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Plant-Seed Predator Interactions – Ecological and Evolutionary Aspects

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Plant-Seed Predator Interactions – Ecological and Evolutionary Aspects 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 pre- dispersal 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 dis- tribution 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 pre- dispersal seed predation in 46 host populations of the perennial herb Lathy- rus vernus . I recorded damage by beetle pre-dispersal seed predators, mainly Apion opeticum and Bruchus atomarius with different host ranges on L. ver- nus 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 in- creased 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 preda- tion 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 ad- vanced ability to locate fruits with high probability of retention. Taken to- gether, different factors influencing abundance of the seed predator species, different preferences, and context dependent trait selection are likely to re- sult in complex spatio-temporal variation in overall seed losses and trait selection in the common host plant. Keywords – apparent competition, community context, fruit abortion, de- fence, host range, monophagous, offence, oligophagous, plant-animal inter- actions, 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 varia- tion. 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 oc- casional seed predator. Manuscript . IV Östergård, H., P. A. Hambäck, and J. Ehrlén. 2007. Pre-dispersal seed predation: The role of fruit abortion and selective oviposi- tion. 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 inter- actions, 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. re- productive organs, seeds or seedlings. Both mutualistic and antagonistic interactions between plants and animals have important and sometimes re- ciprocal 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 re- source 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, pre- dispersal 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 in- sects are often specialized on one or a few host plants. The evolution of spe- cialization in herbivorous insects is suggested to be a trade-off between ad- aptations to a particular host trait and the ability to utilize multiple hosts (Jaenike 1990, Thompson 1994, Agrawal 2000). The commonness of spe- cialization 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 effec- tiveness 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 mono- phagous to polyphagous, and the intermediate oligophagous species, may have differential effects on the plant due to differences in abundance or pref- erence. 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, tempo- ral 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 com- position 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
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