American Society of Naturalists

Lalasia Bialic-Murphy, Christopher D. Heckel, Robert M. McElderry, and Susan Kalisz (Jan 2020)

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Deer indirectly affect the reproductive strategy of an unpalatable forest perennial

While necessary for life to persist, reproduction is a costly endeavor. Many plants and animals can reproduce both sexually and asexually and can express both male and female form. To examine how human-induced changes in the environment alter a species reproductive strategy, Bialic-Murphy et al. studied a sexually labile understory perennial, Arisaema triphyllum (Jack in the pulpit), across a deer impact gradient. Arisaema is strongly influenced by environmental conditions, and individuals commonly switch between male and female form multiple times over their lifespan (40+ years). Humans have dramatically reduced the abundance of large carnivores in native ecosystems, which in turn has increased the density of large herbivores (e.g., white-tailed deer). Increased deer impact is known to have significant effects on soil dynamics, including a decrease in soil moisture and an increase in soil compaction. In this study, researchers show that increased deer impacts on environmental conditions result in delayed female sex expression for Arisaema to unsustainably large plant sizes and leads to more pronounced plant shrinkage following seed production, effectively increasing the cost of reproduction. Arisaema at high deer impact also reproduces less often and invest more in asexual reproduction than sexual reproduction. Populations at high deer impact sites are extremely male-biased, with only 7% of the sexually reproductive plants producing female flowers. These results illustrate the dramatic effects of human-induced change on the sex expression of plants in the forest understory.

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Abstract

Environmental conditions impose restrictions and costs on reproduction. Multiple reproductive options exist when increased reproductive costs drive plant populations toward alternative reproductive strategies. Using four years of demographic data across a deer impact gradient, where deer alter the abiotic environment, we parameterize a size-dependent integral projection model for a sexually labile and unpalatable forest perennial to investigate the demographic processes driving differentiation in the operational sex ratio (OSR) of local populations. In addition to a relative increase in asexual reproduction, our results illustrate that non-trophic indirect effects by overabundant deer on this perennial result in delayed female sex expression to unsustainably large plant sizes and leads to more pronounced plant shrinkage following female sex expression, effectively increasing the cost of reproduction. Among plants of reproductive age, increased deer impact decreases the size-dependent probability of flowering and reduces reproductive consistency over time. This pattern in sex expression skews populations toward female-biased OSRs at low deer impact sites and male-biased OSRs at intermediate and high deer impact sites. While this shift toward a male-biased OSR may ameliorate pollen limitation, it also decreases the effective population size when coupled with increased asexual reproduction. The divergence of reproductive strategies and reduced lifetime fitness in response to indirect deer impacts illustrate the persistent long-term effects of overabundant herbivores on unpalatable understory perennials.