Bridging the physiology and ecology of hemiparasitic plants

Abstract

Metabolism based on photosynthesis is a defining feature of plants. However, some flowering plant lineages have adopted a heterotrophic lifestyle based on parasitism, either reducing or completely abandoning their ability to photosynthesize. Approximately 1-2% of all angiosperms directly parasitize other plants, attaching to the vascular tissue of one or more host plants using specialized structures called haustoria. All lineages that have evolved away from autotrophy display profound changes in morphological, biochemical, and molecular traits. In addition, the adoption of a parasitic lifestyle necessitates certain physiological adaptations that allow the parasite to locate, attach to, and effectively siphon resources away from the host. As a consequence of the expression of these physiological traits, parasitic plants can occupy unique ecological roles in their natural communities. Hemiparasites, parasitic plants that can photosynthesize, both compete with and parasitize host plants, simultaneously acting as producers and consumers. Hemiparasites often disproportionately parasitize certain species in a community, changing the competitive dynamics between host and non-host species and affecting vegetation structure and diversity within a plant community. However, while research into the role of hemiparasites in their communities is growing, it is still largely based on only a few genera. Furthermore, while some hemiparasitic species are considered to be keystone species, profoundly impacting community structure, others exert little to no effect. However, due to a relative lack of representation of diverse genera in hemiparasitic plant literature, we cannot adequately address the mechanisms of such variation. I examined the physiology and ecology of the Castillejinae tribe in the Orobanchaceae, a species-rich yet largely understudied group of annual and perennial genera. In several greenhouse experiments, I assessed the resource flow between host and hemiparasite and investigated whether the pattern of resource gain varied based on hemiparasite growth form (annuals or perennials). Like other hemiparasitic plants, that these genera had higher concentrations of mineral nutrients than their hosts. However, by experimentally allowing or preventing parasitism, I was able to show that phosphorous limits the growth of unattached hemiparasites. Furthermore, unattached hemiparasites invested more in their roots than attached hemiparasites. Thus, hemiparasites in the Castillejinae conform to physiological patterns observed with other hemiparasites for several key traits. I expanded my study group to North American hemiparasites as a whole to study the interactions of these hemiparasites with their natural communities. Through analysis of vegetation plots across national parks in the United States, I found that hemiparasites are associated with higher evenness in plant communities across the United States, however, their relationship with richness is not as pronounced. Almost all of the species in this dataset are absent from hemiparasitic plant literature, suggesting that the current research only captures part of the mechanisms by which a hemiparasite can affect its community. Building on my research and the existing literature, I propose that the life history may be an important mediator influencing the physiology of hemiparasites, and therefore, their relationships with their hosts and communities. This body of physiological, ecological, and theoretical work enhances our understanding of hemiparasitic plant biology. Given that hemiparasites are a common component of the world flora, this research represents an important step towards incorporating hemiparasites into community ecological theory.