Spiny plants, mammal browsers, and the origin of African savannas

Abstract

Savannas first began to spread across Africa during the Miocene. A major hypothesis for explaining this vegetation change is the increase in C 4 grasses, promoting fire. We investigated whether mammals could also have contributed to savanna expansion by using spinescence as a marker of mammal herbivory. Looking at the present distribution of 1,852 tree species, we established that spinescence is mainly associated with two functional types of mammals: large browsers and medium-sized mixed feeders. Using a dated phylogeny for the same tree species, we found that spinescence evolved at least 55 times. The diversification of spiny plants occurred long after the evolution of Afrotherian proboscideans and hyracoids. However, it is remarkably congruent with diversification of bovids, the lineage including the antelope that predominantly browse these plants today. Our findings suggest that herbivore-adapted savannas evolved several million years before fire-maintained savannas and probably, in different environmental conditions. Spiny savannas with abundant mammal herbivores occur in drier climates and on nutrient-rich soils, whereas fire-maintained savannas occur in wetter climates on nutrient-poor soils.Africa | Bovidae | coevolution | mammalian herbivory | savanna T he origin and spread of savannas have been topics of intensive research, but many questions remain. The C 4 grasses that dominate savannas emerged in the late Oligocene (∼30 Ma), but savannas only began to emerge as one of the world's major biomes in the late Miocene more than 20 My later (1). What changed to roll back the forests, allowing the rapid spread of grasslands? Ehleringer et al. (2) first linked the rise of savannas to a drop in atmospheric CO 2 , which would favor C 4 grasses over their C 3 grass predecessors. Low CO 2 can also reduce woody cover by increasing the risk of recruitment failure in woody plants whether from drought, fire, or browsing (3). However, the timing of the onset of low CO 2 is much earlier than the spread of savannas; therefore, although low CO 2 may have contributed to savanna expansion, it cannot explain the long time lag between C 4 origins and savanna spread. Climate change is the usual explanation for changing vegetation over time. Increased aridity in the late Miocene has been shown to cause the retreat of forests in North America and Eurasia, allowing grasslands to spread in their place (4, 5). However, large areas of extant savannas occur in climates that are wet enough to support forests and other closed woody types (6-8). Fires are frequent in high-rainfall savannas and have been considered the major agents accounting for open ecosystems in climates that can support forests. Fossil charcoal, mostly from marine cores, shows a surge in fire activity from the late Miocene correlated with the spread of savannas (9, 10). Phylogenetic studies have shown the emergence of fire-adapted woody plants from the late Miocene through to the Pleistocene in both Brazil and Africa, consistent with fossil evidence for increasing f...

Inserting Tropical Dry Forests Into the Discussion on Biome Transitions in the Tropics

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Good neighbors make good defenses: associational refuges reduce defense investment in African savanna plants

“…Here, we show that, by reducing the frequency and intensity of browsing damage, associational refuges cause predictable variation in defense phenotype for species that respond to browsing by inducing defenses. In African savannas, the distribution and abundance of associational refuges is determined by a combination of biotic and abiotic factors (Sankaran et al 2005, Staver et al 2011, Charles-Dominique et al 2016, while the prevalence of induced resistance is driven largely by intense, yet spatiotemporally variable, topdown pressure by large mammalian herbivores (Augustine 2010). In African savannas, the distribution and abundance of associational refuges is determined by a combination of biotic and abiotic factors (Sankaran et al 2005, Staver et al 2011, Charles-Dominique et al 2016, while the prevalence of induced resistance is driven largely by intense, yet spatiotemporally variable, topdown pressure by large mammalian herbivores (Augustine 2010).…”

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

“…A long‐standing conundrum in ecology is how plants persist in the face of intense herbivory when resources are limited. Plants growing in African savannas have a long history of co‐evolution with a diverse array of mammalian herbivores, and have evolved a range of different strategies to deal with herbivory (Charles‐Dominique et al, ). Classical defence theory suggests that plants can respond to herbivory in two ways, i.e.…”