Strong but opposing effects of associational resistance and susceptibility on defense phenotype in an African savanna plant

Abstract

The susceptibility of plants to herbivores can be strongly influenced by the identity, morphology and palatability of neighboring plants. While the defensive traits of neighbors often determine the mechanism and strength of associational resistance and susceptibility, the effect of neighbors on plant defense phenotype remains poorly understood. We used field surveys and a prickle‐removal experiment in a semi‐arid Kenyan savanna to evaluate the efficacy of physical defenses against large mammalian herbivores in a common understory plant, Solanum campylacanthum. We then quantified the respective effects of spinescent Acacia trees and short‐statured grasses on browsing damage and prickle density in S. campylacanthum. We paired measurements of prickle density beneath and outside tree canopies with long‐term herbivore‐exclusion experiments to evaluate whether associational resistance reduced defense investment by decreasing browsing damage. Likewise, we compared defense phenotype within and outside pre‐existing and experimentally created clearings to determine whether grass neighbors increased defense investment via associational susceptibility. Removing prickles increased the frequency of browsing by ~25%, and surveys of herbivory damage on defended leaves suggested that herbivores tended to avoid prickles. As predicted, associational resistance and susceptibility had opposing effects on plant phenotype: individuals growing beneath Acacia canopies (or, analogously, within large‐herbivore exclosures) had a significantly lower proportion of their leaves browsed and produced ~ 70–80% fewer prickles than those outside refuges, whereas plants in grass‐dominated clearings were more heavily browsed and produced nearly twice as many prickles as plants outside clearings. Our results demonstrate that associational resistance and susceptibility have strong, but opposing, effects on plant defense phenotype, and that variable herbivore damage is a major source of intraspecific variation in defense phenotype in this system.

Landscape variation in defense traits along gradients of multiple resources and mammalian herbivory

“…Our field survey limits our power of inference and field experiments that manipulate different resource levels and herbivory are likely necessary to determine cause-effect relationships of resources and herbivory risk on defense traits. Although our analysis is limited to a single species, S. incanum represents a type of “model” plant for intraspecific variation studies because it exhibits multiple types of defenses, is common in an unusually wide variety of environments (i.e., was present at 43 of the 61 sites) and is consumed by multiple mammalian herbivore species (Kartzinel et al 2015, Coverdale et al 2019, Veldhuis et al, unpubl.). Even though our work maybe easily extended to a vast majority of species in Solanaceae that invest in different types of defenses, future work on different plant families will help evaluate any generality of our results.…”

“…Study organism: Solanum incanum (hereafter Solanum ), is a pan-African and pan-Asian herbaceous plant which is consumed by several browser and mixed-feeding herbivore species (hereafter “browsers”) such as impala, elephant, gazelles and eland (Kartzinel et al 2015, Coverdale et al 2019, Veldhuis et al, unpubl.). Even within the Serengeti, Solanum is widely distributed and is almost as common as Digitaria macroblephara and Themeda triandra , two of the most abundant grasses in the park.…”

“…Unlike the grasses, Solanum incanum invests in both physical and chemical defenses. Their stems have spines which can vary drastically in density and have been shown to be inducible by herbivory (Coverdale et al 2019). Additionally, it produces both phenolics and alkaloids, the latter of which is mostly present in the fruits.…”

“…Firstly, chemical defenses may be less effective against mammalian herbivores that may mix secondary metabolites from multiple consumed plant species and thus dilute the impact of any single chemical (Mattson 1980). Secondly, mammalian consumption of whole or large portions of an individual plant in a single bite poses a different set of challenges to plants than invertebrate herbivory (Sanson 2006) and possibly results in different types of anti-herbivore strategies, such as avoidance through divaricate branching or structural defenses such as spines (Hanley et al 2007, Tomlinson et al 2016, Coverdale et al 2019, Wigley et al 2019). Unlike most chemical defenses, resources allocated to physical defenses cannot be metabolically reverted to resources for future plant growth and reproduction.…”

Experimental insect suppression causes loss of induced, but not constitutive, resistance in Solanum carolinense

“…In support of this notion, investigations spanning macroevolutionary (Becerra et al, 2009; Charles‐Dominique et al, 2016) and microevolutionary (Bode & Kessler, 2012; Kalske & Kessler, 2020) timescales have repeatedly found tight correspondence between plant investment in resistance traits and the intensity of herbivory. The same is true regarding spatial variation in herbivory across landscapes (Coverdale et al, 2018, 2019).…”