Defence against vertebrate herbivores trades off into architectural and low nutrient strategies amongst savanna Fabaceae species

Abstract

Herbivory contributes substantially to plant functional diversity and in ways that move far beyond direct defence trait patterns, as effective growth strategies under herbivory require modification of multiple functional traits that are indirectly related to defence. In order to understand how herbivory has shaped plant functional diversity, we need to consider the physiology and architecture of the herbivores and how this constrains effective defence strategies. Here we consider herbivory by mammals in savanna communities that range from semi‐arid to humid conditions. We posited that the saplings of savanna trees can be grouped into two contrasting defence strategies against mammals, namely architectural defence versus low nutrient defence. We provide a mechanistic explanation for these different strategies based on the fact that plants are under competing selection pressures to limit herbivore damage and outcompete neighbouring plants. Plant competitiveness depends on growth rate, itself a function of leaf mass fraction (LMF) and leaf nitrogen per unit mass (Nm). Architectural defence against vertebrates (which includes spinescence) limits herbivore access to plant leaf materials, and partly depends on leaf‐size reduction, thereby compromising LMF. Low nutrient defence requires that leaf material is of insufficient nutrient value to support vertebrate metabolic requirements, which depends on low Nm. Thus there is an enforced tradeoff between LMF and Nm, leading to distinct trait suites for each defence strategy. We demonstrate this tradeoff by showing that numerous traits can be distinguished between 28 spinescent (architectural defenders) and non‐spinescent (low nutrient defenders) Fabaceae tree species from savannas, where mammalian herbivory is an important constraint on plant growth. Distributions of the strategies along an LMF‐Nm tradeoff further provides a predictive and parsimonious explanation for the uneven distribution of spinescent and non‐spinescent species across water and nutrient gradients.

A thorny issue: Woody plant defence and growth in an East African savanna

“…Specifically, we asked the following questions: (a) Are the defence strategies observed in the dominant fine‐ and broad‐leaved woody species of this East African savanna similar to those documented in other savanna ecosystems—e.g. low nutrient/high chemical defence strategy (sensuTomlinson et al, ) versus nutrition and defence strategy (Tomlinson et al, ; Wigley et al, )? (b) Are there differences in the extent to which alternative defence strategies are successful at resisting herbivory, i.e.…”

“…see Stamp, 2003 for a review of the different theories), it is less clear under what conditions (i.e. resource and herbivory levels) plants should invest in structural defences and more specifically in spines as none of the existing defence theories are able to clearly predict the incidence of spinescence (Grubb, 1992;Hanley, Lamont, Fairbanks, & Rafferty, 2007;Herms & Mattson, 1992;Tomlinson et al, 2016).…”

“…same soil fertility status) employ similar suites or combinations of defences (defence syndromes). We note that "syndrome" or "strategy" and "cluster" or "group" have often been used interchangeably in the plant defence literature (Agrawal & Fishbein, 2006;Da Silva & Batalha, 2011;Tomlinson et al, 2016). For the sake of expediency, we consistently use "strategy" and "group" hereafter to encompass the definitions of syndrome and cluster respectively.…”

“…which traits are more inducible? Based on previous work (Da Silva & Batalha, 2011;Tomlinson et al, 2016;Wigley et al, 2018), we expected to find different defence strategies being employed by woody plants in our study system with various combinations of chemical and structural defences. We expected that these different strategies will determine how successful plants are at resisting herbivory, i.e.…”

The impact of herbivore exclusion on forb diversity: Comparing species and functional responses during a drought

“…Conversely, it has been widely documented that herbivores enhance, or at least maintain species diversity by removing some, but not all biomass of these dominant species, thereby reducing competitive effects between species (Jacobs & Naiman, ; Olff & Ritchie, ; Riginos et al, ; Savadogo, Tiveau, Sawadogo, & Tigabu, ). The inherent increase in system heterogeneity by herbivores through the creation of grazing patches, wallows and game paths allows more species which are functionally different to coexist (Jacobs & Naiman, ; Olff & Ritchie, ; Savadogo et al, ), thereby enhancing functional diversity (Tomlinson et al, ).…”