The Spatial and Temporal Dynamics of Plant-Animal Interactions in the Forest Herb Actaea Spicata

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 frequently 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 predation 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 importance of plant-animal interactions during different phases of the life cycle. The spatial configuration of host plants plays an important role for the outcome of plant-animal interactions and trophic cascades.

Keywords – Eupithecia immundata, parasitoid, rodent, seed predation, dispersal, recruitment, multitrophic, metapopulation, trophic cascades, community 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 trophic levels. Manuscript.

IV von Zeipel, H., Ehrlén, J. Spatio-temporal dynamics in a tritrophic 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 heterogeneity 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 depend on the mobility of the focal species.

One simplification that is often made is to divide the environment into suitable 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 isolation 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 performance, 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 isolation affects pollen transportation and the chance of dispersal into other occupied or unoccupied patches. It also affects the risk of herbivory. Plant metapopulations with a high degree of local turnover through extinctions and colonizations exist primarily among short-lived dispersive plants, while long-lived plants, and plants with a persisting seed bank, have slower dynamics and may form remnant populations that are able to withstand unfa- vorable conditions during considerable time periods (Eriksson 1996). In specialized plant-animal interactions, the effect of spatial context on species occurrence can affect both of the involved trophic levels. For the plant, occurrence of an animal species could either be negative (e. g. an antagonistic plant-herbivore interaction) or positive (e. g. a mutualistic plant-pollinator interaction).

It is well established that the incidence of an insect species increases with host population size and decreases with isolation (e.g. Kruess and Tscharntke, 2000; Kery et al. 2001; Ehlers and Olesen, 2003; Colling and Matthies, 2004). Small populations are more susceptible to demographic (Shaffer 1981, Lande 1993, Kery et al. 2003) and genetic (Ellstrand and Elam 1993) stochasticity. Small populations experience low per capita growth rate, i.e. the Allée effect. Apart from inbreeding depression, they can have problems with skewed sex ratios; females may need more time to mate or fail to mate (Lande 1987). Emigration rates in small patch sizes may be

10 higher than in large patches (Kuussaari et al. 1996, Hill et al. 1996), and immigrants may avoid small patches (Smith and Peacock 1990).

The effect of landscape features on species occurrence is believed to increase in strength with increasing trophic level (Davies et al. 2000, Kruess and Tscharntke 1994, 2000, Holt 2002, Thies et al. 2003). This is because the extinction of one trophic level breaks a specialist food chain and causes extinction of higher trophic levels, and sometimes because higher trophic levels are able to maintain smaller population sizes. For example, natural enemies (i.e. parasitoids) are restricted to plant patches occupied by herbivores and, as a consequence, usually more affected by size and isolation of host plant populations than herbivores (Kruess and Tscharntke, 1994; Lei and Hanski, 1997; van Nouhuys and Hanski, 1999; Kruess and Tscharntke, 2000). In a metapopulation with frequent extinctions and recolonisations, higher trophic levels may not be able track host populations perfectly and the probability of extinction at the metapopulation level will increase with trophic level. However, processes may not necessarily be that simplistic. Holt (2002) showed that the existence of a third trophic level can stabilize fluc- tuations at the first and second level, thereby even increasing possibilities of persistence of the intermediate level.

Plant-insect interactions

Plants interact with animals throughout their lifecycles. Evolution of mutualistic and antagonistic relationships shapes the morphology and physiology of all plants. Most ecosystems involve a tremendous diversity of interactions between plants and animals, interactions being direct or indirect. Seed predators constitute a special group of herbivores since they actually kill individual plants (in the seed stage); hence the term “predator”. For plant- seed predator interactions, an increasing number of studies have shown that not only bottom-up effects are important but that seed predators can have great influence on population dynamics and trait selection in their host plants (Kolb et al. 2007). For many years, studies have focused on pair-wise interactions, e. g. plant-herbivore, plant-pollinator or plant-disperser. More re- cently, however, several studies have demonstrated that community context can influence the outcome of pair-wise interactions (Strauss and Irwin 2004, Strauss et al. 2005). There is also a growing appreciation of that interactions are inherently variable over time and space. Over the last two decades ecologists have been trying to grasp more complex interactions and assess the importance of spatio-temporal variation (e. g. Price et al., 1980, Weis and Abrahamson 1985, Schmitz et al. 2000, Tscharntke and Hawkins 2002, Strauss and Irwin 2004). These undertakings have applied theoretical tools to trophic cascades (Paine 1980), geographic selection mosaics (Thompson

11 1994) and complex food webs (Polis and Strong 1996), as well as more powerful analytical tools.

Studies of tritrophic interactions were triggered by the search for biological control agents to manage insect pests (Price et al. 1980), although the debate on the relative importance of bottom-up and top-down control is older than that. Hairston et al. (1960) concluded that predator densities are affected mainly in a bottom-up fashion whereas herbivores are mainly limited by top- down control. Producers are left to compete for resources and this is why “the world is green”. This argument was later developed by Fretwell (1977) and Oksanen et al. (1981), suggesting that ecosystem productivity would limit the number of trophic levels. Ecosystem productivity should have a profound cascading effect on vegetation, the effect depending on whether the number of links is even (producers limited by grazers) or odd (producers limited by resources). The authors also pointed to several cases as supporting their theory. A central feature of these models was the important role of trophic “cascades”. An example of a trophic cascade is when the negative effect of predators on prey translates into positive effects on prey resources, in terms of plant abundance and distribution. Fretwells and Oksanens theory suggests a community-wide response affecting the vegetation type (for in- stance grasses or trees). Polis (1999) separated community-wide cascades from species cascades where only a few species are involved. The general conception is currently that community-wide classical trophic cascades affecting plant biomass are weak in terrestrial systems compared to aquatic (Strong 1992, Polis and Strong 1996, Shurin et al. 2002). Still, also in terrestrial systems cascades may often be important for individual species (Duffy 2002, Schmitz 2003 and 2006).

In this thesis I present results from studies on spatial and temporal variation in interspecific interactions related to the perennial forest herb Actaea spicata. I incorporate effects of other plants but mainly focus on plant-animal interactions. In the study area Actaea appears to interact with a limited number of animals. Pollination is predominantly by one beetle species, Byturus ochraceus (Pellmyr 1984) and pre-dispersal seed predation is only by larvae of one specialized moth species, Eupithecia immundata. Fruit dispersal (and to a certain extent post-dispersal predation) is, to a large extent, carried out by a guild of rodent species (Eriksson 1994), including Clethrionomys glareolus (bank vole) and Apodemus spp. (wood mice). Further, all animals interact with other species as well (e.g. the larval development of Byturus occurs on Geum urbanum) and there is ample scope for studies on food webs and multitrophic interactions in the system. I have focused on one tritrophic interaction, including seed predators and a guild of parasitoids on Eupithe- cia. Larvae of the seed predator are parasitized by at least four hymenopteran species and there is a potential for cascades from parasitoids to plants. I in-

12 vestigate how important the spatial configuration of Actaea populations is for these interactions and evaluate how landscape effects, such has habitat size and isolation, affect the complexity of communities, i.e. food chain length.

Questions asked in this thesis

In this thesis I ask the following main questions: How is a tritrophic interaction and the distribution of the involved organisms affected by patch size and isolation (Paper I)? Does fruit removal depend on local context of fruits sharing the same dispersers? (Paper II)? How does flowering phenology and number of flowers in the inflorescences affect seed production, seed predation and larval parasitism in a tritrophic system (Paper III)? What are the spatial and temporal dynamics, over four years, in a tritrophic plant-seed predator-parasitoid system, and how important are intertrophic processes (Paper IV)?

13 Methods

Study system

The basal resource for the study system is the plant Actaea spicata (Ranun- culaceae), (Fig. 2). It is a long-lived herb with a geographical range extend- ing through Scandinavia, central and Eastern Europe (Hultén and Fries 1986). The average life expectancy for plant surviving until blooming is 20.2 years, or 22.2 if the time from seed production until germination is included (Johan Dahlgren, unpublished data). The plant is a characteristic species in deciduous and rich coniferous forests in southern Sweden. Flowers are presented in conspicuous inflorescences from late spring to early summer. Most of the flowers appear at the primary inflorescences but a fraction of plants also present flowers sequentially in up to four later inflorescences. Later inflorescences are always smaller. One of the plants oddest features are the fruits, which are large, oval (roughly 1 cm diameter), fleshy, and black. The fruit type is unique to the genus Actaea within the Ranunculaceae family, and has given the species its Swedish name: Trollduva (“trolls grape”). The English name, Baneberry, refers to the toxicity of the fruits. The toxic fleshy fruits are a trait that the species share with several unrelated species found in the same habitats, e.g. Convallaria majalis (Convallariaceae), Polygonatum multiflorum (Convallariaceae) and Paris quadrifoila (Trilliaceae). Fruit set of Actaea is often 100% (Pellmyr 1984, Eriksson 1995). Ripe and intact fruits are attractive to rodents (Eriksson 1994) but dispersal is ineffective and often occurs over short distances. Many fruits remain in infructescences far into the autumn or, when dropped to the ground, remain unnoticed (HvZ, personal observation). Accordingly, 95% of the seedlings are found within 1 meter of an adult plant (Eriksson 1994). Germination is overall poor; less than 3% of seeds emerge as seedlings (Fröborg and Eriksson 2003). Pre- dispersal seed predation by the moth Eupithecia immundata is intense. In a seed addition experiment compensating for losses to seed predation, seedling emergence increased in deciduous forest populations but still, the overall effect of seed predation on population growth was found to be small while survival of established plants and transition between plant stages were more important (Fröborg and Eriksson 2003).

Figure 2 . An infructescence of Actaea spicata, in mid August, with mature fruits.

Eupithecia is the sole pre-dispersal seed predator on Actaea in the area. Ovi- position is restricted to a short period after flowering. One larva develops in each berry and leaves the berry through an exit hole in the middle of July – August. The moth is univoltine and completely specialized on Actaea. The species is categorized by the Swedish Threatened Species Unit as “vulner- able”. However, just like the host plant, it is very common in the study area. In the largest population, the estimated population size of larvae was about 30 000 all years from 2001 to 2004. Still, I have observed adults very rarely and oviposition only once. The ovipositing female spent a long time visiting several flowers on one inflorescence before parting.

In the study area, larvae of Eupithecia are infested by four hymenopteran parasitoids: Scambus buolianae (Ichneumonidae), Bracon sp. (Braconidae), and two Pteromalus spp. (Pteromalidae). Parasitoids oviposit into the devel- oping moth larvae, and the parasitoid larvae pupate inside the berries. I have observed oviposition of two of the species and on all occasions in July shortly before Eupithecia larvae complete their development, indicating that at least Scambus buolianae and Bracon sp. are univoltine. These two species are common and are possible to identify on the basis of pupal characteristics. The Pteromalus species, I have encountered rarely as developed adults inside berries from the largest populations. Some species of Pteromalus are known to be hyperparasitoids, which may be the case also for the species in this study system.

15 Study area

The field studies were carried out in the surroundings of Tullgarn, 75 kilo- meters SSW of Stockholm (58°6'N, 17°4'E, Fig. 1, paper I). The landscape is characterized by rich deciduous and mixed coniferous woodland fragments interspersed by pastures, meadows and arable land. The northern part has larger continuous forests, varying from relatively species-poor pine stands on sandy soils to richer spruce-dominated parts with a more diverse flora. The open areas in the agricultural landscape and variation in soil conditions in forested parts most likely creates dispersal barriers for Actaea and insects, resulting in suitable patches of habitat that varies in size and isolation in a matrix of unsuitable habitat. Hence, the study area is suitable for studies of the influence of spatial configuration on plant-animal interactions.

In the study area, more than 150 distinct populations of Actaea were found. Populations and habitats varied concerning forest cover, vegetation, light conditions, population size and isolation. The number of flowering individuals varied from zero to over 3000. However most populations were small, containing less than ten flowering individuals and less than 20 populations had more than 100 flowering individuals.

Data collection and aims of the different studies

During four consecutive years (2001–2004), I measured the intensity of seed predation and parasitization on Eupithecia in all plant populations. Up to 20 (30 in 2003) infructescences were examined in each population. I counted the number of fruits successfully attacked by Eupithecia (i.e. fruits with an exit hole), fruits containing a parasitized larva, fruits with a larva that had died from an unknown cause, and intact fruits. Plant population size was measured by the number of primary inflorescences. We calculated the proportion of fruits attacked, the proportion of Eupithecia larvae parasitized and mortality rates of Eupithecia, as well as Eupithecia population sizes. To test for edge effects, I sampled infructescences at the edge and in the interior of 50 plant populations in 2007. In 2005, ninety experimental sites were set up, within and outside Actaea populations, spread out over the study area to study effects of spatial context on fruit removal. All fruits were collected outside the study area and placed in five different treatments in each site. All sites were then revisited and number of fruits removed and consumed in the spot was recorded. In 2006, flowering phenology on 341 Actaea plants was recorded within five of the largest Actaea populations. I measured flowering phenology and the number of flowers in inflorescences. Later fruits from these plants were collected, seeds in intact fruits counted and presence of Eupithecia and parasitoids recorded.

16 Paper I – In this study I examined if spatial configuration of host plant populations affects tritrophic interactions (Actaea, Eupithecia and parasitoids). In 85 plant populations, I collected data on number of vegetative and flowering adults, seedlings, seed predation and parasitization. I tested if incidence patterns of insects were in accordance with the metapopulation theory. Based on the Fretwell-Oksanen model I developed a hypothesis for how the level of herbivory should be related to the size of plant populations in a specialized tritrophic system. The hypothesis is that the size of the basal resource determines food chain length. This, in turn will have cascading, top-down effects so that seed predation affects plant recruitment negatively and parasitization affects plants positively by reducing subsequent generations of the seed predator. Since the food chain length is expected to decrease with basal resource size the parasitoids should be present only in the largest plant populations. The seed predator, on the other hand, should be missing only from the smallest plant populations. This will result in a curvilinear and unimodal relationship between plant population size and level of seed predation.

Paper II – In this study I examined conspecific and heterospecific effects from neighboring plants on fruit removal. I asked whether surrounding plant abundance, and number and composition of fruits in aggregations affects removal and consumption of fruits. I recorded removal and in situ consumption of fruits from experimental plots of four species with fleshy berries attractive to rodents. The plant species were Actaea (the main study species) and, Convallaria majalis (Convallariaceae). Also kernels of Prunus avium fruits and acorns of Quercus robur were included. Fruits were placed in aggregations differing in composition (Actaea only vs. Actaea + other species), and size (number of fruits) in 90 sites, 60 within Actaea populations of varying size and 30 outside of existing populations. In the center of each site, separated by at least 10 m, 5 different plots were set up, containing; (i) 5 Actaea fruits, (ii) 15 Actaea fruits, (iii) 5 Actaea fruits + 10 Convallaria fruits, (iv) 5 Actaea fruits + 10 Quercus acorns and (v) 5 Actaea fruits + 10 Prunus stones. The experiment started in the middle of September and all plots were revisited at the end of the experiment in the middle of November.

Paper III – In this study I asked if flowering phenology and inflorescence size influence fertilization and seed set, seed predation, and parasitization of Eupithecia larvae. Flowering phenology (start date and duration of flowering) and flower number of a total of 341 inflorescences in five populations were recorded. Fruits were later collected, and checked for presence of Eupithecia larvae and parasitoids. Numbers of seeds in intact fruits were counted. Response variables, calculated per inflorescence, were average number of seeds in intact fruit, incidence and proportion of fruits preyed upon by Eupithecia, and incidence and proportion of Eupithecia larvae attacked by parasitoids. I also collected data on light conditions.

17 Paper IV – In this study I investigated how the same tritrophic interactions examined in Paper I vary over time and space and how species dynamics are influenced by intertrophic processes. I examined data on Actaea population size, number of seedlings, Eupithecia and parasitoid population sizes during four years, 2001–2004. Data on insect abundance and adult Actaea population size were recorded in all populations within the study area. I also carried out an experimental test of Eupithecia recolonization ability, to serve as a basis for computing connectivity measures. Lastly, I recorded insect abundance at edges and in centers of plant populations.

18 Results and Discussion

Paper I – Effects of resource population size on insect distribution at two trophic levels

Resource population size and connectivity had important effects on the incidence of the seed predator Eupithecia as well as its parasitoids. Food chain length in the plant-seed predator-parasitoid system was determined by its basal resource, Actaea population size. Eupithecia was missing from only a few of the smallest plant populations while parasitoids were missing from many of the small and intermediate sized Actaea populations. I could not detect any effect of connectivity on insect incidences. Seed predation rate was curvilinearly and unimodally related to Actaea population size, a pattern that supported our hypothesis. Further, Actaea populations with intense seed predation had fewer seedlings per adult than populations with low seed predation.

Paper II – effects of plant and fruit abundance on fruit removal by rodents

Presence of fruits from other species belonging to the same dispersal syndrome significantly increased fruit removal of Actaea. Removal of fruits from Actaea and removal of the other species fruits were correlated within sites and removal rates were higher from large than small aggregations of fruits. Fruits from the other species enhanced removal in the same way as conspecific fruits. Fruit removal was higher within than outside Actaea populations. Among existing Actaea populations, removal was not related to plant abundance. Hence, I found experimental evidence of heterospecific effects on removal by shared dispersers. I conclude that the biotic context on a small scale is important, presumably because of rodent search behavior. I found large variation in removal rates between sites, but correlations between plant species within sites. This suggests that there are “hot spots” for dispersal related to unknown factors.

19 Paper III – seed set and insects in relation to flowering phenology and inflorescence size

Seed set, seed predation and parasitization were not related to start or duration of flowering. Seed set, and incidence of the seed predator Eupithecia, increased with increasing flower number while the increase in incidence of parasitoids on the Eupithecia was only marginally significant. The proportion of fruits preyed upon was not related to inflorescence size, implying that attack risks on individual fruits are not higher in large inflorescences. There was a tendency for a higher parasitization rate, i.e. proportion of Eupithecia larvae attacked, with increasing number of flowers. Parasitization rate was also clearly positively related to number of Eupithecia larvae within inflorescences. Hence, parasitoids seem to be able to aggregate on large occurrences of its resource, whereas Eupithecia does not. Taken together, these results suggest that there may be selection for larger inflorescences. A higher number flowers gives more fruits, more seeds per fruit and possibly higher parasitization rate of the seed predator (which means more intact seeds attacked fruits), while the proportion of seeds lost to predation is not affected.

Paper IV – dynamics of three trophic levels over four years

Incidences of both Eupithecia and parasitoids were positively related to their respective resource size in all years. Extinctions were negatively and colonizations positively related to resource size, creating the observed incidence pattern. Effects of patch connectivity for immigration into new patches were established for Eupithecia in several ways. Connectivity affected colonization into new patches in the natural patch system. Further, it significantly predicted colonization rate in an experiment. Lastly, it was evident as a rescue effect where small populations were sustained by nearby large populations. However, I found no evidence of an effect of connectivity for parasitoids.

A curvilinear relationship between seed predation and plant population size was found in three of four years. Average seed predation in small Actaea populations was low, probably due to higher demographic stochasticity in both host plant and seed predator populations. Maximum seed predation level attained decreased for the largest populations. However, I did not find clear evidence that this pattern was the result of parasitoid attacks; high parasitoid-induced larval mortality in one year was not associated with lower seed predation the following year. However, parasitization does seem to be able to drive small Eupithecia populations to local extinction. Lower levels of seed predation in large Actaea populations appeared to be related to that the moth preferentially oviposits at patch edges, relaxing seed predation

20 intensity in population interiors. Due to a decreasing proportion of plants situated near edges in larger populations this should result in lower average intensity of seed predation. Variation in seed predation translated into effects on plant recruitment in one of three years. After removing effects of predation, recruitment was positively related also to Actaea population size. My interpretation is that this can be attributed to generally more suitable environmental conditions, rather than improved outcrossing. One conclusion is that Eupithecia can be a limiting factor for population growth in intermediate-sized Actaea populations in which seed predation rates are consistently very high. The study also shows that spatial context is important for three trophic levels considered, and that affects at one level cascade to the other levels.

21 Concluding remarks

Spatial configuration of habitat patches had important effects on community complexity and the outcome of species interactions in Actaea spicata in the study area. On a larger scale, food chain length in the plant-seed predator- parasitoid system was determined by basal resources, in terms of host plant population size (Paper I, IV). Further, rodent consumers/dispersers were more likely to find fruits within, than outside Actaea populations (paper II). At a smaller scale, there was a patch edge-effect on pre-dispersal seed predation (Paper IV) and an effect fruits aggregation size in the fruit removal experiment (Paper II). Individual seed mass and total seed mass within fruits were not related to plant population size (Paper I). On the other hand, seedling emergence was strongly positively related to adult abundance (Paper IV). Fruit removal was unaffected by Actaea population size. Hence, plant population size appears to have weaker effects in the Actaea-rodent interaction than in the Actaea-Eupithecia interaction. This makes sense biologi- cally, since Eupithecia larval development is completely specialized on Ac- taea whereas the plants fruits make up a small and dispensable resource for any rodent species.

The study of the tritrophic Actaea-Eupithecia-parasitoid system (Paper I, III and IV) revealed several interesting aspects on how spatial configuration influences intertrophic dynamics. Both resource size and connectivity (in the case of Eupithecia) had an effect on insect occurrence. In paper I, I sug- gested that parasitization relaxed the pressure from Eupithecia on Actaea in large populations by reducing subsequent moth populations. I was confident in this interpretation since parasitoids caused considerable larval mortality. Further I saw indications (Paper I, Fig. 2) that plant populations with parasitoid incidence had consistently lower seed predation rate than other plant populations of similar size. However, this just goes to show the problems with inferring processes from patterns. Indeed, parasitization was positively related to extinction risk of small Eupithecia populations. Apart from that, analyzing the dynamics of the system in the four-year study did not provide evidence of that parasitization rate had an overall negative effect on seed predation in Actaea populations in the following year. The explanation for this apparent contradiction may be associated with that large plant populations are different from small not only in that they constitute a larger re-

22 source base and can support longer food chains. They also differ concerning the relationship between edge and interior; the larger the patch the smaller the proportion of host plants situated near the edge. The results from 2007 (Paper IV) shows that plants at edges were more likely to be attacked by a seed predator than plants in the interiors. I also saw that this effect was more pronounced in larger populations, presumably because there is little distance between edge and interior in smaller populations. These results make the system very similar to the one presented by Elzinga et al. (2005), with the only difference that their seed predator was not missing from small populations. I also collected within-patch data in 2003 and 2004 (HvZ, unpublished data) which showed that seed predation was positively related to plant density (distance to nearest neighbor), but only in large populations. This is likely to be the same, or at least a similar, effect as in the edge/interior study since large populations in general probably are denser at the edges. Parasiti- zation did not differ between edges and interiors. Still, I found that parasitoids aggregated on large occurrences of Eupithecia larvae at the level of plant individuals. It is possible that this aggregation is the result of the parasitoids ability to recognize Eupithecia larvae only from a limited distance. On a larger scale parasitoids do not, like Eupithecia, aggregate at plant (and Eupithecia) population edges. Overall, I have found effects of metapopulation dynamics, intertrophic dynamics and search behavior on the distribution of insects, among and within patches. The spatial configuration of Actaea patches is the principal predictor of Eupithecia incidence and abundance. However, on a smaller scale and for the effect on Actaea, individual plant localization within patches is also important. For recruitment in small Actaea populations parasitoids can also be of tremendous importance, causing extinctions of Eupithecia populations and chances for recruitment in certain season in plant populations that are otherwise often subject to intense seed predation.

In large plant populations, the effects of parasitoids appear not to cascade down to the plant level. A higher larval mortality due to parasitization may be compensated for by the female moths’ ability to produce many eggs or by immigration from other patches. Instead, Eupithecia populations are mainly influenced by resource availability (the number of fruits) and geometry (edge vs. interior) of the plant patch. In small and isolated Actaea populations, Eupithecia is often missing or present in small numbers. This is probably due to extinctions related to demographic stochasticity in both host plants and seed predators, immigration effects related to patch size, but also parasitoids ability to drive local Eupithecia populations, and thereby also themselves, to extinctions. Hence, insects populations of two trophic levels are maintained in small Actaea patches through recurrent extinctions and recolonizations, and the seed predator metapopulation can escape its natural enemy by its ability to disperse more efficiently among small patches. In a

23 system with a lower dispersal rate of the seed predator, due to a poorer dispersal capacity or a more fragmented landscape, one should expect a lower incidence of both the seed predator and its parasitoids. In fact, one should expect the same with more dispersive parasitoids.

Seed predation frequently damaged more than 80% of seeds within populations. There were also significant or marginally significant negative effects of seed predation on plant recruitment in two of three years. Seedling emergence in Actaea is very low, dispersal is ineffective and interspecific competition intense (Fröborg and Eriksson, 2003). Losses to seed predation may therefore not necessarily result in a proportional loss in seedling recruits. Nevertheless, our results suggest that recruitment is limited by seed predation in some years, which makes it likely that seed predation affects plant population dynamics in the long run. Another factor that is known to affect recruitment is the removal and transportation of fruits and seeds into favor- able microsites (vander Wall 2003). In Actaea, removal rate was unrelated to Actaea abundance among existing populations. I did, however, find an effect at a smaller, inside patch, scale. Fruit removal was enhanced in the presence of other fruits and the effect was similar for conspecific and heterospecific fruits. Presuming that removal overall is beneficial for plant dispersal and recruitment, Actaea plants benefit from growing together with other species sharing the same dispersal syndrome, such as Convallaria majalis, Paris quadrifolia and Polygonatum multiflorum. All these four species are often found in the same habitat and they all have large fleshy fruits. If, as it seems, these species are attractive to the same rodent species, then animal dispersal is one factor that may promote coexistence. One positive effect of fruit removal that is inherently difficult to quantify is an increased probability of dispersal to, and colonization of, unoccupied habitats. Since, fruit removal was independent of Actaea abundance and average seed predation is lowest in the smallest Actaea populations, probability of dispersal into new habitats, on a per plant basis, may actually be higher from small Actaea populations. Still, connectivity of populations may be most important in this respect.

To summarize, this thesis shows that spatial configuration, on small and large scales, affects community complexity and importance of interspecific interactions. I have demonstrated ecological effects of population size and connectivity on species occurrence and abundance. Several trophic interactions are important for Actaea and these interactions can be affected by a third trophic level or other species at the same trophic level. Almost all trophic interactions related to Actaea were influenced by plant population size, and for several of them also spatial differences within population are important. Hence, Actaea plants belonging to populations of different size, or standing in different parts of one patch are links in qualitatively different trophic webs.

24 Acknowledgement

I am grateful to Johan Ehrlén, Ove Eriksson and Didrik Vanhoenacker for valuable comments on this text.

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29 Svensk sammanfattning

Hur landskapets utformning påverkar biodiversitet och förekomst av olika arter har intresserat forskare och ekologer en längre tid. Arters förekomst beror inte bara den lokala miljön. Det är också av yttersta vikt hur stora habi- taten är och hur de är placerade i relation till varandra. En art kan saknas på en plats, som har alla miljömässiga krav, bara föra att platsen är för liten eller ligger för långt ifrån andra förekomster av arten. Habitatens yta och isolering påverkar chansen att arter ska kunna kolonisera platsen och risken att dö ut. Landskapets utformning kan också påverka hur, när och var olika organismer interagerar med varandra. De flesta arter har åtminstone en hand- full arter som de interagerar med, som mutualister eller antagonister. Habita- tens rumsliga fördelning påverkar vilka av dessa arter som finns i ett område. Denna avhandling handlar om dessa rumsliga mönster av interaktioner mellan arter.

Jag har i mina studier utgått från växten trolldruva, en långlivad ört som är relativt vanlig i lövskogar och rika barrskogar i södra och mellersta Sverige. Fältstudierna gjordes i området runt Tullgarns slott i Södermanland. Troll- druvan är där lokalt mycket vanlig, jag har funnit omkring 150 enskilda populationer. Några av dem är väldigt stora (den största har mer än 3000 blommande trolldruvor) men de flesta består endast av ett fåtal individer. Landskapet består till stora delar av ett jordbrukslandskap med inslag av skogsklädda kullar och impediment. Bland dessa finns trolldruvepopulationer, som varierar i storlek och i grad av isolering. I området finns en nattfjä- ril, Eupithecia immundata (oren malmätare), en fröpredator vars larver är helt specialiserade på trolldruva och har sin utveckling inuti trolldruvans frukter. Arten är nationellt ovanligt men lokalt mycket vanlig. Fjärilens larver attackeras i sin tur av ett antal arter av parasitoidsteklar, varav två är vanliga. Dessa attackerar larverna inuti frukterna och larverna lever sedan av Eupithecia-larven, som dör varefter stekellarverna förpuppas inuti trolldruvans frukt.

I artikel I undersökte jag förekomst av Eupithecia och parasitoider i trolldruvepopulationerna. Jag fann att förekomsten av arterna var starkt relaterat till respektive värdorganisms populationsstorlek. Eupithecia saknades endast i några av de minst trolldruvepopulationerna. Parasitoiderna i sin tur saknades

30 från en stor del av de mindre Eupithecia-populationerna. Följden av detta var att antalet arter i näringskedjorna till stor del bestämdes av basresursens, trolldruvans, förekomst. Endast i de största och några av de mellanstora växtpopulationerna fann jag alla tre nivåerna. Eupithecia visade sig ofta kunna förstöra en mycket stor andel av trolldruvornas frön. Även parasitoiderna visade sig ha en stor effekt på Eupithecia, i vissa populationer dödades en stor del av larverna genom dessa parasitoidangrepp. För trolldruvan fann jag att andelen frön som prederades var kurvilinjärt relaterat till trolldruve- populationens storlek. I genomsnitt förstördes den största andelen frukter i mellanstora populationer, medan en större andel undgick angrepp både bland de små och bland de riktigt stor växtpopulationerna. Jag tolkade detta som att parasitoiderna hjälpte trolldruvan i de största populationerna genom att öka dödligheten bland larver och på så sätt minska storleken på kommande generationer av Eupithecia. De låga genomsnittliga nivåerna av fröpredation i små populationer tolkades som en effekt av att Eupithecia inte lyckas kolonisera dessa, och dessutom högre risk för utdöende p.g.a. små populationsstorlekar.

I artikel II undersökte jag hur smågnagare sprider trolldruvans frukter. Jag ville se om möjligheterna för trolldruvan att sprida sina frön påverkas av hur stor trolldruvepopulationen är. Även om inga gnagare är helt beroende av trolldruvans frukter kan de förväntas utgöra en viktig resurs under höst och vinter. Gnagare skulle kunna leta mer efter dessa frukter där dessa är vanli- gast eftersom det kan vara mer effektivt att koncentrera sig på några få typer av föda än att leta efter allt samtidigt. I området finns även andra växter som liksom trolldruvan har stora och köttiga frukter som antas vara attraktiva för samma arter av gnagare. Jag ville därför testa om förekomsten av liljekonvalj, ormbär och storrams påverkade spridningsframgången hos trolldruva. Under studien placerades frukter av dessa olika arter ut i en antal olika kom- binationer på 90 områden med varierande förekomst av trolldruva och de andra arterna. När jag sedan analyserade från vilka ställen frukter hade av- lägsnats kunde jag utskilja några intressanta mönster. Andelen frukter som försvann under försöker varierade kraftigt mellan försöksområdena, men på en mindre skala, inom områdena, var avlägsnandet starkt korrelerat. Fler frukter hämtades från försöksplatser inom trolldruvepopulationer än utanför men bland dessa verkade det inte spela någon roll hur stor trolldruvepopulationen var. Frukter hade lika stor chans att plockas bort från en liten som från en stor trolldruvepopulation. Jag fann också att frukter hade större chans att plockas från stora fruktsamlingar än små. Intressant nog spelade det ingen roll från vilka av arterna de andra frukterna i samlingen kom. En trolldruve- frukt plockades alltså med större sannolikhet bort ifall den låg tillsammans med liljekonvaljfrukter än om den låg ensam. Slutsatsen från studien var att såväl storskaligt som småskaligt sammanhang påverkade fruktspridningen

31 och förekomst både av den egna arten och även andra inverkade på chansen att plockas bort.

För artikel III återvände jag till Eupithecia och parasitoiderna. Jag hade tidi- gare konstaterat ett rumsligt mönster där fler frukter undgår predation i stora trolldruvepopulationer. Jag hade även noterat att hela blomställningar i dessa ofta undgick angrepp. Frågan jag ställde mig var om blomningsfenologin (vid vilken tidpunkt en blomställning går i blom och hur länge den blommar) samt blomställningens storlek (antalet blommor) kan påverka vilka plantor som angrips. Samtidigt ville jag se om dess faktorer påverkar frösättningen (antal frön per frukt) och även parasitoidangrepp. Blomningsfenologi visade sig inte vara relaterat till någon av de variabler jag mätte. Frösättningen var däremot positivt relaterad till blomantal. Risken för angrepp av Eupithecia i någon av frukterna ökade med blomantal men andelen angripna frukter på- verkades inte. Vad det gäller parasitoidangreppen fanns en tendens till att andelen parasiterade Eupithecia-larver steg med ökande blomantal. Andelen parasiterade Eupithecia-larver var samtidigt tydligt relaterat till antalet larver i blomställningen. Slutsatsen av denna studie är det kan förekomma selektion för större blomställningar. Dessa får nämligen fler frukter, fler frön per frukt och möjligen även en större andel parasitangrepp på Eupithecia. Sedan tidi- gare har det visat sig att fler frön förblir intakta i frukter där Eupithecia- larven parasiterats.

Avhandlingens sista artikel är en flerårsstudie av systemet jag undersökte i artikel I. I artikel IV kan jag till stora delar slå fast de mönster som kom fram i artikel I samt även analysera processerna bakom dessa mönster. Före- komstmönstren visade sig uppkomma genom att såväl kolonisationer och utdöenden av Eupithecia och parasitoider var kopplade till deras respektive resursers populationsstorlekar. I små populationer av värdorganismer var koloniseringar mindre, och utdöenden mer sannolika. Eupithecia visade sig även på flera sätt påverkas av habitatens isolering. Det påverkade chansen till nykolonisering i trolldruvepopulationer. Vidare hölls små populationers storlekar upp av närliggande stora populationer. Fröpredationen visade sig påverka nyrekryteringen av groddplantor i trolldruvepopulationerna negativt. Det kurvilinjära sambandet mellan fröpredation och trolldruvepopulationernas storlek återkom i 3 av 4 år. Låga genomsnittliga angreppsnivåer kunde kopplas till små Eupithecia-populationers ökade risk för utdöende. Detta späs på ytterligare av att alla adulta trolldruveplantor inte blommar varje år. I en liten trolldruvepopulation kan Eupithecia-populationen dö ut för att det under en säsong helt enkelt inte produceras några frukter. Jag kunde även visa att parastoidangreppen påverkar utdöenden i små Eupithecia- populationer. Däremot kunde jag i stora trolldruvepopulationer inte se nå- gon effekt av parasitering. Hur stora angreppen än var på Eupithecia- populationerna påverkade detta inte fröpredationen påföljande år. Alltså

32 måste den generella trenden med lägre fröpredation i stora trolldruvepopulationer bero på något annat. Det visade sig vara kopplat till geometriska för- hållanden i trolldruvepopulationerna. Äggläggningsbeteendet hos Eupithecia gör att graden av angrepp blir högre i trolldruvepopulationernas kanter en i deras centra. Riktigt vad detta beteende har sin grund i är för Eupithecia okänt men det finns flera teorier om varför kanteffekter uppstår och liknande mönster har hittats i andra studier. Följden för trolldruvorna blir att an- greppsgraden sjunker när andelen av kantzon i populationen sjunker. Små populationer har ju, per definition, ingen del som inte är kantzon medan andelen av denna minskar ju större populationerna blir. Slutsatsen blir att populationer som är så stora att Eupithecia-populationerna inte dör ut, men tillräckligt små för att fortfarande bestå mest av kantzon, kan påverkas mest negativt av fröpredation.

För att summera, i avhandlingen visar jag att rumsligt sammanhang, i liten och stor skala, påverkar samhällens komplexitet och hur arter interagerar med varandra. Jag har visat på ekologiska effekter av populationers storlek och isolering på arters förekomst och abundans. För trolldruva är ett antal interaktioner mellan arter på flera olika trofinivåer viktiga, och dessa kan påverkas både av en tredje trofisk nivå (parasitoiderna) och också av andra arter inom samma trofinivå (liljekonvalj till exempel). Nästan alla interaktioner relaterade till trolldruva, påverkas av växtens populationsstorlek, och i flera avseenden är även rumsliga skillnader inom populationerna viktiga. Sålunda är trolldruveplantor som växer i populationer av olika storlek, eller i olika delar inom en population, länkar i kvalitativt åtskilda födovävar.

33 Tack

Ett stort tack till mina handledare Johan och Ove. Jag har alltid lämnat våra möten med lättare steg än de jag kommit med. Tack Johan, för att du har tagit dig tid och varit fenomenal på att hitta nya infallsvinklar när jag kört fast eller när mina resultat tyckts intetsägande. Tack Ove, för att du är så in- i-vassen effektiv och pragmatisk. Det låter kanske torrt men jag uppskattar verkligen din förmåga att alltid se och välja den enklaste vägen framåt, både i forskningen och i annat. Inte minst är jag tacksam för att jag kunde hyra rum på mittuniversitet under det sista året.

Jag startade doktorerandet samtidigt som Didrik och då gick även startskottet för en evolutionärt ekologisk studiecirkel i rum 539. Den fick sedermera välkommet besök av Mathias. Och Karin hade inget val. Vi har haft väldigt många idéer även om dessa sällan kom nära att formuleras som en forskningsplan. En del kom längre, någon drog till och med iväg mig, Didrik och Mathias till Väddö (punktering) och Eskilstuna (konstaterande att vissa tydligen kan förväxla olvon med berberis). Jag tror även att jag utvecklade mitt ekologiska och pedagogiska tänkande så långt det någonsin var möjligt. Tack Mathias och Didrik, det var förbaskat roligt! Tack Karin för att den tid du var med och diskuterade och… tja, stod ut med oss :).

Denna tid var över när jag flyttade till Sundsvall och den definitiva slutpunkten för doktorerandet är förstås denna avhandling. Den hade varit mycket svårare att få ihop utan Didrik, ekologiskt orakel, statistiskt geni och hyvens hjälpsam kompis i samma person. Tack! Stor hjälp har jag även fått från Johan D, Mathias och Micke. I fält och på labb har jag också fått hjälp av Paula Jokela, Samira Englund, Anna Weise och Mia Bengtsson. Tack Leena, Annette, Katariina och Hannah för pepp inför snack på konferenser. Tack Leena för alla tips i slutfasen. Jag har också uppskattat att snacka fotboll och andra, nästan lika allvarliga, ämnen med Micke och Mathias. Tack alla tullbotorpare, det är trevligare där när man inte är ensam. Ett stort tack också till Didrik och Petra med familj för alla övernattningar!

Och så tack alla andra som har varit med, doktorander, forskare, assistenter, ex-jobbare, och förgyllt fikaraster, innebandy, fester, kurser, konferenser och resor. Mallorca var en höjdarresa som jag sent ska glömma! Andra självklara höjdpunkter har BioGeos kurs på tovetorp i juni varit. Tack Lenn och Didrik för allt skoj vi har haft och allt jag lärt mig där.

Slutligen, tack kära familj. Nu Jenny, Irma och Molly, nu kommer jag ut ur bubblan.