Biotic Interactions Contribute to the Geographic Range Limit of an Annual Plant: Herbivory and Phenology Mediate Fitness beyond a Range Margin

Species' geographic distributions have already shifted during the Anthropocene. However, we often do not know what aspects of the environment drive range dynamics, much less which traits mediate organisms' responses to these environmental gradients. Most studies focus on possible climatic limits to species' distributions and have ignored the role of biotic interactions, despite theoretical support for their importance in setting distributional limits. We used field experiments and simulations to estimate contributions of mammalian herbivory to a range boundary in the Californian annual plant Clarkia xantiana ssp. xantiana. A steep gradient of increasing probability of herbivory occurred across the boundary, and a reanalysis of prior transplant experiments revealed that herbivory drove severalfold declines in lifetime fitness at and beyond the boundary. Simulations showed that populations could potentially persist beyond the range margin in the absence of herbivory. Using data from a narrowly sympatric subspecies, Clarkia xantiana parviflora, we also showed that delayed phenology is strongly associated with C. xantiana ssp. xantiana's susceptibility to herbivory and low fitness beyond its border. Overall, our results provide some of the most comprehensive evidence to date of how the interplay of demography, traits, and spatial gradients in species interactions can produce a geographic range limit, and they lend empirical support to recent developments in range limits theory.