011) Evolutionary consequences of habitat fragmentation: population size and density affect selection on inflorescence size in a perennial herb. Evol Ecol 25:417–428

    Article  Google Scholar 

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Acknowledgments

We thank Inga Hiiesalu, Raili Hansen, Hanna Kitt and Aino-Maria Helm for field assistance, Ülle Aarna for laboratory work, Tatjana Oja and Tiina Talve for the genetic analysis, Jesse M. Kalwij, Tsipe Aavik and Robert Szava-Kovats for helpful comments on an earlier version of this manuscript. We also thank the editor and four anonymous reviewers for their valuable comments on the manuscript. This study was funded by the Estonian Research Council (Grants no 9223 and 8613) and the European Union through the European Regional Development Fund (Centre of Excellence FIBIR).

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Correspondence to Krista Takkis.

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Takkis, K., Pärtel, M., Saar, L. et al. Extinction debt in a common grassland species: immediate and delayed responses of plant and population fitness. Plant Ecol 214, 953–963 (2013). https://doi.org/10.1007/s11258-013-0221-y

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