Grass leaf silicification: Natural selection for an inducible defense against herbivores

Abstract

Plants from four populations of three species of African grasses were collected from grasslands in Tanzania's Serengeti National Park that differ in the grazing intensity that they experience. Plants were grown in the laboratory in a factorial experiment in which variables were plant origin, species identification ofplants, defoliation intensity, and supply of soluble silicate in the nutrient medium. All plants accumulated silica in leafblades in the absence of soluble silicate from the nutrient medium. Plants native to the more heavily grazed grassland. accumulated more silica in their leaf blades than did plants from the less heavily grazed site. Blade silica content was higher-when plants were defoliated, indicating that silicification is an inducible defense against herbivores. The quantitative heterogeneity of this qualitatively homogeneous plant defense system may have contributed to the evolution of high species diversity in the grazing fauna.Grasses and grazing mammals have had an extended, intimate evolutionary history from their simultaneous appearance in the Eocene to their spectacular adaptive radiations during the Pliocene and Pleistocene (1-4). The evolution of hypsodont dentition during the faunal radiations provides presumptive evidence that plant leafsilicification was a major evolutionary trend in the Poaceae (5,6). In addition to silica's deleterious effects upon herbivores due to the mechanical abrasion of enamel surfaces (7), ingestion of plant silica is involved in the etiology of several pathological conditions in animals (8, 9). Adaptive radiation in grazing mammals and grasses was fundamentally different from the radiations of dicotyledonous plants and herbivorous insects (10). The latter were characterized by structural and chemical complexity ofthe plants and sophisticated feeding modes, chemical tolerances, and detoxification mechanisms within the animals (11)(12)(13)(14). Grasses, in contrast, are comparatively simple structurally and lack the diverse secondary chemistry characteristic of dicotyledons. They appear to be a comparatively uniform food source by comparison with dicotyledons. How did such comparatively simple anti-herbivore defenses as silicification of grass leaves lead to the adaptive radiation of a highly diverse grazing mammal fauna? We here-report an experiment with grasses native to an unmanaged ecosystem supporting some semblance of the Pleistocene megafauna. The results indicate that the diversity ofgrasses and the mammals that feed upon them may have been influenced by the quantitative heterogeneity ofa qualitatively homogeneous plant defense system. MATERIALS AND METHODSThe experimental design was a 24 factorial with the following variables: (i) Origin: plants were obtained from the heavily grazed (15-17) short grasslands of the southeastern Serengeti National Park in Tanzania and from a comparatively lightly grazed (15)(16)(17) Silica in leaf blades was determined by wet ashing and weighing (20). Data are expressed as a percentage of leaf dry weight. ...

Increased thorn length in Acacia depranolobium ?an induced response to browsing

“…Several other physical plant defenses have been shown to be inducible, including structural silica (McNaughton and Tarrants 1983), tree gum (Karban 1983), and leaf toughness (Schultz and Baldwin 1982). These physical defenses are mostly irreversible.…”

“…Induced resistance to insect attack has been inferred from increased production of chemical or physical defenses, or reduced fitness of herbivorous insects (Rhoades 1983; Schultz and Baldwin 1982;McNaughton and Tarrants 1983;Karban 1983;Karban and Carey 1984). Such plasticity in plant defenses allows plants to divert resources to defense only when they are needed, increasing overall efficiency of resource allocation.…”

Herbivore specific induction of silica-based plant defences

“…To date, only two studies have found evidence for induction of silica (McNaughton and Tarrants 1983;McNaughton et al 1985). This may be due to the fact that most studies examining potential damage-induced silica deposition in grass leaves have tested induction in response to mechanical damage (McNaughton and Tarrants 1983;McNaughton et al 1985;Brizuela et al 1986;Cid et al 1989;Cid et al 1990;Banuelos and Obeso 2000).…”

“…This may be due to the fact that most studies examining potential damage-induced silica deposition in grass leaves have tested induction in response to mechanical damage (McNaughton and Tarrants 1983;McNaughton et al 1985;Brizuela et al 1986;Cid et al 1989;Cid et al 1990;Banuelos and Obeso 2000). It has long been known that artificial Hartley and Lawton 1991).…”

Dynamics of Ni‐based defence and organic defences in the Ni hyperaccumulator, Streptanthus polygaloides (Brassicaceae)

“…With the exception of McNaughton & Tarrants (1983), no studies have attempted to place elemental plant defences into either category. McNaughton & Tarrants (1983) showed that silica contents of several African savanna grass species increased after exposure to simulated herbivory treatments ; thus, they considered silicification to be an inducible defence. The response of foliar metal concentrations of hyperaccumulators to herbivore damage has not been determined.…”