From plants to predators: investigating the phytochemical landscape from the herbivore's perspective

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Authors

Diethelm, Aramee

Issue Date

2023

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Dissertation

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Asclepias , Danaus plexippus , phytochemistry , plant-insect-predator , tritrophic

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The phytochemical landscape—the diverse and spatially heterogeneous distribution of plant chemical compounds—plays a crucial role in shaping tritrophic interactions. Focused on the perspective of herbivores, this dissertation investigates variations in plant chemistry along an environmental gradient, the responses of herbivore predators to climatic conditions, and the resulting impacts on trophic dynamics. Specifically, it presents an overview of how environmental stress, predator-exposure, and food plant identity interact to influence the larval performance of a specialist Lepidopteran, the monarch butterfly (Danaus plexippus L.), which is exclusively reliant on Asclepias (milkweed) species during its larval stage. Focusing on two prevalent species of western milkweed (A. fascicularis and A. speciosa), this dissertation provides invaluable insights into the relationships between herbivores, their natural enemies, and the ever-changing environment that they inhabit.Chapter 1 delves into the effects of climate at the seed source on plant chemical plasticity in response to water stress. By employing common gardens of A. fascicularis and A. speciosa sourced from sites across an aridity gradient, the study uncovers patterns of constitutive and induced expression of antioxidant compounds in the chemical class flavonols. Flavonols were found in higher constitutive concentrations in plants sourced from drier sites, and both species exhibited increased leaf flavonol concentrations in response to water stress. Interestingly, A. fascicularis plants from wetter sites displayed higher flavonol plasticity, while A. speciosa demonstrated weaker patterns. Such opposing patterns of constitutive and induced flavonol expression led to a reduction in the variation between populations under water stress, suggesting the influence of local adaptation in shaping phytochemical strategies for water limitation. Chapter 2 investigated the consequences of combined water and herbivory stress on plant traits and phytochemical diversity using A. fascicularis milkweeds. With this study, I found that water limitation alone increased the evenness of UV-absorbent secondary metabolites (plant defensive phytochemicals), whereas herbivory alone increased the richness of metabolites. However, plants experiencing combined water and herbivory stress displayed similar phytochemical diversity to control plants, associated with a reduction in relative growth rates. Leaf chemistry average constitutive levels and plasticities exhibited clinal variation corresponding to seed-source water deficits, suggesting climatic history can influence phytochemical plasticity, while co-occurring herbivory disrupted these patterns. Chapter 3 builds upon the previous studies to explore the tritrophic perspective, with a focus on the non-consumptive impacts of predators on monarch larval performance. Here, I investigated how exposure to predators affected larval development and survival, and whether those effects could be modulated by food plant identity, using the two species of milkweed from Chapter 1. I found that monarchs developed more slowly when exposed to predators, particularly when feeding on A. speciosa. Overall, the results suggest that larvae developing on architecturally simple A. speciosa plants spent more time avoiding predators and less time eating compared to larvae on bushier, more branching A. fascicularis plants. The findings underscore the role of predation risk in monarch larval performance and highlight the importance of larval food plant species in mediating non-consumptive predator effects. Lastly, Chapter 4 examines the interplay between predator exposure, abiotic conditions, and food plant identity in shaping monarch larval performance across a water-availability gradient. Exposure to predators significantly reduced larval survival, and had sub-lethal effects where increasing diversity for predator communities lead to greater delays in larvae reaching adulthood. Moreover, extreme climatic conditions influenced the developmental timing and adult size of monarch larvae, further highlighting the complexity of interactions between biotic and abiotic stressors impacting larval success. In conclusion, this dissertation underscores the vital role of the phytochemical landscape in shaping tritrophic interactions. Specifically, it sheds light on how environmental stress, predator-exposure, and food plant identity interact to influence the larval performance of a specialist herbivore, the monarch butterfly.

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