The spatial and temporal dynamics of plant-animal interactions in the forest herb Actaea spicata Hugo von Zeipel Stockholm University ©Hugo von Zeipel, Stockholm 2007 Cover: Actaea spicata and fruits with exit holes from larvae of the moth Eupithecia immundata. Photo: Hugo von Zeipel ISBN 978-91-7155-535-9 Printed in Sweden by Universitetsservice, US-AB, Stockholm 2007 Distributor: Department of Botany, Stockholm University Till slut Doctoral dissertation Hugo von Zeipel Department of Botany Stockholm University SE-10691 Stockholm Sweden The spatial and temporal dynamics of plant-animal interactions in the forest herb Actaea spicata Abstract – Landscape effects on species performance currently receives much attention. Habitat loss and fragmentation are considered major threats to species diversity. Deciduous forests in southern Sweden are previous wooded pastures that have become species-rich communities appearing as islands in agricultural landscapes, varying in species composition. Actaea spicata is a long-lived plant occurring in these forests. In 150 populations in a 10-km2 area, I studied pre-dispersal seed predation, seed dispersal and pollination. I investigated spatio-temporal dynamics of a tritrophic system including Actaea, a specialist seed predator, Eupithecia immundata, and its parasitoids. In addition, effects of biotic context on rodent fruit dispersal and effects of flowering time and flower number on seed set, seed predation and parasitization were studied. Insect incidences of both trophic levels were related to resource population size and small Eupithecia populations were maintained by the rescue effect. There was a unimodal relationship between seed predation and plant population size. Seed predator populations fre- quently went extinct in small plant populations, resulting in low average seed predation. Parasitoids were present in large plant populations but did not affect seed predator density. Seed predators aggregated at edges, relaxing seed predation in patch interiors. Flowering phenology was unrelated to seed set and insect incidence. A higher flower number did not influence seed pre- dation but was associated with higher seed set and a tendency for a higher parasitization rate. In the study on fruit dispersal more fruits were removed inside than outside populations. Within plant populations more fruits were removed from large aggregations. Overall, this thesis underlines the impor- tance of plant-animal interactions during different phases of the life cycle. The spatial configuration of host plants plays an important role for the out- come of plant-animal interactions and trophic cascades. Keywords – Eupithecia immundata, parasitoid, rodent, seed predation, dis- persal, recruitment, multitrophic, metapopulation, trophic cascades, commu- nity complexity List of papers This thesis is based on the following papers, referred to in the text by their Roman numerals: I von Zeipel, H., Eriksson, O. and Ehrlén, J. 2006. Host plant population size determines cascading effects in a plant- herbivore-parasitoid system. Basic and Applied Ecology 7: 191-200. II von Zeipel, H. and Eriksson, O. 2007. Fruit removal in the forest herb Actaea spicata depends on local context of fruits sharing the same dispersers. International Journal of Plant Sciences 168: 855-860. III von Zeipel, H., Dahlgren, J., Ehrlén, J. Effects of flowering phenology and inflorescence size on interactions at three tro- phic levels. Manuscript. IV von Zeipel, H., Ehrlén, J. Spatio-temporal dynamics in a tri- trophic plant-seed predator-parasitoid system. Manuscript. Previously printed and accepted papers are printed in this thesis with the kind permission from the copyright holders. Contents Introduction .....................................................................................................9 Landscape studies of intertrophic relationships..............................................9 Plant-insect interactions................................................................................11 Questions asked in this thesis ......................................................................13 Methods.........................................................................................................14 Study system.................................................................................................14 Study area.....................................................................................................16 Data collection and aims of the different studies ..........................................16 Results and Discussion.................................................................................19 Paper I – Effects of resource population size on insect distribution at two trophic levels .................................................................................................19 Paper II – effects of plant and fruit abundance on fruit removal by rodents.19 Paper III – seed set and insects in relation to flowering phenology and inflorescence size..........................................................................................20 Paper IV – dynamics of three trophic levels over four years ........................20 Concluding remarks ......................................................................................22 Acknowledgement.........................................................................................25 References....................................................................................................26 Svensk sammanfattning................................................................................30 Tack...............................................................................................................34 Introduction Landscape studies of intertrophic relationships Nature is heterogeneous. Spatial ecologists try to describe the spatial hetero- geneity as accurately as possible. However, when nature is translated into data, this is bound to be associated with a loss of information. First, since time and resources are limited, we always need to make simplifications. Second, we do not always have a perfect understanding of how the landscape is perceived by the organisms we study. Collection of data in spatial ecology is thus dependent on judgements made by the researchers. The heterogeneity of nature can be perceived at all scales (Fig. 1), from the largest geographical scale representing the species world wide distribution at a very coarse reso- lution, to the smallest small scale heterogeneity surrounding individual plants. The relevant scale for studies of organisms and interactions will de- pend on the mobility of the focal species. One simplification that is often made is to divide the environment into suit- able and unsuitable habitat for a species. A species’ suitable habitat is an area where the environmental conditions allow individuals to survive and reproduce. Suitable patches for a specialized herbivore may be defined by the distribution of its host plant. However, host plant patches might still be unsuitable because of the abiotic environment. For plants it is usually more difficult to define suitable habitat than for specialized insects. Figure 1. Schematic view of a hypothetical landscape. Plant populations are depicted at three different scales, zooming in and increasing details from left to right. Which level to choose should be based on the biology of the species in focus but it is often arbitrary and up to the researcher to decide. In this study the distance separating two patches was set to 25 meters. Colonizations and extinctions among patches indicate that this patch definition is reasonable. 9 Metapopulation ecology is based on such a division of habitats into suitable and unsuitable. It recognizes three important processes, “migration and how it affects local dynamics, population extinction and the establishment of new local populations” (Hanski, 1999). The common definition of a population is that individuals are more likely to breed with other individuals within the population than with individuals from other populations. A metapopulation consists of a set of local populations that are connected by migration but where migration is limited (Hanski and Gilpin 1997). Movements between habitat patches ensure a long-term balance between local extinctions and recolonizations, allowing the metapopulation to persist at an equilibrium fraction of patch occupancy. This fraction is influenced by the size and isola- tion of the individual patches (Hanski 1999). Metapopulation theory has contributed considerably to the insight that not only the quality but also the spatial arrangement of habitat may be important for species survival. Along with the recognition of human impact on landscape features there has been an increasing concern for how landscape changes affect species perform- ance, and in the long run biodiversity. A large number of studies have show alarming effects of habitat loss, whereas the effects of fragmentation per se are less clear as they are often associated with habitat loss (Fahrig 2003). Plant metapopulation dynamics involves spatial effects on the probability of interacting with mutualistic and antagonistic animals. Patch size and isola- tion affects pollen transportation and the chance of dispersal into other occu- pied or unoccupied patches. It also affects the risk of herbivory. Plant meta- populations with a high degree of local turnover through extinctions and colonizations exist primarily among short-lived