Effect of abrasive properties of sedges on intestinal absorptive surface and Resting Metabolic Rate of the root voles

Abstract

Recent studies on grasses and sedges suggest that the induction of a mechanism reducing digestibility of plant tissues in response to herbivore damage may drive rodent population cycles. This defence mechanism seems to rely on the abrasive properties of ingested plants. However, the underlying mechanism has not been demonstrated in small wild herbivores. Therefore, we carried out an experiment in which we determined the joint effect of abrasive sedge components on the histological structure of small intestine as well as resting metabolic rate (RMR) of the root vole (Microtus oeconomus). Histological examination revealed that voles fed with a sedgedominated diet had shorter villi composed from narrower enterocytes in duodenum, jejunum and ileum. Reduction in the height of villi decreased along the small intestine. Activity of the mucus secretion increased along the small intestine and was significantly higher in the ileum. The intestinal abrasion exceeded the compensatory capabilities of voles, which responded to a sedge-dominated diet by a reduction of body mass and a concomitant decrease in whole body RMR. These results explain the inverse association between body mass and the probability of winter survival observed in voles inhabiting homogenous sedge wetlands. KEY WORDS: Body mass, Plant defensive mechanism, Sedges, Silicon, Small intestine INTRODUCTIONGrasses and sedges dominate many terrestrial ecosystems and are the food base for numerous cyclical populations of small herbivores. This plant food contains a high concentration of silicon (Hodson et al., 2005), which together with fibre (Vincent, 1982;Grzelak et al., 2011), increases its abrasive properties (Montagne et al., 2003;. The abrasive properties of this plant food have been proposed as an anti-herbivore defence mechanism (Massey et al., 2008). Our previous studies showed that changes in the silicon concentration in fibrous tussock sedge (Carex appropinquata Schumacher 1801) were induced by a high density of cyclical population of the root voles (Microtus oeconomus Pallas 1776) at the end of the previous summer. We also found that smaller (lighter) voles were characterised by lower mortality during early winter Zub et al., 2014), which might be correlated with the low quality of their food base. However, the underlying proximate mechanism promoting smaller individuals is not known. Low body mass of voles feeding on a highly silicated and fibrous diet (Massey et al., 2008) may reflect the need to reduce absolute energy requirements (Ergon et al., 2004), to bring them into line with reduced digestive efficiency . This efficiency may be compromised because of a reduction of the intestinal surface and its function of nutrient absorption, stemming from the mechanical abrasion of the apex of villi where the widest mature enterocytes, which produce digestive enzymes, are located (Montagne et al., 2003;Abbas et al., 1989;Barker et al., 2008). However, as far as we know the above putative mechanism has not yet been demonstrated in the context of the ...

The ecology of herbivore‐induced silicon defences in grasses

“…Nevertheless, the work in Polish and English grassland systems, including the advances in understanding the effects of eating high‐silicon diets on animals’ digestive physiology (Wieczorek et al . ), gives some support to the hypothesis that silicon defences may drive vole population cycles. The next step is to expand these studies to understand how local effects of silicon on vole meta‐populations drive population cycles at a landscape scale.…”

Population‐level manipulations of field vole densities induce subsequent changes in plant quality but no impacts on vole demography

“…In voles, evidence compatible with a possible reciprocal negative feedback between grazing and silicon induction has been observed under laboratory conditions; high levels of vole grazing increased silicon levels by up to 400% (Garbuzov, Reidinger, & Hartley, ; Massey, Ennos, & Hartley, 2007b), in turn significantly reducing vole growth rates, possibly because silicon impeded voles’ ability to extract nitrogen from food (Massey & Hartley, ). More recently, the abrasive properties of silicon phytoliths have also been shown to increase tooth wear in voles (Calandra, Zub, Szafrańska, Zalewski, & Merceron, ), as well as damage their small intestine, reducing body mass and metabolic rate (Wieczorek, Szafrańska, Labecka, Lázaro, & Konarzewski, ). Population models incorporating the observed silicon induction response, and the assumption that the empirical relationship between past vole density and timing of onset of vole spring reproduction (Ergon et al., ) is mediated by leaf silicon concentrations, consistently predicted cyclic changes in vole population densities (Reynolds et al., ).…”

Silicon-based plant defences, tooth wear and voles

“…1A), were considered in this study. Ten individuals were raised in laboratory conditions on two different pelleted diets: the Sdiet and the C-diet (see tables S1 and S2 in Wieczorek et al, 2015a for details). One of the root voles (Table S1) was removed from the analysis because of potential surface alteration.…”

“…Instead, intestinal damage (Wieczorek et al, 2015a) and resistance to cell crushing (Hunt et al, 2008) are more likely to be responsible for the cyclic mortality of vole populations due to plant defences. Yet, DMTA has been proven to indicate dietary abrasiveness in a wide range of mammals, so, if confirmed by future studies on voles, it could be used as a proxy of leaf Si concentration.…”

“…First, silicon has been found to induce intestinal abrasion, leading to a decrease in body mass and in whole-body resting metabolic rate (Wieczorek et al, 2015a). Second, the presence of phytoliths lining the cell walls may prevent the crushing of cells, so the herbivores extract less energy from silicon-rich monocotyledons (Hunt et al, 2008).…”