Survey
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
Plant-seed predator interactions – ecological and evolutionary aspects Hannah Östergård Stockholm University ©Hannah Östergård, Stockholm 2008 Cover: Flowering Lathyrus vernus and mating pair of the predispersal seed predator Bruchus atomarius. Photo: Hannah Östergård ISBN (978-91-7155-643-1) Printed in Sweden by Universitetsservice, US-AB, Stockholm 2008 Distributor: Department of Botany, Stockholm University Till Kim och Märta. - Ett frö! - Vadå för ett frö? - Vadå för ett frö? - Ett busfrö! Doctoral dissertation Hannah Östergård Department of Botany Stockholm University SE-106 91 Stockholm Sweden Plant-seed predator interactions – ecological and evolutionary aspects Abstract - Plant-animal interactions are affected by both abundance and distribution of interacting species and the community context in which they occur. However, the relative importance of these factors is poorly known. I examined the effects of predator host range, environmental factors, host plant populations, plant traits and fruit abortion on the intensity of predispersal seed predation in 46 host populations of the perennial herb Lathyrus vernus. I recorded damage by beetle pre-dispersal seed predators, mainly Apion opeticum and Bruchus atomarius with different host ranges on L. vernus as well as on two additional host plants. Local seed predator population size was mainly influenced by plant population size, current seed production and beetle population size in the previous year, but was not strongly affected by connectivity. The monophagous seed predator was less abundant and had lower densities than the oligophagous. Both predator species had a strong ability to track fluctuations in seed production; intensity of predation increased with relative increases in seed production. Oligophagous predation on L. vernus increased with the abundance of alternative hosts, but presence of L. vernus did not affect predation on alternative hosts. Abundances and trait preferences differed among three co-occurring seed predators, but were also associated with the abundance of the other species. Overall, seed predation influenced selection on flower number. I found clear indications of seed predator offence but no obvious plant defence. The pattern of fruit abortion was associated with reduced plant fitness since the seed predator had an advanced ability to locate fruits with high probability of retention. Taken together, different factors influencing abundance of the seed predator species, different preferences, and context dependent trait selection are likely to result in complex spatio-temporal variation in overall seed losses and trait selection in the common host plant. Keywords – apparent competition, community context, fruit abortion, defence, host range, monophagous, offence, oligophagous, plant-animal interactions, pre-dispersal seed predation, selection, spatio-temporal variation List of papers The thesis is comprised by a summary and four papers, which are referred to by their Roman numerals: I Östergård, H., and J. Ehrlén. 2005. Among population variation in specialist and generalist seed predation - the importance of host plant distribution, alternative hosts and environmental variation. Oikos 111:39-46. II Östergård, H., P. A. Hambäck, and J. Ehrlén. Regional dynamics and host plant utilization by two pre-dispersal seed predators. Manuscript. III Östergård, H., and J. Ehrlén. Phenotypic selection pressures on Lathyrus vernus by a monophagous, an oligophagous and an occasional seed predator. Manuscript. IV Östergård, H., P. A. Hambäck, and J. Ehrlén. 2007. Pre-dispersal seed predation: The role of fruit abortion and selective oviposition. Ecology 88:2959-2965. Previously printed and accepted papers are reprinted in this thesis by the kind permission of the copyright holders. Contents Introduction .....................................................................................................7 Ecological aspects ........................................................................................................8 Evolutionary aspects .....................................................................................................9 Aim of the thesis............................................................................................11 Methods ........................................................................................................12 Study system ..............................................................................................................12 Data collection ............................................................................................................13 Data analysis ..............................................................................................................15 Results ..........................................................................................................18 Discussion .....................................................................................................20 Concluding remarks ....................................................................................................22 Acknowledgements .......................................................................................23 References ....................................................................................................24 Svensk sammanfattning................................................................................28 Tack...............................................................................................................32 Introduction Plants are generally involved in multiple mutualistic and antagonistic interactions, which may occur simultaneously or be separated in time, and may affect one or several plant organs or different stages of the lifecycle, i.e. reproductive organs, seeds or seedlings. Both mutualistic and antagonistic interactions between plants and animals have important and sometimes reciprocal effects. Herbivory is an antagonistic interaction displaying a wide variety of forms. Pre-dispersal seed predation deviates from other kinds of herbivory in several important aspects, such as the discrete packaging of the resource, time-limited access to the seeds and the higher variation in resource production as compared to other plant resources. Another aspect is that the interaction between plant and pre-dispersal seed predator generally takes place during or in close proximity to the flowering period. Thus, predispersal seed predators are often active during the same period and attracted to the same features as pollinators, causing conflicting selection pressures in the plant. Different species utilizing the same resource may vary in host range. In spite of the obvious advantages of utilizing multiple hosts, herbivorous insects are often specialized on one or a few host plants. The evolution of specialization in herbivorous insects is suggested to be a trade-off between adaptations to a particular host trait and the ability to utilize multiple hosts (Jaenike 1990, Thompson 1994, Agrawal 2000). The commonness of specialization has been explained by the information-processing hypothesis, stating that the limited neural capacity in an insect should gain in efficiency on a narrow host range since they only need to respond to a few cues in searching for host plant (Levins 1969, Janz and Nylin 1997, Bernays 1998, Egan and Funk 2006). In addition, specialists that have overcome a plant chemical defence may also improve the search accuracy by utilizing the defensive chemicals as an attractant in host finding (Van Zandt and Agrawal 2004, Lankau 2007). A generalist, on the other hand, would suffer in effectiveness by having to screen multiple stimuli from their various hosts, but also have a reduced need of increasing efficiency. Pre-dispersal seed predators with different host ranges, from monophagous to polyphagous, and the intermediate oligophagous species, may have differential effects on the plant due to differences in abundance or preference. To understand population dynamics and plant trait evolution it is therefore necessary to identify the factors that determine the strength of these 7 interactions. This thesis examines the antagonistic interaction between a perennial herb and its beetle pre-dispersal seed predators in a spatial, temporal and evolutionary context. Ecological aspects The spatial distribution of species is generally patchy and patchiness is found over both small and large scales in the global distribution of a species. On the landscape level, the incidence and abundance of herbivores have often been studied within the theoretical framework of metapopulation theory. Metapopulation theory predicts that animal populations will more often go extinct in small host plant populations and will colonize more isolated host patches less frequently (Levins 1969, Hanski 1998, 1999). Such effects of spatial and temporal variation in resources will most likely have different impacts on different herbivores because resource-tracking in time and space will be the result of species specific behavioural and population processes (Hambäck and Englund 2005). From the plant perspective, variation in the abundance and species composition of seed predators will result in variable effects on local population dynamics. Reductions in plant reproductive output and subsequent fitness losses by pre-dispersal seed predation has been observed in several systems (Louda and Potvin 1995, Traveset 1995, Ehrlén 1996). The impact of seed predation on plant population dynamics may depend on whether recruitment is seed- or microsite limited. When seed densities are low, seed predation may reduce recruitment but as seed densities increase, recruitment will be limited by microsites or density dependent regulation of seedling survival and impacts of seed predation may therefore be lower (Crawley 1992). However, persistent reductions of seeds may, via reduced accumulation of seeds in the seed bank, have considerable effects on mean abundance even if recruitment is microsite limited (Maron and Kauffman 2006). The long-term intensity of seed predation can in some plant species be reduced by synchronized irregular variation of seed production, i.e. mast seeding (Kelly 1994, Silvertown and Charlesworth 2001). From the animal perspective, the spatio-temporal variation of resources will affect the distribution and abundance of herbivores (Bach 1988a, b, Turchin 1991). In some systems also higher trophic levels have effects on herbivore density (Elzinga et al. 2005, von Zeipel et al. 2006). Search behaviour and the relevant scales in resource tracking may vary due to what cues herbivores use and their efficiency in using those cues (Kunin 1999). Host plant clustering will cause different responses depending on whether an animal uses visual or olfactory cues. The relative probability of an individual host being targeted by visual cues may decrease with aggregation of hosts because single individuals will be less conspicuous within a cluster. When 8 olfactory cues are used the effects of clustering may be the reversed because increased aggregation increases detection distances (Cain 1985, Kunin 1999). Herbivores will also respond differently to host patch size and density depending on whether they are active or passive dispersers and whether they are poor or effective dispersers. Active dispersers may respond more to patch edges whereas passive dispersers will be most affected by patch area. Poor dispersers are more affected by distances among resource patches than good dispersers. Interactions between plants and consumers are also likely to be influenced by host range of the consumer since specialist species are completely dependent on their one food source whereas more general feeders have the possibility to alter between hosts. This will have consequences both for regional and local population dynamics since specialist feeders are more prone to go extinct as their single resources decrease, as well as being more severely affected by fragmentation of host populations than generalists (Zabel and Tscharntke 1998, Östergård and Ehrlén 2005). Host range will thus affect the spatio-temporal variation of coexistence of multiple interactors causing local variation in predation intensity. Evolutionary aspects The fitness and population dynamics of herbivores will largely depend on the ability of insects to track the resource and select suitable oviposition sites (Ehrlich and Raven 1964, Thompson and Pellmyr 1991). Search behaviour will have consequences both for seed predator dynamics and for the smallscale choice of oviposition sites. The negative effects experienced by the plant of an antagonistic interaction have resulted in the evolution of various defensive strategies of plants. Plants may reduce attack rates in several ways, i.e. by producing poisonous or deterring chemicals, avoidance traits, abscising damaged parts or by hiding in time or space (Augner et al. 1991, Augner 1994, Eriksson 1995, Wilson and Addicott 1998, Tiffin 2000). The evolution of flower and fruit abscission patterns may depend on whether they are the result of selection to decrease losses from predation or a result of that the resources available for fruit development are partly unknown at the flowering and fruit initiation stages (Lloyd 1980). Not uncommonly, antagonist insects outwit plant defences since their shorter generation time results in a higher evolutionary potential (Toju and Sota 2006). Antagonists are likely to exert selective pressures not only on plant defences but also on nondefensive plant traits as a result of their choices and preferences among different plant individuals (Brody 1992, Herrera et al. 2002, Leimu et al. 2002, Cariveau et al. 2004). Many of the floral traits in plants that are attributed to attracting pollinators (Thompson and Pellmyr 1989, Eckhart 1992, Herrera 1993, Brody and Mitchell 1997) will also attract antagonists. Thus, the optimal trait values are often the result of a trade-off between benefits by in9 creased pollination and costs by increased herbivory (Brody 1992, Brody and Mitchell 1997, Ehrlén 1997, Strauss 1997, Vanhoenacker et al. 2006). Coevolution is the reciprocal evolutionary change in interacting species and spatial variation in these interactions forms the basis for geographic mosaics of coevolution (Thompson 1994, Gomulkiewicz et al. 2000). In natural systems interactions between plants and insects are rarely a simple affair within a single pair of species, but will mostly occur within the context of other interactions experienced by the plant as well as by the insect. An interaction will depend on context because it is influenced, directly or indirectly, by both the number and intensity of other interactions (Johnson and Stinchcombe 2007). Indirect selection on plant traits, caused by contextdependent intensity of interactions, is suggested to result in a diffuse rather than pairwise coevolution (Janzen 1980, Thompson 1994, Strauss et al. 2005, Agrawal et al. 2006, Morris et al. 2007). However, the complexity of interactions is more than diffuse evolutionary responses. On the contrary, it offers an exciting challenge to detect and understand an interaction within its relevant context. The abundance and composition of the interacting insect community is often highly variable in time and space. The spatio-temporal variation in the context of a plant-animal interaction will thus translate into a mosaic variation of selection among different plant populations. 10 Aim of the thesis The overall aim of this thesis was to investigate how variation in the intensity of plant-animal interactions is affected by the spatio-temporal variation of resources and environmental conditions within the framework of host range, community context and plant trait variation. I used a system with one focal host plant the perennial understory herb, Lathyrus vernus, two alternative host plants, Lathyrus linifolius and Vicia sepium, and three pre-dispersal seed predators, the monophagous Apion opeticum, the oligophagous Bruchus atomarius and the more polyphagous Tychius quinqepunctatus only occasionally attacking L. vernus. The interactions were studied both within and among plant populations. Specifically I asked the following questions: (1) Is the intensity of pre-dispersal seed predation affected by spatio-temporal variance in host plant population size, seed production, connectivity and local environmental factors and does the relative importance of those factors differ with host range (Paper I & II)? (2) Do seed predators, species by species and in combination, change trait selection gradients in their host plant, and what are the underlying mechanisms of such changes (Paper III)? (3) How is the relationship between seed predator offence and plant defence related to the production of flowers, young fruits and the pattern of fruit abortion in individual plants (Paper IV)? 11 Methods Study system The long-lived perennial understory herb Lathyrus vernus has a Eurasian distribution (Hultén 1971). In the study area it mainly occurs in deciduous or mixed forests (Fig. 1). Individuals are well defined and have no special features for vegetative spread. The subterranean rhizome produces one to several shoots annually and the average life-span of an individual reaching maturity is estimated to 44.1 years (Ehrlén and Lehtilä 2002). Flowering usually takes place in early May, and each shoot carries 1-5 racemes with 1-9 purple-red flowers per raceme (Fig.2). Number of flowers is determined in the previous summer when flower buds differentiate. Flowering is sequential, starting with the proximal (closest to the stem) flowers on the basal (closest to the ground) raceme. All flower buds are visible at the onset of flowering. The plant is selfcompatible but lacks mechanisms for selfpollination. Pollination is mostly carried Figure 1. Deciduous forest islands surrounded by out by Bombus spp. moved meadows representing the typical Lathyrus Recruitment is seed vernus habitats in the study area. limited (Ehrlen 2003). Lathyrus vernus seeds have an average mass of 12.0 ± 3.5 mg (Ehrlén and van Groenendael 2001). Apion opeticum (Coleoptera: Aphidae) is monophagous on L. vernus in the study area. It has a restricted distribution in Sweden but occurs scattered across Europe, East Palearctic and Near East (Alonso-Zarazaga 2004a). Females insert eggs in young fruits through the closure of a pod, and pods are glued together to avoid dehiscence before development is completed. Larvae 12 develop inside the pod, discretely consuming one or rarely two seeds. Pods are glued to avoid dehiscence before development is completed. Adults exit the pod by cutting a hole through the exocarp. Bruchus atomarius (Coleoptera: Bruchidae) utilizes a few species of the closely related genera Vicia and Lathyrus but shows a preference for L. vernus in the study area, attacking a relatively large proportion of seeds every year. It is common in the study area and is distributed widely across Europe (Audisio 2004). Eggs are laid on the exterior of young pods and larvae enter through the exocarp. Larvae develop inside a single seed and disperse with the seeds as pods dehisce at maturity. Figure 2. Flowering individual of the Tychius quinqepunctatus (Colperennial understory herb Lathyrus eoptera: Curculionidae) attacks L. vernus vernus only in some years. Its host range is not fully known but it is reported to attack species of Vicia and Lathyrus (Bullock 1992) and has been reported as a plague on cultivated Lens esculenta (Monreal et al. 1990). It has a wide distribution across Europe, East Palearctic, Near East and North Africa (Alonso-Zarazaga 2004b). The oviposition procedure is not known. Larvae develop and move around inside a pod, consuming one to several seeds, and adults are found in mature pods. Data collection The study was performed in a 5 x 5 km area in the province of Uppland, central eastern Sweden (Fig. 3). The area is dominated by coniferous forest but a large fraction consists of a mixture of meadows, pastures, cultivated fields and broad-leaved deciduous or mixed forests. This mosaic landscape is partly protected and managed to preserve the pre-industrial agricultural landscape structure. Studies were performed during six consecutive years (2000– 2005) and within the study area, I localized 46 Lathyrus vernus patches and recorded their size and degree of isolation. 13 Population studies To study the effects of spatio-temporal variation of plant resources on the intensity of seed predation (paper I and II) I recorded several characteristics of the 46 plant patches. A Lathyrus vernus patch was defined as a group of individuals separated from conspecifics by at least 20 m. I used a geographical information system to map the spatial location of each patch. I calculated the area of each patch by making polygons within field monitored GPS-positions on a digital map. To examine effects of Figure 3. The location of 46 Lathyrus vernus populathe adjacent landtions in a 5 x 5 km area in the province of Uppland, scape, I calculated central eastern Sweden (black dots). Yellow areas reprethe proportion of sent open areas, e.g. meadows, arable fields or pastures. the patch perimeter Green areas represent forested landscape. Blue-ruled areas represent watercourse. adjoining to open areas. All spatial variables were calculated in ArcView GIS 3.2. The intensity of predation from the two beetles as well as variables describing host plant population seed production and patch characteristics was recorded in all patches that were not to heavily grazed by cattle. I measured environmental variables in each patch, such as the height of the field layer, litter layer and canopy cover. Each year the number of flowering L. vernus individuals was counted in all patches at peak flowering and at fruit maturity I estimated the proportion of flowering individuals producing fruit. The abundance of the alternative host plants utilized by B. atomarius was estimated both within patches and in the matrix landscape surrounding L. vernus patches. The number of seeds per plant was estimated within each L. vernus patch by collecting pods from up to 20 randomly chosen individuals with mature fruits. In these individuals I also recorded the number of flowers and fruits. The damage rate of B. atomarius and A. opeticum was estimated from the collected fruits. The 14 number of seeds per patch was calculated as the mean number of seeds per individual in fruiting individuals multiplied by the number of individuals that produced fruits. Apion opeticum and B. atomarius population sizes were calculated as the proportion of seeds damaged multiplied by the number of seeds in the patch. Selection studies To study phenotypic selection pressures through seed predation (paper III), I followed 107 L. vernus individuals from initiation of flowering to fruit maturation and recorded flowering phenology in terms of the first flowering date (FFD). At maturity all fruits were collected, and the number of non-fruiting flowers, in terms of pedicel scars, counted. Seeds and adult beetles of all three seed predators remained in the collected fruits, making it easy to quantify the number of undamaged seeds and assign damaged seeds to each respective seed predator. I estimated gross seed production, the total number of intact and damaged fully developed seeds as well as net seed production, the number of fully developed seeds that escaped damage. I also calculated the number of seeds that escaped damage from each of the three predators, by subtracting number of seeds damaged by each predator from gross seed production. Gross seed production was considered an accurate estimate of plant seed production and fitness in the absence of seed predators. To study the relationship between seed predator offence and plant defence (paper IV), I followed fruit initiation and early fruit abortion (before seedexpansion) on fifty randomly selected Lathyrus vernus individuals. Individual fruits were surveyed from the initiation of the first fruit until oviposition activity ended, which occurred as flowering in the latest flowering individuals ended. The total number of flowers on an individual was recorded and sorted in each individual raceme and each flower was followed individually throughout the study by recording its position within the raceme. Fruit initiation and the subsequent state of fruits (retained or aborted) were recorded on each flower position on four occasions. I used the date of the first observation of an initiated fruit at a flower position as a measure of fruit phenology. On all visits each fruit (both newly-initiated and previously present) was carefully surveyed for Bruchus atomarius eggs and the number of eggs present was recorded. At fruit maturation all fruits on each plant were collected and the number of larval entrance holes in the endocarp, adult beetles and damaged seeds were counted. I counted each egg that developed into an adult beetle as a successful larva. Data analysis Connectivity between patches was estimated separately for each species and year as Si = Σexp(αdij)Ntj (Hanski 1999), where α is a constant describing 15 how the number of migrants decline with increasing distance, dij is the distance between patch i and j, and Ntj is the population size of A. opeticum, B. atomarius or L. vernus respectively in patch j, year t. I examined several values of α and I then selected the best fit (α = 0.02), corresponding to an average migration distance of 50 m (Hanski 1999). To examine effects of spatial patterns and local environment on seed predation intensity (Paper I), I used generalized linear models that were built in three steps. First I examined all candidate predictor variables for each response variable by univariate tests. Response variables were incidence of predation by A. opeticum, proportion of individuals preyed, proportion of seeds damaged and population size of A. opeticum and B. atomarius respectively, and total seed loss. Second, multiple models were constructed with population size and isolation, number of flowering L. vernus and connectivity included in all models. Other predictor variables were included if P < 0.10 in the respective univariate tests. Third, I used AIC (Akaike information criterion) to rank models. I calculated AIC as –2(log-likelihood of fitted model) + 2(number of predictors in the fitted model) (Venables and Ripley 1999), and selected models with the lowest AIC that included population size and connectivity. A log-linear model was used to test if A. opeticum and B. atomarius utilized L. vernus individuals independently of each other in nine patches where they co-occurred. To examine how temporal variation in seed predation intensity was affected by resource- abundance and variation (paper II), I used logistic regressions to test how colonization and extinction events were related to seed predator population size and connectivity. I used linear mixed-effects models nested within patch to examine how changes in seed production between two adjacent years affected the proportion of seeds preyed, and how previous year population size, current seed production and patch openness affected abundance of A. opeticum and B. atomarius in a given year. Models were simplified by removing variables that did not significantly improve fit. To examine phenotypic selection pressures by seed predation (paper III), I first performed selection analysis, using the relative number of seeds as a measure of individual fitness. I quantified phenotypic selection on number of flowers and first flowering day using regression methods with standardized trait values according to Lande and Arnold (1983). To estimate how predispersal seed predation changed selection on flower number and first flowering day, I compared the partial regression coefficients in absence and presence of the seed predators. Since residuals were not normally distributed I assessed 95 % confidence intervals of selection differentials and selection gradients by bootstrapping. Data were resampled 10000 times, and the confidence intervals were constructed using bias-corrected and accelerated methods based on saved coefficients from each bootstrapping in package “boot” in R. Preference by each of the seed predators was measured by the proportion of seeds of a Lathyrus vernus individual that were attacked by a 16 focal seed predator. Preference patterns were examined with models containing number of flowers, first flowering day and seeds per flower. I used AIC to rank models and selected the model having the lowest AIC. To evaluate how the oviposition pattern affected B. atomarius fitness (Paper IV) in terms of egg survival, I first assessed the relationship between the number of eggs per fruit and the number of developed beetles per fruit. I then fitted the function y = a + bx + cx 2 , where x is number of eggs on retained fruits; y is number of developed beetles and the quadratic term models density dependent egg survival. To calculate the number of beetles for a random oviposition scenario, I used the mean number of eggs per fruit on all initiated fruits (retained + aborted) as the value of x in this fitted function. The effects on reproductive output of the oviposition pattern for the plant was estimated as the difference between the actual number of intact seeds produced and the number of seeds that would have been the result of random oviposition. To investigate the effects of beetle oviposition pattern on average beetle fitness I used a t-test. Individual plant traits, i.e. number of flowers, fruit phenology, and fruit abortion patterns among and within individuals, versus egg laying patterns were tested with linear regressions models. In cases where the causal relation between variables was uncertain I used a model II regression (Bartlett's three-group method, Sokal and Rohlf 2001). I tested for effects of individual fruit position and phenology on the number of Bruchus atomarius eggs on a Lathyrus vernus fruit with a generalized linear model. 17 Results Spatio-temporal variance in host plant population size, seed production, connectivity and local environmental factors had partly different and partly similar effects on the intensity of pre-dispersal seed predation in two seed predators with different host range. Different host ranges resulted in varying local abundances and disparate distributions in time and space. Pre-dispersal seed predators had potential to change trait selection gradients in their host plant and this depended on the context in terms of co-occurrence of species. The underlying mechanisms of the trait changes were differing trait preferences in species with differing host range and trait preferences also changed with differing abundances of the co-occurring species. The predictive pattern of fruit abortion in a long-lived perennial plant resulted in an advantage for seed predator offence over plant defence. Paper I – effects of plant patches and environment on seed predation intensity The intensity of pre-dispersal specialist and generalist seed predation was affected by both host plant population size and local environmental factors. Effects of plant population size were relatively more important in the specialist than in the generalist seed predator, and the specialist seed predator occurred in less than half of the patches whereas the generalist was present in nearly all patches. Generalist seed predation was affected by environmental factors, such as the height of the field layer. Intensity of generalist seed predation on Lathyrus vernus increased with the abundance of the alternative hosts but there were no effects in the reversed direction; presence or absence of L. vernus did not affect the predation rate on alternative hosts. My results suggest that the relative importance of different factors influencing the intensity of interactions depend on the degree of specialization. Paper II – dynamics of two pre-dispersal seed predators over six years The temporal variation in the intensity of seed predation was affected mainly by seed production but also by environmental conditions. Relative increases in seed production from one year to the next resulted in an increased intensity of predation by the monophagous Apion opeticum. The trend was similar in the oligophagous Bruchus atomarius. I found relatively weak effects of connectivity and relatively strong effects of previous years population size and the current years seed production within patches, indicating that popula18 tion dynamics were relatively more affected by local factors than by migration. Although, the monophagous A. opeticum was less abundant and had lower population densities, abundance of the oligophagous B. atomarius was more correlated to seed production. Openness of patch edges when seed production was high had positive effects on the abundance of A. opeticum. Extinction events were related to local population size of B. atomarius but not for A. opeticum. Connectivity did not affect population size of A. opeticum and for B. atomarius it was only important in closed forests. Paper III – plant trait selection, effects of seed predation and seed predator preferences Selection on flower number was influenced by pre-dispersal seed predation. My results show that the patterns of preference differed among the three investigated seed predators with differing host plant range but also show that trait-preferences were associated with the abundance of the other seed predators. Thus, the impact on phenotypic selection of seed predation was the result of relatively complicated relationships between co-occurrence and preference patterns in the seed predators. The increase in fitness with increasing number of flowers in presence, but not in the absence, of seed predation was disproportional, indicating satiation of seed predators at the level of plant individuals. Paper IV – the role of fruit abortion and selective oviposition The relative effects by the observed oviposition and fruit abortion patterns on seed predator and plant fitness indicated a clear seed predator offence but no obvious plant defence. Lathyrus vernus individuals had a predictable abortion pattern, late fruits and fruits in distal positions had a higher probability of abortion. Bruchus atomarius females preferentially laid their eggs on fruits with a lower than average probability of abortion and appeared to use fruit position and phenology as well as some additional unidentified cue. From the plant perspective, the average reproductive output was reduced by the observed oviposition as compared to a random oviposition pattern indicating that the abortion pattern has evolved to optimize allocation of resources rather than as a response to seed predation. 19 Discussion Ecological aspects Varying host range was associated with differences in abundance and predation intensity by the three seed predators. The most polyphagous species Tychius quinqepunctatus only occasionally attacked Lathyrus vernus, the oligophagous Bruchus atomarius was most abundant and was positively affected by the abundance of the alternative hosts, and the monophagous Apion opeticum had lower abundance and was most closely related to host plant population size. The consumer dynamics in this system with moderate temporal variation in the resource were relatively stable and responses to relative variation in resources differed in both magnitude and direction from those reported from systems with high fluctuations (cf. Kelly 1994). Shortterm responses to resource fluctuations were qualitatively the same in monophagous and oligophagous seed predators. However, a narrower host range resulted in lower densities and fewer patches colonized. Thus, the effect of differential resource availability may result in long-term effects of host range. Predation by the oligophagous seed predator on L. vernus increased with increasing abundance of alternative hosts indicating apparent competition. There was no reverse effect by presence or absence of L. vernus on seed predation rate on alternative hosts. Effects of the local environment on the two species were partly different, but both seed predators seemed to benefit from the same conditions that were favourable for seed production, thus experiencing dynamics well synchronized with the temporal resource variation. The seed predator species differed in attack rates and seed loss in L. vernus was relatively high (mean: 34 %, range 0-100%) and varied considerably in time and space. Evolutionary aspects Given that seed predator species exert at least partly different selection pressures, the net selection pressure will vary spatially as a consequence of all factors affecting any of the involved predators. Interactions will take different expressions at varying scales and this will partly depend on the search behaviour in the insect. The predation rates on plant individuals may be affected by distance among neighbouring plants or by preference for individual fruits within plant individuals, hence variation host density on the patch 20 level are not necessarily mirrored by processes acting at lower hierarchical levels. The number of flowers in individual plants is an important character, determining the number of seeds and the fitness potential. The number of flowers also has the dual role of simultaneously attracting pollinators and seed predators. The difference in selection on flower number in absence or presence of pre-dispersal seed predation was the combined effect of the three seed predators different preference patterns. Relative fitness in the presence of seed predation increased disproportionately with higher flower numbers. Thus, even though seed predators preferred plants with many flowers, a larger proportion of seeds escaped damage in these plants with higher number of flowers. This suggests that high numbers of flowers may result in predator satiation and that it may be beneficial, in the presence but not in the absence of seed predators, to concentrate reproductive efforts to only some seasons, i.e. not to flower every year. The negative relationship between seed predator abundances and differing preferences with varying abundances of the other species suggests that occurrence patterns are a ghost of competition past. The complex pattern of trait preferences of all three seed predators for flower number suggest that plant trait selection mediated by a seed predator will vary with varying abundances of co-occurring species. The production of surplus flowers is a common phenomena (Burd 1998). The subsequent excess of young fruits enables high rates of fruit abortion potentially reducing seed loss through pre-dispersal seed predation (Stephenson 1981, Ehrlén 1993, Holland et al. 2004). Initial herbivore damage could be a potential cue to future damage and would thereby enable suitable plant responses, such as induced fruit abortion, similar to the induction of chemical defences (Dicke and Hilker 2003). However, I found no evidence that L. vernus reduced seed loss due to pre-dispersal seed predation through an increased mean abortion rate of fruits at high levels of infestation. On the contrary B. atomarius was highly capable of locating viable fruits. The patterns observed in my study suggest that Lathyrus vernus is constrained by the predictive fruit abortion that has evolved independently of the seed predation, i.e. due to sequential resource allocation (cf Lloyd 1980). Nevertheless, some fruits with eggs were aborted which may suggest an evolutionary potential in L. vernus to reduce seed loss caused by predispersal seed predation. Poor defensive strategies in plants in combination with highly offensive strategies of consumers are likely the result of differential evolutionary capacities due to the large discrepancy in generation time (Gandon and Michalakis 2002). 21 Concluding remarks All is a matter of scale and context. This thesis has shown that interactions between plants and antagonists vary in time, that processes differ at varying scales, that differing host range results in different damage intensity as well as in differing trait preferences. Moreover, pairwise interactions are affected by the abundance of co-occurring plants and animals. Taken together, this will result in complex selection mosaics and coevolutionary trajectories. Such complex interactions among co-occurring antagonists in combination with spatial and temporal variation in abundances will result in diffuse selection on plant traits as well as in the reciprocal selection on antagonists. The fact that coevolutionary processes are diffuse gives further emphasis to the importance of studying coevolutionary relationships in their full context (cf. Thompson 1994). A step towards dissecting diffuse coevolutionary relationships would be the examination of variation of interaction processes on a geographical scale by comparing trait selection in populations that vary in the seed predator guild. Further studies should also benefit of examining the mechanisms involved in search behaviour and host choice, such as the degree of competition within a consumer guild and the relative role of defensive, visual and olfactory cues. 22 Acknowledgements I am grateful to Johan Dahlgren, Johan Ehrlén and Peter Hambäck for valuable comments on this text. 23 References Agrawal, A. A. 2000. Host-range evolution: Adaptation and trade-offs in fitness of mites on alternative hosts. Ecology 81:500-508. Agrawal, A. A., J. A. Lau, and P. A. Hambäck. 2006. Community heterogeneity and the evolution of interactions between plants and insect herbivores. Quarterly Review of Biology 81:349-376. Alonso-Zarazaga, M. A. 2004a. Fauna Europaea: Coleoptera, Apionidae. in. Fauna Europaea version 1.1, http://www.faunaeur.org. Alonso-Zarazaga, M. A. 2004b. Fauna Europaea: Coleoptera, Curculionidae. in. Fauna Europaea version 1.1, http://www.faunaeur.org. Audisio, P. 2004. Fauna Europaea: Coleoptera, Chrysomelidae. in. Fauna Europaea version 1.1, http://www.faunaeur.org. Augner, M. 1994. Should a plant always signal its defense against herbivores. Oikos 70:322-332. Augner, M., T. Fagerström, and J. Tuomi. 1991. Competition, defense and games between plants. Behavioral Ecology and Sociobiology 29:231-234. Bach, C. E. 1988a. Effects of host plant patch size on herbivore density: Patterns. Ecology 69:1090-1102. Bach, C. E. 1988b. Effects of host plant patch size on herbivore density: Underlying mechanisms. Ecology 69:1103-1117. Bernays, E. A. 1998. The value of being a resource specialist: Behavioral support for a neural hypothesis. American Naturalist 151:451-464. Brody, A. K. 1992. Oviposition choices by a predispersal seed predator (Hylemya Sp). 2. A positive association between female choice and fruit-set. Oecologia 91:63-67. Brody, A. K., and R. J. Mitchell. 1997. Effects of experimental manipulation of inflorescence size on pollination and pre-dispersal seed predation in the hummingbird-pollinated plant Ipomopsis aggregata. Oecologia 110:86-93. Bullock, J. A. 1992. Host plants of British beetles: a list of recorded associations. Amateur Entomolgists' Society (AES). Burd, M. 1998. "Excess" flower production and selective fruit abortion: A model of potential benefits. Ecology 79:2123-2132. Cain, M. L. 1985. Random search by herbivorous insects - a simulation-model. Ecology 66:876-888. Cariveau, D., R. E. Irwin, A. K. Brody, L. S. Garcia-Mayeya, and A. von der Ohe. 2004. Direct and indirect effects of pollinators and seed predators to selection on plant and floral traits. Oikos 104:15-26. Crawley, M. J. 1992. Seed predators and plant population dynamics. Pages 157-191 in M. Fenner, editor. The ecology of regeneration in plant communities. C A B International, Melksham. Dicke, M., and M. Hilker. 2003. Induced plant defences: from molecular biology to evolutionary ecology. Basic and Applied Ecology 4:3-14. 24 Eckhart, V. M. 1992. Spatiotemporal variation in abundance and variation in foraging behavior of the pollinators of gynodioecious Phacelia linearis (Hydrophyllaceae). Oikos 64:573-586. Egan, S. P., and D. J. Funk. 2006. Individual advantages to ecological specialization: insights on cognitive constraints from three conspecific taxa. Proceedings of the Royal Society B-Biological Sciences 273:843-848. Ehrlen, J. 2003. Fitness components versus total demographic effects: Evaluating herbivore impacts on a perennial herb. American Naturalist 162:796-810. Ehrlén, J. 1993. Ultimate functions of non-fruiting flowers in Lathyrus vernus. Oikos 68:45-52. Ehrlén, J. 1996. Spatiotemporal variation in predispersal seed predation intensity. Oecologia 108:708-713. Ehrlén, J. 1997. Risk of grazing and flower number in a perennial plant. Oikos 80:428-434. Ehrlén, J., and K. Lehtilä. 2002. How perennial are perennial plants? Oikos 98:308322. Ehrlén, J., and J. van Groenendael. 2001. Storage and the delayed costs of reproduction in the understorey perennial Lathyrus vernus. Journal of Ecology 89:237246. Ehrlich, P. R., and P. H. Raven. 1964. Butterflies and plants - a study in coevolution. Evolution 18:586-608. Elzinga, J. A., H. Turin, J. M. M. van Damme, and A. Biere. 2005. Plant population size and isolation affect herbivory of Silene latifolia by the specialist herbivore Hadena bicruris and parasitism of the herbivore by parasitoids. Oecologia 144:416-426. Eriksson, O. 1995. Asynchronous flowering reduces seed predation in the perennial forest herb Actaea spicata. Acta Oecologica-International Journal of Ecology 16:195-203. Gandon, S., and Y. Michalakis. 2002. Local adaptation, evolutionary potential and host-parasite coevolution: interactions between migration, mutation, population size and generation time. Journal of Evolutionary Biology 15:451-462. Gomulkiewicz, R., J. N. Thompson, R. D. Holt, S. L. Nuismer, and M. E. Hochberg. 2000. Hot spots, cold spots, and the geographic mosaic theory of coevolution. American Naturalist 156:156-174. Hambäck, P. A., and G. Englund. 2005. Patch area, population density and the scaling of migration rates: the resource concentration hypothesis revisited. Ecology Letters 8:1057-1065. Hanski, I. 1998. Metapopulation dynamics. Nature 396:41-49. Hanski, I. 1999. Metapopulation Ecology, 1st edition. Oxford University Press, New York. Herrera, C. M. 1993. Selection on floral morphology and environmental determinants of fecundity in a hawk moth-pollinated violet. Ecological Monographs 63:398-398. Herrera, C. M., M. Medrano, P. J. Rey, A. M. Sanchez-Lafuente, M. B. Garcia, J. Guitian, and A. J. Manzaneda. 2002. Interaction of pollinators and herbivores on plant fitness suggests a pathway for correlated evolution of mutualism- and antagonism-related traits. Proceedings of the National Academy of Sciences of the United States of America 99:16823-16828. Holland, J. N., J. L. Bronstein, and D. L. DeAngelis. 2004. Testing hypotheses for excess flower production and low fruit-to-flower ratios in a pollinating seedconsuming mutualism. Oikos 105:633-640. 25 Hultén, E. 1971. Atlas över växternas utbredning i Norden: fanerogamer och ormbunksväxter, 2nd edition. Generalstabens litografiska anstalts förlag, Stockholm. Jaenike, J. 1990. Host specialization in phytophagous insects. Annual Review of Ecology and Systematics 21:243-273. Janz, N., and S. Nylin. 1997. The role of female search behaviour in determining host plant range in plant feeding insects: A test of the information processing hypothesis. Proceedings of the Royal Society of London Series B-Biological Sciences 264:701-707. Janzen, D. H. 1980. When is it coevolution. Evolution 34:611-612. Johnson, M. T. J., and J. R. Stinchcombe. 2007. An emerging synthesis between community ecology and evolutionary biology. Trends in Ecology & Evolution 22:250-257. Kelly, D. 1994. The evolutionary ecology of mast seeding. Trends in Ecology & Evolution 9:465-470. Kunin, W. E. 1999. Patterns of herbivore incidence on experimental arrays and field populations of ragwort, Senecio jacobaea. Oikos 84:515-525. Lande, R., and S. J. Arnold. 1983. The measurement of selection on correlated characters. Evolution 37:1210-1226. Lankau, R. A. 2007. Specialist and generalist herbivores exert opposing selection on a chemical defense. New Phytologist 175:176-184. Leimu, R., K. Syrjanen, J. Ehrlen, and K. Lehtila. 2002. Pre-dispersal seed predation in Primula veris: among-population variation in damage intensity and selection on flower number. Oecologia 133:510-516. Levins, R. 1969. Some demographic and genetic consequences of environmental heterogeneity for biological control. Bulletin of the Entomological Society America 15:237-240. Lloyd, D. G. 1980. Sexual strategies in plants. 1. An hypothesis of serial adjustment of maternal investment during one reproductive session. New Phytologist 86:6979. Louda, S. M., and M. A. Potvin. 1995. Effect of inflorescence-feeding insects on the demography and lifetime fitness of a native plant. Ecology 76:229-245. Maron, J. L., and M. J. Kauffman. 2006. Habitat-specific impacts of multiple consumers on plant population dynamics. Ecology 87:113-124. Monreal, J. A., D. Salvador, and J. Mansilla Martinez. 1990. Tychius quinquepunctatus L. (Col. Curculionidae), una nueva plaga de la lenteja. Boletín de salud vegetal: Plagas 16:5-9. Morris, W. F., R. A. Hufbauer, A. A. Agrawal, J. D. Bever, V. A. Borowicz, G. S. Gilbert, J. L. Maron, C. E. Mitchell, I. M. Parker, A. G. Power, M. E. Torchin, and D. P. Vazquez. 2007. Direct and interactive effects of enemies and mutualists on plant performance: A meta-analysis. Ecology 88:1021-1029. Östergård, H., and J. Ehrlén. 2005. Among population variation in specialist and generalist seed predation - the importance of host plant distribution, alternative hosts and environmental variation. Oikos 111:39-46. Silvertown, J., and D. Charlesworth. 2001. Plant population biology, 4 edition. Blackwell Science Ltd, Great Britain. Sokal, R. R., and F. J. Rohlf. 2001. Biometry - the principles and practice of statistics in biological research, 3 edition. W. H. Freeman and Company, New York. Stephenson, A. G. 1981. Flower and fruit abortion: proximate causes and ultimate functions. Annual Review of Ecology and Systematics 12:253-279. Strauss, S. Y. 1997. Floral characters link herbivores, pollinators, and plant fitness. Ecology 78:1640-1645. 26 Strauss, S. Y., H. Sahli, and J. K. Conner. 2005. Toward a more trait-centered approach to diffuse (co)evolution. New Phytologist 165:81-89. Thompson, J. N. 1994. The coevolutionary process, 1 edition. The University of Chicago Press, Chicago and London. Thompson, J. N., and O. Pellmyr. 1989. Origins of variance in seed number and mass - interaction of sex expression and herbivory in Lomatium salmoniflorum. Oecologia 79:395-402. Thompson, J. N., and O. Pellmyr. 1991. Evolution of oviposition behavior and host preference in Lepidoptera. Annual Review of Entomology 36:65-89. Tiffin, P. 2000. Are tolerance, avoidance, and antibiosis evolutionarily and ecologically equivalent responses of plants to herbivores? American Naturalist 155:128-138. Toju, H., and T. Sota. 2006. Imbalance of predator and prey armament: Geographic clines in phenotypic interface and natural selection. American Naturalist 167:105-117. Traveset, A. 1995. Spatio-temporal variation in pre-dispersal reproductive losses of a mediterranean shrub, Euphorbia dendrois L. Oecologia 103:118-126. Turchin, P. 1991. Translating foraging movements in heterogeneous environments into the spatial distribution of foragers. Ecology 72:1253-1266. Van Zandt, P. A., and A. A. Agrawal. 2004. Specificity of induced plant responses to specialist herbivores of the common milkweed Asclepias syriaca. Oikos 104:401-409. Vanhoenacker, D., J. Ågren, and J. Ehrlén. 2006. Spatio-temporal variation in pollen limitation and reproductive success of two scape morphs in Primula farinosa. New Phytologist 169:615-621. Venables, W. N., and B. D. Ripley. 1999. Modern applied statistics with S-PLUS, 3 edition. Springer, New York. Wilson, R. D., and J. F. Addicott. 1998. Regulation of mutualism between yuccas and yucca moths: is oviposition behavior responsive to selective abscission of flowers? Oikos 81:109-118. von Zeipel, H., O. Eriksson, and J. Ehrlen. 2006. Host plant population size determines cascading effects in a plant-herbivore-parasitoid system. Basic and Applied Ecology 7:191-200. Zabel, J., and T. Tscharntke. 1998. Does fragmentation of Urtica habitats affect phytophagous and predatory insects differentially? Oecologia 116:419-425. 27 Svensk sammanfattning I den här avhandlingen har jag studerat interaktionen (samspelet) mellan vårärt, Lathyrus vernus, och tre fröätande skalbaggar (fröpredatorer), Apion opeticum (gruppen spetsvivlar), Bruchus atomarius (ärtsmyg eller bönbagge) och Tychius quinqepunctatus (gruppen vivlar), med olika grad av värdväxtspecialisering. De vuxna skalbaggarna lägger sina ägg på eller i vårärtens frukter (baljor) och därefter utvecklas larverna inuti baljan, eller inuti enskilda frön, tills de är fullvuxna skalbaggar. Apion angriper endast vårärt och har en begränsad utbredning i Sverige, Bruchus föredrar vårärt men angriper också bland annat gökärt, Lathyrus linifolius, och häckvicker, Vicia sepium och Tychius förekommer bara vissa år på vårärt och använder flera arter inom släktena Lathyrus och Vicia och även andra ärtväxter. Syftet med studierna var att undersöka hur intensiteten i växt-djurinteraktioner påverkas av födoresursens variation i tid och rum med särskilt avseende på effekter av värdväxtspecialisering, artsammansättning och växtegenskaper. Interaktioner mellan växter och djur påverkas på många sätt av såväl miljöfaktorer som förekomst, utbredning och egenskaper hos de berörda arterna. Växter är ofta fläckvis utbredda i landskapet, i både små och stora växtpopulationer på varierande avstånd från varandra, och detta påverkar de interagerande djurens möjligheter till spridning och lokal överlevnad. En växt är ofta involverad i åtskilliga, både mutualistiska och antagonistiska, interaktioner och styrkan av en interaktion är oftast beroende av övriga interaktörer. Mutualistiska interaktioner (t ex pollinering) är gynnsamma för båda parter medan det i antagonistiska interaktioner är en part som gynnas på bekostnad av den andra. Fröpredation (fröätande) delas in två kategorier, beroende på om angreppet sker före eller efter fröspridningen, på grund av att de ekologiska och evolutionära konsekvenserna skiljer sig åt mellan de två typerna. Jag har studerat fröpredation före fröspridning som förekommer inom många djurgrupper men främst bland insekter. Eftersom interaktioner sällan sker oberoende av varandra är det viktigt att ta hänsyn till olika interaktioners effekter på varandra, till exempel kan närvaron av en art påverka beteendet hos en annan. Värdväxtspecialisering förekommer i olika grad hos djur som angriper växter, en del är helt specialiserade på en enda art (monofaga), andra arter använder ett fåtal närbesläktade eller likartade växter (oligofaga) och de arter som är generalister använder ett stort antal växtarter (polyfaga). Interaktionen mellan växt och insekt påverkas av graden av 28 värdväxtspecialisering, bland annat genom att specialister är helt beroende av sin enda värdart och därmed får en mer begränsad spridningsförmåga och löper en större risk för ett lokalt utdöende vid de tillfällen då växtresursen minskar. Generalister har oftast ytterligare resurser att tillgå, i form av alternativa värdväxter. Trots fördelarna med att ha ett stort antal värdväxter är det vanligt att insekter är specialister och detta tror man bland annat beror på att specialister blir effektivare på att både finna och nyttja sin födoresurs. Fröpredatorer med olika grad av specialisering kan ha skilda effekter på den gemensamma värdväxten, både på grund av skillnader i förekomst och antal, men också för att deras val (preferens) mellan växtindivider med olika egenskaper (t ex blomantal) kan skilja sig åt. Preferensen för olika växtegenskaper skiljer sig sannolikt åt hos insekter med olika värdväxtspecialisering och påverkas förmodligen också av förekomsten av andra arter som konkurrerar om samma resurs. Preferens för specifika växtegenskaper leder till varierande reproduktionsframgång (fitness) för olika växtindivider (selektionstryck) och om egenskaperna är ärftliga kommer variationen av egenskaper inom arten att förändras. Individer med många blommor är attraktiva för pollinatörer men lockar samtidigt till sig fler fröpredatorer, vilket kan leda till motstående selektionstryck från pollinatörer och fröpredatorer eftersom de förra gynnar reproduktionen och de senare reducerar den. Coevolution (samevolution), är ömsesidiga evolutionära anpassningar hos växt och insekt, som uppstår då växtegenskaper resulterar i anpassningar hos insekterna vilka i sin tur kan ge upphov till nya anpassningar hos växten osv. Eftersom interaktioner sällan är en enskild företeelse mellan två parter är sådana anpassningar (adaptationer) oftast svåra att härleda, vilket gör det ännu viktigare att ta hänsyn till hela nätverket av interaktioner som en art ingår i. Möjligheterna till anpassning påverkas också av hur långlivade arterna är. Eftersom insekter oftast har väsentligt mycket kortare generationstid än värdväxterna så har de en större kapacitet till evolutionär respons (anpassning) än vad långlivade växter har. I många fall har man funnit att insekter övervunnit, och ibland till och med kunnat dra nytta av, försvarskaraktärer hos växten. Under evolutionen har olika försvarsstrategier mot antagonister uppstått hos växter såsom produktion av gifter, taggar och tornar. Även andra strategier kan minska angreppsgraden, till exempel kan en växt minska skadan av ett angrepp genom att avlägsna angripna delar och därmed strypa resursen för angriparen. Det omgivande växtsamhället påverkar också intensiteten av en interaktion, eller angreppsgraden, beroende på hur mycket alternativa värdväxter det finns tillgång till, och ibland kan växter indirekt konkurrera med varandra genom att förekomst av en art ökar angreppsgraden på en annan. Vårärt blommar som namnet antyder i maj och förekommer i Sverige oftast i lövskog eller örtrika blandskogar. Jag lokaliserade 46 29 vårärtspopulationer inom ett 5 km x 5 km stort område några mil norr om Uppsala. Mitt i detta område finns ett naturreservat, Andersby ängsbackar, där ett jordbrukslandskap med förindustriell karaktär har bevarats. Under sex år följdes dessa populationer från blomning till frömognad då baljprover samlades in från samtliga populationer för att beräkna fröproduktion och angrepp av respektive skalbagge. På varje undersökt växtindivid noterades antalet blommor och frukter. I varje population räknades antalet blommande individer, och yta och avstånd till övriga populationer mättes. Jag mätte också ett antal miljöfaktorer, till exempel trädkronornas täckningsgrad, som påverkar ljusförhållandena, och markvegetationens sammansättning. Förekomsten av alternativa värdarter (gökärt och häckvicker) noterades också, både i och mellan vårärtspopulationerna. I den första och andra studien (Paper I & II) fann jag att vårärtspopulationernas storlek samt de lokala miljöförhållandena påverkade angreppsgraden av både Apion (specialist) och Bruchus (generalist). Apion förekom bara i hälften av populationerna medan Bruchus förekom i alla utom en. Båda skalbaggarna populationsstorlekar ökade med ökande storlek på vårärtspopulationen och effekten var störst för Apion. Miljöfaktorer och tillgången till alternativa värdväxter ökade graden av Bruchus-angrepp på vårärt. Förekomst av vårärt hade däremot ingen effekt på angreppsgraden på de alternativa värdväxterna utan de blev lika hårt angripna där vårärt fanns som där den inte fanns. Skalbaggarnas populationsdynamik (variation i populationsstorlek mellan år) varierade under de sex åren och populationsstorleken var starkt knuten både till årlig fröproduktion och till föregående års skalbaggsantal hos båda arterna. I den tredje studien (Paper III) fann jag att selektionstrycket på blomantal skiljde sig åt i närvaro eller frånvaro av fröpredation. Vårärtsindivider med många blommor hade högre reproduktionsframgång (fitness) både med och utan fröpredation, men i närvaro av fröpredation hade individer med stort blomantal en oproportionerligt högre fitness än de med färre blommor. Den här skillnaden verkade bero på att de tre skalbaggsarterna delvis föredrog olika växtindivider och att deras preferens (förkärlek) för individer med många blommor påverkades av närvaron av de andra arterna. Det var skillnader i skalbaggarnas preferens och deras påverkan på varandra, som sammantaget förändrade selektionstrycket på blomantal hos vårärt. Det är alltså troligt att selektionstrycket av fröpredation kommer variera beroende på hur många arter som samexisterar. I den fjärde studien (Paper IV) fann jag att växten aborterade unga baljor i ett förutsägbart mönster, och att skalbaggen (Bruchus atomarius) lade sina ägg på de baljor som hade lägst sannolikhet att bli aborterade. Resultatet av växtens aborteringsmönster och skalbaggens äggläggningsmönster visade att skalbaggen ökade sin fitness (antalet fullutvecklade skalbaggar) jämfört med om den lagt sina ägg slumpmässigt. Däremot minskade vårärtens reproduktionsframgång (antalet oskadda frön) jämfört med ett slumpmässigt 30 scenario, alltså hade växten ingen förmåga att minska skadorna av fröpredationen genom att abortera angripna frukter. Sammantaget visar de fyra studierna att växtpopulationens storleksvariation i tid och rum, fröproduktion, avstånd till övriga populationer, lokala miljöfaktorer delvis hade olika och delvis likartade effekter på två fröätande skalbaggar med olika grad av värdväxtspecialisering. Fröpredation påverkade selektionstrycket på värdväxten och detta var beroende av hur varje art påverkades av samexistensen med de övriga. Ett förutsägbart utvecklingsmönster hos växten var fördelaktigt för angripande insekter. Allt som allt kommer detta att leda till en brokig blandning av olika selektionstryck på olika växtpopulationer. Resultatet blir en stor variation av diffusa anpassningar hos både växter och djur vilket understryker vikten av att studera hela nätverket av interaktioner som en art är involverad i för att få ökade kunskaper om hur interaktioner påverkar populationsdynamik och evolutionära anpassningar. Tack Karin, Kim och Peter för värdefulla synpunkter på den här sammanfattningen. 31 Tack Jag vill tacka mina handledare för allt tålamod. Johan för allt du har lärt mig om vridande och vändande på idéer och uppslag. Peter för inspiration, alla barngrejer och för att du hjälpte mig att hålla näsan över vattenytan under en särskilt jobbig vecka. Jag vill tacka Gisela för att du alltid hälsat lika glatt, och för goda råd. Tack till Peter och Ingela för goda råd och trevligt jobb nere i växthuset. Tack alla som har jobbat i fält och räknat baljor Ade, Ana, Anna, Camilla, Jessica, John, Karin, Liv, Mia, Samira, Suzanne och Tove. Sofia för trevliga promenader. Åsa och Anna, mina alltid saknade rumskompisar. Åsa du lärde mig som kom utifrån lite om Botan. Anna du lärde mig att allt inte är mitt fel. Maria, tack för hela vår botaniska resa tillsammans men framförallt för att du höll kontakten när du hade valt en annan väg. Micke för diskussioner om livet, arbetet och makten. Tack för att jag slapp fika vid twin-peaksdjurparken någonstans i Dalslands djupaste avkrokar. Kristina för mammakläder, alla trevliga samtal och goda råd. Mathias, för alla tips och mycket uppmuntran inför det avslutande avhandlingsarbetet. Didrik för gemensam avhandlingsstress och för att du gav mig en knuff upp på vägen när jag var utan opplösning. Tack alla som var med på Mallis för en trevlig resa. Johan D, för att du lyssnade på trötthet och frustration. Kajsa för alla trevliga samtal om spindlar och musik. Leena för all uppmuntran. Hugo och Karin för trevligt sällskap på kurser. Sonja för allt trevligt ventilerande om barn och annat. Camilla och Jessica, utan er hjälteinsats med baljorna hade jag aldrig hunnit. Alla trevliga människor som jag har mött under min tid på Botan. Jag vill tacka alla mina vänner och släktingar för att ni finns kvar trots att jag ofta varit distraherad. Karin, tack för sällskap i fält, för tak över huvudet, för alla resor och för allt stöd när tillvaron inte kändes så hanterbar. Åsa för att du alltid är en vän var du än är. Lotta för all bio och alla fikasamtal, kom hem snart. Ana, because you once told me I had to try science. Elize for company when I was starting my project. John för dina tappra försök i fält och för att du alltid varit intresserad, Towe för att du alltid trott på min förmåga, Bengt för alla filosofiska diskussioner och mamma för att du älskar blommor. Karin F, Mona och Bengt för att ni passade Märta när dagiset kapsejsat. Märta och Kim, utan er hade det aldrig gått. Tack för att ni har väntat på mig. Nu kommer jag tillbaka! 32