Changes in feeding behavior can enable individual animals to cure themselves of parasite infections or other physiological distress. All animals have immunological defenses that can potentially change in strength based on an individual's diet. In addition, herbivores such as caterpillars may kill their parasites by ingesting and accumulating toxic chemicals found in the plants they eat. This research project will investigate these two means of anti-parasite behavior by the woolly bear caterpillar Grammia geneura. This species is suspected from previous study to ward off natural parasites through its feeding choices. First, behavioral experiments will characterize the dietary choices of experimentally parasitized caterpillars in relation to unparasitized caterpillars. Second, to evaluate the role of specific diets in resistance against parasites, the survival of parasitized and unparasitized caterpillars on different diets will be tested. Third, physiological experiments will evaluate the effects of these diets on the caterpillar's immune response to parasites. Finally, to analyze direct effects of caterpillar diet without the immune system, the parasites will be raised on artificial diets that reflect different caterpillar diets. Caterpillars newly infected by the potentially lethal, parasitic fly Exorista mella, are expected to choose a nutritious diet to enhance their immunological resistance. This mechanism is expected to carry minimal physiological costs for the caterpillar. However, caterpillars threatened by late-stage parasitic infections are expected to choose a diet rich in natural plant toxins called pyrrolizidine alkaloids. Ingesting unusually large quantities of alkaloids is expected to be physiologically costly for the caterpillar, and thus used as a last resort.
The broader impacts of this research include training diverse students and a post-doctoral fellow in linking behavior, physiology, and ecology to animal health. Through public presentations, this project will also educate the public about the scientific link between animal health, behavior, and the environment.
Intellectual merit This project investigated how a woolly bear caterpillar can use chemicals in the plants it eats to overcome its parasites. It focused on the caterpillar’s ingestion of plant toxins that kill the parasites as well as nutrients that might enhance the immune system. The woolly bear caterpillar, Grammia incorrupta, feeds on a variety of plant species that differ in nutrition and toxicity. These chemical differences can affect this caterpillar’s defenses against its enemies. Like most caterpillars, it falls victim to flies and wasps called parasitoids. The larval parasitoids feed and develop in the caterpillar host, eventually killing the host if the host cannot stop them. But caterpillars and other insects can sometimes overcome parasitoid infections with an immune response called encapsulation. If encapsulation is successful, host cells completely surround the parasite, become dark (melanization), and kill it. The process of melanization produces toxic free radical molecules that damage and kill the encapsulated parasite. Factors that determine the likelihood of successful encapsulation are poorly understood but previous work on other insects suggests that dietary nutrients, such as protein, can enhance the encapsulation response, including melanization. This project studied the magnitude of melanization in the encapsulation response of G. incorrupta caterpillars reared on synthetic diets that differ in nutrition. Although the results show that immune-challenged caterpillars increased the proportion of protein in their diet relative to control caterpillars, a protein-biased diet did not increase the magnitude of melanization in the encapsulation response. However, not all aspects of the immunological response were tested, so it remains possible that dietary protein does enhance the immune system in some other measure. This project also tested the hypothesis that the caterpillar’s ingestion of plant toxins called pyrrolizidine alkaloids (PA) could serve as a secondary line of defense against parasitoids. Plants containing PA were previously observed to provide G. incorrupta with resistance against parasitoids. The caterpillars were expected to specifically increase their PA ingestion when parasitized because dietary PA can be harmful to caterpillar development. This project’s experiments show that PA ingestion by G. incorrupta caterpillars enhanced the survival of caterpillars infected with parasitoid flies, and that PA ingestion reduced the survival of unparasitized caterpillars. As predicted, parasitized caterpillars did increase their PA ingestion above amounts eaten by unparasitized caterpillars, a rare example of self-medication by an invertebrate animal. Additional experiments show that caterpillars increased PA ingestion around 48 hours after the start of parasitoid infection, reinforcing the hypothesis that this defense is a secondary line of defense (probably initiated if the immune system fails to kill the parasitoid). These results illustrate the importance of foraging choices for anti-parasite defense in addition to the better known functions of growth and proper development. For a caterpillar like G. incorrupta, making adaptive foraging choices requires enough plant diversity in its habitat to meet its nutritive and defensive needs. Other herbivores, wild and domestic, might have similar requirements to maintain healthy populations. Moreover, this clear case of self-medication by a caterpillar suggests that other invertebrate as well as vertebrate animals might have evolved to forage for medicine as well as food. This nascent field, sometimes called Darwinian medicine, offers great promise for advancing understanding of the links between behavior, health, and the environment. Broader impacts The project made several important contributions to education. A post-doc, a graduate student and several undergraduates received training in the conceptualization, methodology, and analysis of self-medication behavior. By nature, this training was multi-disciplinary, involving behavior, ecology, evolution, physiology, and biochemistry. This educational experience and impact was enhanced by linking the research training with other undergraduate programs already in place at Wesleyan University. This work was also incorporated into public science lectures given by the research team to diverse audiences such as K-12 classes, avocational organizations, and undergraduate student groups. The project’s results were broadly disseminated to the scientific community through presentations at conferences as well as publications. Furthermore, some of the key findings were broadcast to the public through several international media outlets, including print journalism, internet journalism and blogs, and radio journalism.
