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The Effect of Reductions in Population Size and Habitat Variables on Levels Habitat quality and Genetics in Cirsium dissectum 1 The original publication is available at www.springerlink.com 2 http://dx.doi.org/10.1007/s00442-008-1203-y 3 Oecologia (2009) 159:59-68 4 5 Population size and habitat quality affect genetic diversity 6 and fitness in the clonal herb, Cirsium dissectum 7 Natasha de Vere, Eelke Jongejans, Amy Plowman & Eirene Williams 8 9 1. Field Conservation and Research Department, Whitley Wildlife Conservation 10 Trust, UK. And The National Botanic Garden of Wales, Llanarthne, 11 Carmarthenshire, SA32 8HG, UK. email: [email protected] tel: 12 01558 667198 fax: 01558 668933 13 2. Department of Experimental Plant Ecology, Radboud University Nijmegen, 14 Toernooiveld 1, 6525 ED Nijmegen, The Netherlands. And: Department of 15 Biology, Pennsylvania State University, 208 Mueller Lab, 16802 PA University 16 Park, USA. 17 3. Field Conservation and Research Department, Whitley Wildlife Conservation 18 Trust, UK 19 4. School of Biological Sciences, University of Plymouth, Plymouth, UK 20 Abstract Remaining populations of plant species in fragmented landscapes are 21 threatened by declining habitat quality and reduced genetic diversity, but the 22 interactions of these major factors are rarely studied together for species conservation. 23 The interactions between population size, habitat quality, genetic diversity and fitness 24 were investigated in 22 populations of the clonal herb, Cirsium dissectum throughout 25 the British Isles. Regression analysis was used to identify significant factors and a 26 structural equation model was developed to illustrate and integrate these interactions. 27 Smaller populations (measured as the total number of plants) had lower genetic 28 diversity (proportion of polymorphic loci), and reduced genetic diversity (allelic 29 richness) had a negative impact on the survival of seedlings grown under standard 30 conditions. Habitat quality also had a large effect on C. dissectum. Unmanaged sites 31 with tall vegetation, no bare soil and higher nutrient levels had smaller populations of 32 C. dissectum, but flowering was promoted. Flowering was suppressed in heavily 33 grazed sites with short vegetation. Higher levels of bare soil and phosphorus both had 34 a positive influence on genetic diversity, but through distinctly different pathways: 35 bare soil provides safe sites for establishment, whilst phosphorus may promote 36 flowering and improve seed germination. In order to conserve C. dissectum, 37 management needs to maintain site heterogeneity so that C. dissectum can flower and 38 establishment gaps are still available for seedlings; when either component is reduced, 39 negative feedbacks through reduced genetic diversity and individual fitness can be 40 expected. This study therefore highlights the importance of considering both 41 conservation genetics and habitat quality in the conservation of plant species. 42 Keywords Plant species conservation, ecological genetics, habitat management, 43 structural equation model 44 Introduction 45 Habitat destruction and habitat fragmentation continue to threaten the survival of 46 many species worldwide (Tilman et al. 1994; Hanski and Ovaskainen 2000). 47 Biodiversity research that attempts to understand the processes that occur as species 48 decline is thus very important. Ouborg et al. (2006) define two paradigms within 49 biodiversity research: conservation genetics and habitat quality, and they state that Page 1 of 16 Habitat quality and Genetics in Cirsium dissectum 1 research tends to concentrate on one element or the other. However, in order to fully 2 understand and develop conservation solutions, habitat quality and genetics need to be 3 considered together. 4 Conservation genetics emphasises that reductions in population size and 5 increases in population isolation lead to negative consequences that reduce individual 6 fitness and ultimately increase the risk of extinction (Ellstrand and Elam 1993; Reed 7 2005; Oostermeijer et al. 2003). Genetic diversity is likely to decrease in small 8 populations, as rare alleles are lost (Oostermeijer et al. 2003) and this may reduce the 9 ability of a species to adapt to changing environmental conditions (Barrett and Kohn 10 1991). Levels of inbreeding can increase as the number of mates available decrease 11 and also through disruption of processes such as plant-pollinator interactions 12 (Oostermeijer et al. 1998). The consequent reduction in heterozygosity can lead to 13 inbreeding depression (Hartl and Clark 1997); in plant species this is often associated 14 with increased seed abortion, low germination rates, high seedling mortality and poor 15 growth and flowering of offspring (Oostermeijer et al. 2003; Dudash and Fenster 16 2000). Relationships between population size, genetic diversity and fitness have been 17 widely studied and positive correlations between these factors are generally found 18 (Oostermeijer et al. 2003; Leimu et al 2006). 19 Habitat quality, however, may also affect population size, genetic diversity 20 and plant performance by influencing demographic transitions in plant populations. 21 Sexual recruitment, for example, can be reduced or potentially permanently 22 suppressed by environmental variables such as mowing (Schaal and Leverich 1996), 23 canopy closure (Kudoh et al. 1999), climate (Eckert 1999) or an increase in site 24 productivity (Colling et al. 2002; Endels et al. 2004). Reductions in sexual 25 recruitment often lead to a decrease in genetic diversity (Kudoh 1999, Jacquemyn et 26 al. 2005; 2006, Kleijn and Steinger 2002). 27 In natural populations it is likely that population size, genetic diversity and 28 habitat quality all interact to determine individual fitness and the survival of plant 29 populations (Fig. 1). Studies that take this combined approach are therefore very 30 important but are not frequent within the literature (e.g. Schmidt and Jensen 2000). 31 Oostermeijer et al. (1998) demonstrated that habitat factors play an important role 32 alongside population size and genetic diversity in the performance of the rare species 33 Gentiana pneumonanthe. Vergeer et al. (2003) found that larger populations of 34 Succisa pratensis had reduced inbreeding and greater fitness, while high soil 35 ammonium had a negative effect on population size and fitness but did not affect 36 genetic diversity. 37 This study aims to extend this approach to clonal species by exploring key 38 population, habitat and genetic characteristics and relating these factors to individual 39 fitness in Cirsium dissectum, an Asteraceae species that shows considerable clonal as 40 well as sexual reproduction. 41 C. dissectum is found in wet, nutrient-poor, semi-natural grasslands in 42 northwest Europe. It is endangered in Germany and the Netherlands (Buck-Sorlin 43 1993; Buck-Sorlin and Weeda 2000; Soons et al. 2005) and has declined in all of the 44 countries within which it is found (Institut floristique Franco-Belge 1995; Preston et 45 al. 2002; Hackney 1992). 46 C. dissectum is quite specialised in its habitat requirements, but can be 47 abundant in suitable conditions; it has declined due to the loss and modification of its 48 habitat (de Vere 2007a). Its sites were traditionally managed through extensive 49 grazing, burning and hay cutting and it is therefore a casualty of the changes in 50 traditional farming practice that have led to losses in all types of semi-natural, Page 2 of 16 Habitat quality and Genetics in Cirsium dissectum 1 oligotrophic grasslands (HMSO 1995). Reductions in grazing and application of 2 fertilizers have caused an increase in site productivity throughout these grasslands 3 (UK Biodiversity Steering Group 1995). Jongejans et al. (2006a, 2008) discovered 4 that C. dissectum is a poor competitor; it is unable to build up biomass, that is 5 necessary to withstand competition, as productivity increases and this reduces the 6 probability of survival. 7 This study examines the interactions between population size, habitat quality, 8 genetic diversity and individual fitness in a range of natural populations (n = 22) of C. 9 dissectum throughout the British Isles and considers the implications of the results for 10 the conservation of C. dissectum. Specifically we examine: 11 a) The effect of management on habitat quality. 12 b) The effect of population size on genetic diversity and fitness. 13 c) The effect of genetic diversity on fitness. 14 d) The effect of habitat quality on population size, genetic diversity and fitness. 15 Materials and Methods 16 Study species and sites 17 Cirsium dissectum (L.) Hill (Asteraceae) is a rhizomatous herb that forms 18 rosettes with up to five softly prickled leaves. Flowering stems are formed apically 19 with normally one flower head (capitulum), rarely two or three. After seed set a 20 rosette dies off. It is self-compatible but selfed plants produce fewer seeds compared 21 with those that are crossed (Kay and John 1994; de Vere 2007b). The species 22 reproduces vegetatively by means of long rhizomes, which then die leaving 23 independent ramets (de Vere 2007b). 24 Twenty-two populations of C. dissectum were selected throughout the species 25 range in the British Isles (Fig. 2). These populations are representative of the range of 26 population sizes and habitat types within which the species is found. For each of these 27 populations the following four groups of measurements were taken: population size, 28 habitat quality, genetic diversity and fitness (these are listed in Table
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