Plant secondary metabolites and primate food choices: A meta-analysis and future directions.

The role of plant secondary metabolites (PSMs) in shaping the feeding decisions, habitat suitability, and reproductive success of herbivorous mammals has been a major theme in ecology for decades. Although primatologists were among the first to test these ideas, studies of PSMs in the feeding ecology of non-human primates have lagged in recent years, leading to a recent call for primatologists to reconnect with phytochemists to advance our understanding of the primate nutrition. To further this case, we present a formal meta-analysis of diet choice in response to PSMs based on field studies on wild primates. Our analysis of 155 measurements of primate feeding response to PSMs is drawn from 53 studies across 43 primate species which focussed primarily on the effect of three classes of PSMs tannins, phenolics, and alkaloids. We found a small but significant effect of PSMs on the diet choice of wild primates, which was largely driven by the finding that colobine primates showed a moderate aversion to condensed tannins. Conversely, there was no evidence that PSMs had a significant deterrent effect on food choices of non-colobine primates when all were combined into a single group. Furthermore, within the colobine primates, no other PSMs influenced feeding choices and we found no evidence that foregut anatomy significantly affected food choice with respect to PSMs. We suggest that methodological improvements related to experimental approaches and the adoption of new techniques including metabolomics are needed to advance our understanding of primate diet choice.

Cold temperature improves tannin tolerance in a granivorous rodent.

The foraging ecology of mammalian herbivores is regulated in part by their ability to detoxify plant secondary metabolites (PSM). Ambient temperature has been shown to alter liver function in rodents and the toxicity of some PSMs, but little is known about the physiological and nutritional consequences of consuming PSMs at different ambient temperatures. Furthermore, the effect of ambient temperature on the response of mammals to the most ubiquitous class of PSM, tannins, is unknown. We measured the effect of temperature and tannin intake on liver function, and the subsequent effect on the tannin tolerance of wild Japanese wood mice, Apodemus speciosus. The experiment involved acclimation to one of two ambient temperatures (10°C or 20°C) followed by acclimation to a diet of acorns (6.2% tannin DW). Liver function was measured both before and after acclimation to acorns by measuring the clearance time of a hypnotic agent. Finally, the mice were fed only acorns in a 5-day feeding experiment to assess their tolerance to tannin in the diet. Acclimation to acorns had a significant effect on liver function, but the direction of this effect was dependent on ambient temperature. Acorn consumption improved the liver function of wood mice at 10°C, but reduced liver function at 20°C, revealing a complex relationship between ambient temperature and tannin intake on liver function. Furthermore, mice with better liver function, indicated by faster clearance of the hypnotic agent, exhibited higher protein digestibility on an acorn-only diet, indicative of higher tannin tolerance. These results suggest that environmental temperature plays a significant role in the tolerance of A. speciosus to tannins, providing new insight into their seasonal feeding behaviour and winter ecology. We contend that cold-induced tannin tolerance may help to explain the population dynamics of mammalian herbivores with seasonal changes in the tannin content of their diet, and inform predictions about the response of these animals to a changing climate.

The Use of Polyethylene Glycol in Mammalian Herbivore Diet Studies: What Are We Measuring?

Polyethylene glycol (PEG) has been used to study the intake and digestion of tannin-rich plants by mammalian herbivores because it preferentially binds to tannins. However, it is not clear whether the responses of herbivores to dietary PEG is due to increased protein availability from the release of tannin-bound protein, amelioration of tannin effects, or whether PEG also may bind to other compounds and change their activity in the gut. We used three native New Zealand tree species to measure the effect of PEG on the amount of foliage eaten by invasive common brushtail possums (Trichosurus vulpecula) and on in vitro digestible nitrogen (available N). The addition of PEG increased the in vitro available N content of Weinmannia racemosa foliage, and possums ate significantly more PEG-treated foliage than untreated foliage. However, possums also ate more PEG-treated Fuchsia excorticata foliage, even though PEG did not increase in vitro available N in this species. Possums ate very little Melicytus ramiflorus, regardless of PEG treatment, even though M. ramiflorus contained the highest concentration of in vitro available N. These results prompted us to use PEG and a protein supplement, casein, to manipulate the available N concentration of diets containing ground eucalypt foliage, a well-studied food species for possums. Again, the response of possums to PEG was independent of changes in in vitro available N. In addition, altering the protein content of the diet via the addition of casein did not affect how much food the possums consumed. We conclude that the effects of PEG on dry matter intake by mammalian herbivores are not due solely to the release of tannin-bound protein. There is need for a better understanding of PEG-tannin interactions in order to ensure that the use of PEG in nutritional studies does not outstrip an understanding of its mechanisms of action.

Foliar Nutritional Quality Explains Patchy Browsing Damage Caused by an Invasive Mammal.

Introduced herbivores frequently inflict significant, yet patchy damage on native ecosystems through selective browsing. However, there are few instances where the underlying cause of this patchy damage has been revealed. We aimed to determine if the nutritional quality of foliage could predict the browsing preferences of an invasive mammalian herbivore, the common brushtail possum (Trichosurus vulpecula), in a temperate forest in New Zealand. We quantified the spatial and temporal variation in four key aspects of the foliar chemistry (total nitrogen, available nitrogen, in vitro dry matter digestibility and tannin effect) of 275 trees representing five native tree species. Simultaneously, we assessed the severity of browsing damage caused by possums on those trees in order to relate selective browsing to foliar nutritional quality. We found significant spatial and temporal variation in nutritional quality among individuals of each tree species examined, as well as among tree species. There was a positive relationship between the available nitrogen concentration of foliage (a measure of in vitro digestible protein) and the severity of damage caused by browsing by possums. This study highlights the importance of nutritional quality, specifically, the foliar available nitrogen concentration of individual trees, in predicting the impact of an invasive mammal. Revealing the underlying cause of patchy browsing by an invasive mammal provides new insights for conservation of native forests and targeted control of invasive herbivores in forest ecosystems.

A faecal index of diet quality that predicts reproductive success in a marsupial folivore.

Estimating the nutritional value of a herbivore's diet is difficult because it requires knowing what the animal eats, the relative quality of each component and how these components interact in relation to animal physiology. Current methods are cumbersome and rely on many assumptions that are hard to evaluate. We describe a new method for estimating relative diet quality directly from faeces that avoids the problems inherent in other methods. We combine this method with near infrared reflectance spectroscopy (NIRS) to analyse many samples and thus provide a technique with immense value in ecological studies. The method stems from the correlation between the concentrations of dietary and faecal nitrogen in herbivores eating a tannin-free diet, but a weaker relationship in browsers that ingest substantial amounts of tannins, which form complexes with proteins. These complexes reduce the availability of nitrogen and may increase faecal nitrogen concentrations. Using the tannin-binding compound, polyethylene glycol, we showed that tannin-bound nitrogen is a significant and variable part of faecal nitrogen in wild common brushtail possums (Trichosurus vulpecula). We developed a technique to measure faecal available nitrogen and found that it predicted the reproductive success of female brushtail possums in northern Australia. Faecal available nitrogen combined with NIRS provides a powerful tool for estimating the relative nutritional value of the diets of browsing herbivores in many ecological systems. It is a better indicator of diet quality than other commonly used single-nutrient measures such as faecal nitrogen and foliage analysis paired with observed feeding behaviour.

Food for folivores: nutritional explanations linking diets to population density.

Ecologists want to explain why populations of animals are not evenly distributed across landscapes and often turn to nutritional explanations. In seeking to link population attributes with food quality, they often contrast nutritionally positive traits, such as the concentration of nitrogen, against negative ones, such as fibre concentration, by using a ratio of these traits. This specific ratio has attracted attention because it sometimes correlates with the biomass of colobine primates across sites in Asia and Africa. Although empirically successful, we have identified problems with the ratio that may explain why it fails under some conditions to predict colobine biomass. First, available nitrogen, rather than total nitrogen, is nutritionally important, while the presence of tannins is the major factor reducing the availability of nitrogen in browse plant species. Second, tannin complexes inflate measures of fibre. Finally, simple ratios may be unsound statistically because they implicitly assume isometric relationships between variables. We used data on the chemical composition of plants from three continents to examine the relationships between the concentrations of nitrogen, available nitrogen, fibre and tannins in foliage and to evaluate the nitrogen to fibre ratio. Our results suggest that the ratio of the concentration of nitrogen to fibre in leaves does sometimes closely correlate with the concentration of available nitrogen. However, the ratio may give misleading results when leaves contain high concentrations of tannins. The concentration of available nitrogen, which incorporates measures of total nitrogen, dry matter digestibility and tannins, should give a better indication of the nutritional value of leaves for herbivorous mammals that can readily be extrapolated to habitats.