Mechanisms underlying plant sexual dimorphism in multi‐trophic arthropod communities

Abstract

A growing body of research documents the importance of plant genetic effects on arthropod community structure. However, the mechanisms underlying these effects are often unclear. Additionally, plant genetic effects have largely been quantified in common gardens, thus inflating the estimates of their importance by minimizing levels of natural variation. Using Valeriana edulis, a dioecious plant with genetically based sex determination, we conducted surveys and experiments on wild-grown individuals to document field patterns of arthropod association between the sexes and the mechanisms underlying these plant genetic effects. Three years of surveys revealed strong and consistent sex-biased arthropod association in wild-grown plants: female plants supported 4-fold, 1.5-fold, and 4-fold higher densities of aphids, aphid predators, and aphid-tending ants, respectively, compared to males. There was mixed evidence that the female bias for aphids was due to higher plant quality, while we found no difference between plant sexes in aphid preference or the top-down effects of predators and tending ants. Female bias for ants was due to both the greater attractiveness of female plants (direct effect mediated by floral nectar) and an independent, weaker effect of higher aphid abundance on females (density-mediated indirect effect). Conversely, the female bias for predators was driven solely by the greater attractiveness of female plants. We did not find interaction modification, i.e., ant-aphid and predator-aphid interactions were equivalent between plant sexes. Plant sex explained 0.24%, 2.28%, and 4.42% of the variance in aphids, predators, and ants, respectively, values comparable to but slightly weaker than those previously reported from common-garden studies. In contrast to the prediction of diminished plant genetic effects with increasing trophic level, we show how weak indirect effects on predators and parasitoids (via herbivores) can be complemented by strong direct effects via common plant traits (floral resources). In summary, we document direct and indirect effects of genetically based sex on a multi-trophic arthropod community that were expressed in wild-grown plants across multiple years.

Relative effects of genetic variation sensu lato and sexual dimorphism on plant traits and associated arthropod communities

“…Consistent with our results, past studies have shown female plants to recruit more natural enemies (Mooney et al 2012a;Petry et al 2013) by increasing the availability of floral resources that provide nutritional benefits (i.e., nectar) to associated arthropod communities (Ashman and King 2005;Wäckers et al 2005;Pacini and Nepi 2007). Such effects can increase indirect defenses from predators and parasitoids attracted to these floral resources (Cepeda-Cornejo and Dirzo 2010).…”

“…Sexual dimorphism is another important axis of genetic variation that underlies variation in ecologically important traits and may thus have consequences for plant-associated arthropod communities (Petry et al 2013). In particular, the separation of reproductive roles in dioecious plants (separate males and females) has been hypothesized to drive divergence in resource allocation between males and females (Lloyd and Webb 1977;Delph 1999).…”

“…Similarly, Boecklen et al (1990) found that male willows supported higher densities of five species of tenthredinid sawflies than do female willows. However, plant sex might also determine the structure of associated multitrophic communities (Petry et al 2013;Kabir et al 2014;Abdala-Roberts et al 2016). For example, Petry et al (2013) found higher predator to herbivore ratios on Valeriana edulis females relative to males.…”

“…However, plant sex might also determine the structure of associated multitrophic communities (Petry et al 2013;Kabir et al 2014;Abdala-Roberts et al 2016). For example, Petry et al (2013) found higher predator to herbivore ratios on Valeriana edulis females relative to males. Such examples demonstrate that sexual dimorphism can strongly influence plant-arthropod interactions, but less is known about the effects of sexual dimorphism on diverse multitrophic communities.…”

Plant‐sex‐biased tritrophic interactions on dioecious willow

“…Petry et al (2013) also found that insect predators were more abundant on female plants in a system based on Valeriana edulis. The present study is unique in that it shows not only predictable plant sex effects on the densities of herbivores and predators, but also on the predation pressure on the herbivores, as well as a mechanism involving plant effects on predator performance as a candidate key driver behind the observed patterns.…”