“Biotic interactions contribute to the geographic range limit of an annual plant: herbivory and phenology mediate fitness beyond a range margin”

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John W. Benning, Vincent M. Eckhart, Monica A. Geber, and David A. Moeller (June 2019)

The DOI will be https://dx.doi.org/10.1086/703187

Using multiple lines of evidence, Benning et al. show how biotic interactions can contribute to geographic range limits

Can ravenous rabbits restrict ranges?

Clarkia xantiana ssp. xantiana.
(Credit: John W. Benning)

Palm trees don’t grow in Minnesota, and you won’t find any redwoods in Texas. These limits to species’ distributions are one of the most readily apparent ecological phenomena, but are poorly understood. And as environments change worldwide, conservationists and policy makers increasingly need to know how these environmental changes will affect species distributions. Benning et al. show that for a California endemic plant, herbivory by small mammals may play a large role in setting the plant’s range limit.

The researchers have been working with the plant Clarkia xantiana ssp. xantiana for over a decade in the southern Sierra Nevada foothills of California. In a previous experiment where they transplanted seeds outside the range limit in order to see if they could survive there, they noticed that many of the plants were eaten by rabbits and hares. However, plants at the center of the range were rarely eaten. Benning et al. were interested in three main questions: 1) how does the probability of herbivory change going from the center to beyond the range limit; 2) how much does this fatal herbivory lower average fitness in transplanted populations outside the range edge; and 3) is there a specific trait that makes the plant more susceptible to herbivory? Using both field and simulation approaches, they found a sharp increase in herbivory near the range edge, which led to large decreases in fitness outside the range, and found evidence that the slow development of C. x. xantiana exposes it to high rates of herbivory outside its range. Together, these results provide one of the most comprehensive explorations of how biotic interactions can influence large-scale distributions.


Abstract

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 several-fold 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, C. x. 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 lend empirical support to recent developments in range limits theory.