THE MANIPULATION OF PLANT TOXINS BY A FOOD-HOARDING HERBIVORE,OCHOTONA PRINCEPS

Abstract

Generalist mammalian herbivores typically avoid plant species containing high levels of plant secondary compounds because generalists are thought to lack the ability to process large quantities of these chemicals. Here I propose and test two hypotheses: (1) that food-hoarding herbivores behaviorally overcome consumption limits imposed by secondary compounds by storing food until the toxins degrade; and (2) that the presence of secondary compounds in cached plant material facilitates the preservation of these items, as well as other cached items that lack such compounds. To evaluate these hypotheses, I conducted a number of field and laboratory experiments using the North American pika, Ochotona princeps, a generalist herbivore that consumes low-phenolic vegetation in the summer while it simultaneously collects and stores high-phenolic vegetation for subsequent consumption during winter. In experiments investigating decomposition of summer and winter diets of pikas, after 10 mo of storage, the winter diet retained 20.5% more biomass, and was higher in energy, lower in fiber, and equal in nitrogen compared to the summer diet. Moreover, a common food item in the winter diet, Acomastylis rossii, which contains high levels of phenolics, was the only plant extract to deter bacterial growth in a bioassay. Acomastylis rossii leaves with experimentally reduced phenolic levels retained significantly less biomass than leaves with natural phenolic concentrations. However, the presence of A. rossii in artificial caches containing a low-phenolic species, Trifolium parryi, did not facilitate the preservation of T. parryi. Approximately halfway through the typical storage period, phenolic concentrations of pika winter diet samples in artificial caches decreased to levels readily consumed by pikas in their summer diet. Examination of natural haypiles of pikas before and after storage revealed that pikas do increase their intake of A. rossii from the haypile sometime during the winter. In experiments with captive pikas, pikas preferred A. rossii with experimentally reduced phenolic concentrations over those with natural concentrations. Observations of pikas foraging from natural and artificial haypiles suggested that pikas do not increase their intake of A. rossii from the haypile until phenolics levels decrease. Taken together, the results support both of the hypotheses. Pikas manipulate plant chemistry by storing plants rich in allelochemicals and by delaying consumption of these plants until the toxins decay. Moreover, plants with high levels of secondary compounds exhibit superior preservation qualities so that more biomass and nutrients are retained during storage. As food caching is a common strategy among several animal classes and many foods contain potentially deleterious compounds, the manipulation of food toxins by storage may be a prevalent phenomenon.