Life history strategies and biomass allocation the population dynamics of perennial plants in a regional perspective Eelke Jongejans Promotiecommissie Promotoren Prof. dr. F. Berendse Wageningen Universiteit Prof. dr. J.C.J.M. de Kroon Radboud Universiteit Nijmegen Overige leden Prof. dr. J. Ågren Uppsala Universiteit, Zweden Prof. dr. E. van der Meijden Universiteit Leiden Prof. dr. P.H. van Tienderen Universiteit van Amsterdam Prof. dr. ir. P.C. Struik Wageningen Universiteit Dit onderzoek is uitgevoerd binnen de onderzoeksschool SENSE. Life history strategies and biomass allocation the population dynamics of perennial plants in a regional perspective Eelke Jongejans Proefschrift ter verkrijging van de graad van doctor op gezag van de rector magnificus van Wageningen Universiteit, Prof. dr. ir. L. Speelman, in het openbaar te verdedigen op vrijdag 3 december 2004 des namiddags te vier uur in de Aula. Jongejans, E. (2004) Life history strategies and biomass allocation the population dynamics of perennial plants in a regional perspective Ph.D.-thesis, Nature Conservation and Plant Ecology group, Department of Environmental Science, Wageningen University, The Netherlands, with summaries in English and Dutch ISBN 90-8504-101-5 Contents 1. General introduction 1 2. Flexible life history responses to flower and rosette bud removal 11 in three perennial herbs Hartemink N, Jongejans E & de Kroon H 3. Size-dependent and -independent plant reproductive allocation 27 in response to successional replacement Jongejans E, de Kroon H & Berendse F 4. Bottlenecks and spatiotemporal variation in the sexual reproduction 49 pathway of perennials in meadows Jongejans E, Soons MB & de Kroon H 5. Space versus time variation in the population dynamics of Succisa 65 pratensis and two accompanying species Jongejans E & de Kroon H 6. Inbreeding depression significantly influences population dynamics: 89 a population-based model for a long-lived perennial herb Picó FX, Jongejans E, Quintana-Ascencio PF & de Kroon H 7. Effects of increased productivity on the population dynamics of the 103 endagered, clonal herb Cirsium dissectum Jongejans E, de Vere N & de Kroon H 8. A hierarchical population matrix analysis of the effect of nutrient enrichment: a synthesizing discussion 125 Jongejans E, Jorritsma-Wienk LD & de Kroon H Summary 145 Samenvatting 149 Nawoord 155 Affiliations of the co-authors 157 Curriculum vitae 159 1 General introduction Plant populations in a changing landscape Human impact on ecosystems threatens the survival of many species world-wide: their habitats are destroyed or degraded and become more fragmented (Tilman et al. 1994; Hanski & Ovaskainen 2000). Habitat is lost to agriculture, infrastructure and urban areas to satisfy increasing human demands. The remaining habitat patches are often small and isolated, which increases the vulnerability to negative influences from surrounding areas: disturbance, pollution through air or water, changes in water level regime, and, especially in areas of intensive agriculture, influx of nutrients (Saunders et al. 1991; Roem & Berendse 2000). Nutrient enrichment increases the productivity of nutrient-poor ecosystems and more competitive species take over from species that are characteristic for these ecosystems (de Kroon & Bobbink 1997). Besides, species richness can be expected to decrease with productivity in areas that currently receive high levels of nitrogen deposition such as the Netherlands (van Oene et al. 1999). Large population sizes usually buffer environmental, genetic and demographic stochasticity, but the risk of extinction caused by these sources of year-to-year variation increases when populations are reduced to low numbers of individuals by habitat fragmentation and environmental factors (Menges 1998; Oostermeijer 2003). Small populations contain less genetic variation that may be necessary to adapt to changing environmental conditions (Ellstrand & Elam 1993). Demographic stochasticity in population dynamics is for instance the chance event of simultaneously a high death rate and a low establishment rate in one year. Besides, small populations may perform less just because they are small (e.g. because they fail to effectively attract pollinators), which is called the Allee-effect (Fischer & Matthies 1998; Colas et al. 2001), or because inbreeding starts to affect the performance of individuals. The increasing distances between populations amplifies these problems, as they diminish the probabilities of arrival of genetically-different seeds or pollen in areas with populations that are decreasing in size or are already extinct. Genetically impoverished populations are therefore unlikely to survive. Metapopulation theory predicts that the number of occupied habitats declines with habitat size and habitat connectivity (MacArthur & Wilson 1967; Ouborg 1993). Climate change increases the importance of connectivity as species have to disperse to keep up with possible change in the spatial distribution of climates they are adapted to (Thomas et al. 2004). Since most nations engaged the obligation to protect our plant species at the Rio convention on biological diversity (Myers 1993), the above-mentioned issues urge to answer the important question: can plant species survive in highly-fragmented landscapes such as we find in the Netherlands? The research program ‘Survival of plant species in fragmented landscapes’ To generate data and knowledge on the mechanisms that affect the survival chances of plant species in fragmented landscapes, the Netherlands Organization for Scientific Research (NWO-ALW) financed the research program ‘Survival of plant species in fragmented landscapes’. In this program, which was chaired by Jan van Groenendael, plant ecologists from several institutes worked together on different aspects of the topic in the same study system: nutrient-poor, species-rich meadows. Three projects were started on the landscape ecology, local population dynamics, and genetics of a set of model species respectively. The projects were integrated by close cooperation by the PhD students involved and by a post-doctoral modelling project. At Utrecht University Merel Soons finished her PhD thesis in 2003: ‘Habitat fragmentation and connectivity. Spatial and temporal characteristics of the colonization process in plants’. Her research focused on the effects of habitat fragmentation on the dispersal of seeds between habitat patches and the colonization abilities of plants in realistic landscapes. ‘Life history strategies and biomass allocation. The populations dynamics of perennial plants in a regional perspective’ is the title of the second project, that resulted in the PhD thesis in front of you. At Wageningen University I studied the dynamics of natural plant populations, and the impact of nutrient enrichment on life history components of these plants in experiments and population models. At the University of Nijmegen Carolin Mix performed a PhD study entitled ‘Inbreeding and outbreeding: effects of gene flow and local adaptation on the survival of small isolated populations of plants in a regional context’. She investigated the genetic effects of habitat fragmentation on the performance of the remaining populations, which are often small and isolated. Felix Knauer used model exercises and the results of these three projects to study the effectiveness of ecological corridors and agri-environmental schemes, which aim to alleviate the isolation of remnant populations. The title of his post-doctoral project at Alterra (Wageningen UR) was ‘Integration and application: regional survival in changing landscapes’. Study system: herb species of nutrient-poor, species-rich meadows The studied habitats were restricted to nutrient-poor grassland fragments of the Pleistocene soil areas of the Netherlands (Soons 2003), which include the plant communities Molinietalia and Caricetalia (Schaminée et al. 1995; Schaminée et al. General introduction 1996). These moist grasslands were formerly used as hay meadows and increased in 1 abundance in the 19th century when an increasing area of peat bogs and fens was cultivated (Buck-Sorlin 1993). In the 20th century (especially the first half) more than Chapter 99% of these habitats was lost (Soons 2003), probably due to intensification of cultivation for agriculture by drainage and fertilization (Buck-Sorlin 1993). Most of the . remnants of these semi-natural grasslands have now become nature reserves and are 2 3 managed by continuing the old land use practices: mowing and hay removal, in order . Chapter to counter 1) the encroachment of shrubs and trees, and 2) the disrupting effect of nutrient enrichment (Bakker & Berendse 1999). As model species we chose four species that occur in these meadows and that are phylogenetically closely related (all belong to the families Asteraceae or 1 Dipsacaceae). They have the same life history options (i.e. sexual reproduction, General introduction survival and clonal propagation; cf. Fig. 1), but they have distinctly different life history strategies, i.e. they differ in longevity and clonality: Hypochaeris radicata L. plants normally live only for a few years, whereas Succisa pratensis Moench. (through flow lrg sdl sml cl.v cl.f Figure 1. The life cycle of Cirsium dissectum with six stage classes: seedlings (sdl), small vegetative rosettes (sml), large vegetative rosettes (lrg), flowering rosettes (flow), vegetative clonal offspring (cl.v), and flowering clonal offspring (cl.f). The arcs denote the contribution probabilities