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

Authors: COVERDALE, TYLER - Cornell University; MCGEARY, IAN - Princeton University; O'CONNELL, RYAN - University Of Florida; PALMER, TODD - University Of Florida; GOHEEN, JACOB - University Of Wyoming; SANKARAN, MAHESH - National Centre For Biological Sciences; Augustine, David; FORD, ADAM - University Of British Columbia; PRINGLE, ROBERT - Princeton University

Submitted to: Oikos
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/19/2019
Publication Date: 11/29/2019
Citation: Coverdale, T., McGeary, I., O'Connell, R., Palmer, T., Goheen, J., Sankaran, M., Augustine, D.J., Ford, A., Pringle, R. 2019. Strong but opposing effects of associational resistance and susceptibility on defense phenotype in an African savanna plant. Oikos. 128:1772-1782. https://doi.org/10.1111/oik.06644.
DOI: https://doi.org/10.1111/oik.06644

Interpretive Summary: Rangeland plant species vary in how palatable they are to livestock and wild herbivores, in some cases because different species have varying levels of investment in defenses such as spines, thorns or prickles. The degree of herbivory a plant experiences could also depend on the kinds of plants growing in its immediate neighborhood. Plant species with a moderate level of investment in defenses could potentially be eaten less when growing next to well-defended species (termed associational resistance), and eaten more when growing next to palatable, undefended species (termed associational susceptibility). This effect of neighborhood plants could also influence the degree to which the moderately defended species invests in defenses. We studied these interactions in an East African savanna that supported a combination of domestic cattle and multiple large wild herbivores. We examined how a species with moderate investment in spines (Sodom apple) invests in spines when growing in the vicinity of palatable grasses versus growing in the vicinity of Acacia shrubs that have a large investment in thorns. Sodom apple plants growing with palatable grasses had twice as many spines but were more heavily grazed relative to plants growing near Acacias. The neighborhood in which Sodom apple plant grew therefore explains why plants with high prickle density experienced suffered more damage by herbivores, while plants with low prickle density did not.

Technical Abstract: 1. 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 determines the mechanism(s), strength, and efficacy of associational resistance and susceptibility, the effect of neighbors on focal plant phenotype—particularly defense phenotype—remains poorly understood. 2. We used field surveys and a prickle-removal experiment at Mpala Research Centre (Kenya) to evaluate the efficacy of Solanum campylacanthum prickles against large mammalian herbivores. We then quantified the effects of spinescent Acacia trees on prickle density in S. campylacanthum with a series of surveys and long-term field experiments. We paired surveys of S. campylacanthum prickle density beneath and outside tree canopies with long-term herbivore exclosure experiments to evaluate whether associational resistance reduced defense investment by decreasing browsing damage. Likewise, we compared S. campylacanthum defense phenotype within and outside natural and experimental glades, which lack Acacia trees, to determine if associational susceptibility (i.e., enhanced browsing damage) increased defense investment. 3. Removing prickles increased browsing damage by c. 25% and surveys of browsing damage suggested that large mammalian herbivores tended to avoid prickles when browsing, despite the small size of S. campylacanthum prickles. As predicted, associational resistance and susceptibility had marked and opposing influences on S. campylacanthum phenotype: plants growing in close proximity to Acacia trees (or, analogously, within large herbivore exclosures) were significantly less browsed and produced c. 70-80% fewer prickles than conspecifics outside refuges, while individuals in naturally or experimentally treeless glades were more heavily browsed and produced nearly twice as many prickles as those in areas with tree refuges. 4. Synthesis: Our results suggest that associational resistance and susceptibility have strong but opposing effects on focal plant defense phenotype and that intraspecific variation in defense phenotype across habitats in this system is driven by variable herbivore damage. The counterintuitive pattern of greater browsing damage on more heavily defended plants, despite the efficacy of prickles against browsers, suggests that induced resistance may be primarily responsible for the observed intraspecific variation in defense phenotype in S. campylacanthum.