Abstract
The management of remnant populations in highly fragmented landscapes requires a thorough understanding of the processes shaping population persistence. We investigated relationships between population characteristics (i.e. size, density and pollinator abundance), offspring performance, genetic diversity and differentiation in Trollius europaeus, a plant with a nursery pollination system. In 19 populations of different sizes and located in north-east Switzerland, an area which has undergone widespread land use changes over the last decades, we assessed neutral genetic diversity (N total = 383) using AFLPs and plant performance in a greenhouse experiment (N total = 584) using competition and control treatments. Overall genetic differentiation was low (F ST = 0.033) with a marginal significant isolation by distance effect (P = 0.06) indicating (historical) genetic connectivity among the populations. Mean expected heterozygosity was H E of 0.309 (0.0257–0.393) while inbreeding coefficients (F IS) were significant in only three populations. Genetic diversity was not related to population size, plant density or pollinator abundance. Plant performance was reduced under competition (P < 0.001) but the severity of competition was independent of genetic diversity and population size. In summary, remnant populations of T. europaeus retain genetic diversity and seem capable of persisting under the present conditions within an agricultural matrix. T. europaeus is a perennial herb, thus it may require several generations for the negative effects of fragmentation and isolation to manifest. Our findings indicate that small populations are as important as large populations for the conservation and management of genetic resources.


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Amos W, Balmford A (2001) When does conservation genetics matter? Heredity 87:257–265
Bohonak AJ (2002) IBD (isolation by distance): a program for analyses of isolation by distance. J Hered 93:153–154
Bond WJ (1994) Do mutualisms matter-assessing the impact of pollinator and disperser disruption on plant extinction. Philos Trans R Soc Lond B 344(1307):83–90
Booy G, Hendriks RJJ, Smulders MJM, Van Groenendael JM, Vosman B (2000) Genetic diversity and the survival of populations. Plant Biol 2(4):379–395
Bowman G, Perret C, Hoehn S, Galeuchet DJ, Fischer M (2008) Habitat fragmentation and adaptation: a reciprocal replant-transplant experiment among 15 populations of Lychnis flos-cuculi. J Ecol 96(5):1056–1064. doi:10.1111/j.1365-2745.2008.01417.x
Broggi MF, Schlegel H (1989) Mindestbedarf an naturnahen Flächen in der Kulturlandschaft. Dargestellt am Beispiel des schweizerischen Mittellandes. Bericht 31 des Nationalen Forschungsprogrammes ‘Nutzung des Bodens in der Schweiz', Bern
Brownlie H, Playford J, Wallace H, Shapcott A (2009) Population ecology and genetics of the vulnerable Acacia attenuata (Mimosaceae) and their significance for its conservation, recovery and translocation. Aust J Bot 57(8):675–687. doi:10.1071/bt09116
Byers DL, Waller DM (1999) Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annu Rev Ecol Syst 30:479–513
Dasmahapatra KK, Lacy RC, Amos W (2008) Estimating levels of inbreeding using AFLP markers. Heredity 100(3):286–295. doi:10.1038/sj.hdy.6801075
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(1):59–68. doi:10.1007/s00442-008-1203-y
Després L (2003) Sex and pollen: the role of males in stabilising a plant-seed eater pollinating mutualism. Oecologia 135(1):60–66
Després L, Loriot S, Gaudeul M (2002) Geographic pattern of genetic variation in the European globeflower Trollius europaeus L. (Ranunculaceae) inferred from amplified fragment length polymorphism markers. Mol Ecol 11(11):2337–2347
Doroszewska A (1974) The genus Trollius L.—a taxonomical study. In: Kostyniuk M (ed) Monographiae botanicae, vol 41. Warszawa, pp 89–102
Dostalek T, Munzbergova Z, Plackova I (2010) Genetic diversity and its effect on fitness in an endangered plant species Dracocephalum austriacum L. Conserv Genet 11(3):773–783. doi:10.1007/s10592-009-9879-z
Dufay M, Anstett MC (2003) Conflicts between plants and pollinators that reproduce within inflorescences: evolutionary variations on a theme. Oikos 100(1):3–14. doi:10.1034/j.1600-0706.2003.12053.x
Ehrlich PR, Wilson EO (1991) Biodiversity studies-science and policy. Science 253(5021):758–762
Ellenberg H (1996) Vegetation Mitteleuropas mit den Alpen in ökologischer, dynamischer und historischer Sicht 5th edn. Eugen Ulmer Gmbh & C0., Stuttgart (Hohenheim)
Ellstrand NC, Elam DR (1993) Population genetic consequences of small population-Size—implications for plant conservation. Annu Rev Ecol Syst 24:217–242
Eriksson O, Ehrlen J (2001) Landscape fragmentation and the viability of plant populations. In: Silvertown J, Antonovics J (eds) Integrating ecology and evolution in a spatial context. Blackwell, Oxford
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515. doi:10.1146/annurev.ecolsys.34.011802.132419
Fenster C, Dudash M (1994) Genetic considerations for plant population restoration and conservation. In: Bowles M, Whelan C (eds) Restoration of endangered species: conceptual issues, planning, and implementation. Cambridge University Press, Cambridge, pp 34–62
Fischer M, Matthies D (1998) Effects of population size on performance in the rare plant Gentianella germanica. J Ecol 86(2):195–204
Fischer M, van Kleunen M, Schmid B (2000) Genetic allee effects on performance, plasticity and developmental stability in a clonal plant. Ecol Lett 3(6):530–539
Galeuchet DJ, Perret C, Fischer M (2005) Microsatellite variation and structure of 28 populations of the common wetland plant, Lychnis flos-cuculi L., in a fragmented landscape. Mol Ecol 14(4):991–1000
Gaudeul M, Taberlet P, Till-Bottraud I (2000) Genetic diversity in an endangered alpine plant, Eryngium alpinum L. (Apiaceae), inferred from amplified fragment length polymorphism markers. Mol Ecol 9(10):1625–1637
Ghazoul J (2005) Pollen and seed dispersal among dispersed plants. Biol Rev 80(3):413–443
Gough L, Osenberg CW, Gross KL, Collins SL (2000) Fertilization effects on species density and primary productivity in herbaceous plant communities. Oikos 89(3):428–439
Hobbs RJ, Yates CJ (2003) Impacts of ecosystem fragmentation on plant populations: generalising the idiosyncratic. Aust J Bot 51(5):471–488
Jacquemyn H, Brys R, Adriaens D, Honnay O, Roldan-Ruiz I (2009) Effects of population size and forest management on genetic diversity and structure of the tuberous orchid Orchis mascula. Conserv Genet 10(1):161–168. doi:10.1007/s10592-008-9543-z
Jaeger N, Després L (1998) Obligate mutualism between Trollius europaeus and its seed-parasite pollinators Chiastocheta flies in the Alps. C R Acad Sci Paris Life Sci 321(9):789–796
Johannesen J, Loeschcke V (1996) A hierarchical analysis of genetic structure and variability in patchily distributed coexisting Chiastocheta species (Diptera: Anthomyiidae). Heredity 76:437–448
Johnson SD, Steiner KE (2000) Generalization versus specialization in plant pollination systems. Trends Ecol Evol 15(4):140–143
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17(5):230–241
Kery M, Matthies D, Spillmann HH (2000) Reduced fecundity and offspring performance in small populations of the declining grassland plants Primula veris and Gentiana lutea. J Ecol 88(1):17–30
Klank C, Pluess AR, Ghazoul J (2010) Effects of population size on plant reproduction and pollinator abundance in a specialised pollination system. J Ecol 98:1389–1397. doi:10.1111/j.1365-2745.2010.01720.x
Krauss J, Bommarco R, Guardiola M, Heikkinen RK, Helm A, Kuussaari M, Lindborg R, Ockinger E, Partel M, Pino J, Poyry 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(5):597–605. doi:10.1111/j.1461-0248.2010.01457.x
Kuss P, Pluess AR, Aegisdottir HH, Stöcklin J (2008) Spatial isolation and genetic differentiation in naturally fragmented plant populations of the Swiss Alps. J Plant Ecol 1(3):149–159. doi:10.1093/jpe/rtn009
Lammi A, Siikamaki P, Mustajarvi K (1999) Genetic diversity, population size, and fitness in central and peripheral populations of a rare plant Lychnis viscaria. Conserv Biol 13(5):1069–1078
Lauber K, Wagner G (2001) Flora helvetica: Farbfotos von 3000 Blüten- und Farnpflanzen der Schweiz, Artenbeschreibungen und Bestimmungsschlüssel, 3rd edn. Paul Haupt, Bern
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(5):942–952
Lemke T (2011) The situation of Trollius europaeus L. (Ranunculaceae) in the north-east of Central Europe-history, current changes and conservation. Plant Divers Evol 129(3–4):219–228. doi:10.1127/1869-6155/2011/0129-0039
Lienert J, Fischer M, Schneller J, Diemer M (2002) Isozyme variability of the wetland specialist Swertia perennis (Gentianaceae) in relation to habitat size, isolation, and plant fitness. Am J Bot 89(5):801–811
Luijten SH, Dierick A, Oostermeijer JGB, 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(6):1776–1787
Lynch M, Milligan BG (1994) Analysis of population genetic structure with RAPD markers. Mol Ecol 3(2):91–99
Lynch M, Conery J, Burger R (1995) Mutation accumulation and the extinction of small populations. Am Nat 146(4):489–518
Mittelbach GG, Steiner CF, Scheiner SM, Gross KL, Reynolds HL, Waide RB, Willig MR, Dodson SI, Gough L (2001) What is the observed relationship between species richness and productivity? Ecology 82(9):2381–2396
Muncaciu S, Gafta D, Cristea V, Rosca-Casian O, Goia I (2010) Eco-coenotic conditions and structure of Trollius europaeus L. populations in an extrazonal habitat complex (Transylvanian Carpathian foothills). Flora 205(11):711–720. doi:10.1016/j.flora.2010.04.017
Nybom H, Bartish IV (2000) Effects of life history traits and sampling strategies on genetic diversity estimates obtained with RAPD markers in plants. Perspect Plant Ecol Evol Syst 3(2):93–114
Oostermeijer JGB, Vaneijck MW, Dennijs JCM (1994) Offspring fitness in relation to population size and genetic variation in the rare perennial plant species Gentiana pneumonanthe (Gentianaceae). Oecologia 97(3):289–296
Ouborg NJ, Vantreuren R (1994) The Significance of genetic erosion in the process of extinction 4. Inbreeding load and heterosis in relation to population-size in the mint salvia pratensis. Evolution 48(4):996–1008
Ouborg NJ, Vantreuren R (1995) Variation in fitness related characters among small and large populations of Salvia pratensis. J Ecol 83(3):369–380
Pellmyr O (1989) The cost of mutualism-interactions between Trollius europaeus and its pollinating parasites. Oecologia 78(1):53–59
Pellmyr O (1992) The phylogeny of a mutualism-evolution and coadaptation between Trollius and its seed-parasitic pollinators. Biol J Linn Soc 47(4):337–365
Pluess AR, Stöcklin J (2004) Genetic diversity and fitness in Scabiosa columbaria in the Swiss Jura in relation to population size. Conserv Genet 5(2):145–156
Podolsky RH (2001) Genetic variation for morphological and allozyme variation in relation to population size in Clarkia dudleyana, an endemic annual. Conserv Biol 15(2):412–423
Pompanon F, Pettex E, Després L (2006) Patterns of resource exploitation in four coexisting globeflower fly species (Chiastocheta sp.). Acta Oecol 29(2):233–240
Qiu J, Fu YB, Bai YG, Wilmshurst JF (2009) Genetic variation in remnant Festuca hallii populations is weakly differentiated, but geographically associated across the Canadian Prairie. Plant Spec Biol 24(3):156–168. doi:10.1111/j.1442-1984.2009.00251.x
R Development Core Team (2009) R: a language and environment for statistical computing. R Development Core Team, Vienna
Reed DH (2004) Extinction risk in fragmented habitats. Anim Conserv 7:181–191. doi:10.1017/s1367943004001313
Rousset F (1997) Genetic differentiation and estimation of gene flow from F statistics under isolation by distance. Genetics 145(4):1219–1228
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(5459):1770–1774
Saunders DA, Hobbs RJ, Margules CR (1991) Biological consequences of ecosystem fragmentation—a review. Conserv Biol 5(1):18–32
Schippers P, Joenje W (2002) Modelling the effect of fertiliser, mowing, disturbance and width on the biodiversity of plant communities of field boundaries. Agric Ecosyst Environ 93(1–3):351–365
Schleuning M, Niggemann M, Becker U, Matthies D (2009) Negative effects of habitat degradation and fragmentation on the declining grassland plant Trifolium montanum. Basic Appl Ecol 10(1):61–69. doi:10.1016/j.baae.2007.12.002
Schmidt K, Jensen K (2000) Genetic structure and AFLP variation of remnant populations in the rare plant Pedicularis palustris (Scrophulariaceae) and its relation to population size and reproductive components. Am J Bot 87(5):678–689
Schulz B, Dosch F (2005) Trends der Siedlungsflächenentwicklung und ihre Steuerung in der Schweiz und Deutschland. DISP 160:5–15
Shaffer ML (1981) Minimum population sizes for species conservation. Bioscience 31(2):131–134
Snaydon RW (1991) Replacement or additive designs for competition studies. J Appl Ecol 28(3):930–946
Spigler RB, Hamrick JL, Chang SM (2010) Increased inbreeding but not homozygosity in small populations of Sabatia angularis (Gentianaceae). Plant Syst Evol 284(3–4):131–140. doi:10.1007/s00606-009-0245-x
Stephens PA, Sutherland WJ, Freckleton RP (1999) What is the Allee effect? Oikos 87(1):185–190
Suding KN, Collins SL, Gough L, Clark C, Cleland EE, Gross KL, Milchunas DG, Pennings S (2005) Functional- and abundance-based mechanisms explain diversity loss due to N fertilization. Proc Nat Acad Sci USA 102(12):4387–4392
Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5(12):537–542
Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, Erasmus BFN, de Siqueira MF, Grainger A, Hannah L, Hughes L, Huntley B, van Jaarsveld AS, Midgley GF, Miles L, Ortega-Huerta MA, Peterson AT, Phillips OL, Williams SE (2004) Extinction risk from climate change. Nature 427(6970):145–148. doi:10.1038/nature02121
Thompson K, Jones A (1999) Human population density and prediction of local plant extinction in Britain. Conserv Biol 13(1):185–189
Vekemans X, Beauwens T, Lemaire M, Roldan-Ruiz I (2002) Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Mol Ecol 11(1):139–151
Vergeer P, Rengelink R, Copal A, Ouborg NJ (2003a) The interacting effects of genetic variation, habitat quality and population size on performance of Succisa pratensis. J Ecol 91(1):18–26
Vergeer P, Rengelink R, Ouborg NJ, Roelofs JGM (2003b) Effects of population size and genetic variation on the response of Succisa pratensis to eutrophication and acidification. J Ecol 91(4):600–609
Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277(5325):494–499
Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization in pollination systems, and why it matters. Ecology 77(4):1043–1060
Whitlock R, Hipperson H, Mannarelli M, Butlin RK, Burke T (2008) An objective, rapid and reproducible method for scoring AFLP peak-height data that minimizes genotyping error. Mol Ecol Resour 8(4):725–735
Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11(10):413–418
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R Statistics for biology and health. Springer, New York
Acknowledgments
Funding was provided by the Ecosystem Management Group, ETH Zurich. We thank the department of nature conservation of the canton Zurich for their permission to study populations located on nature protection areas, and private land owners for allowing access. Genetic data analysed in this paper were generated in the Genetic Diversity Centre of ETH Zurich, and additional practical support was provided by the Plant Ecological Genetics group, ETH Zurich. We thank Constanze Conradin and Abigail Manalastas for their assistance in the ecological experiment. All experiments complied with the current Swiss laws.
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Klank, C., Ghazoul, J. & Pluess, A.R. Genetic variation and plant performance in fragmented populations of globeflowers (Trollius europaeus) within agricultural landscapes. Conserv Genet 13, 873–884 (2012). https://doi.org/10.1007/s10592-012-0337-y
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DOI: https://doi.org/10.1007/s10592-012-0337-y


