Self-Medication as Adaptive Plasticity: Increased Ingestion of Plant Toxins by Parasitized Caterpillars

Abstract

Self-medication is a specific therapeutic behavioral change in response to disease or parasitism. The empirical literature on self-medication has so far focused entirely on identifying cases of self-medication in which particular behaviors are linked to therapeutic outcomes. In this study, we frame self-medication in the broader realm of adaptive plasticity, which provides several testable predictions for verifying self-medication and advancing its conceptual significance. First, self-medication behavior should improve the fitness of animals infected by parasites or pathogens. Second, self-medication behavior in the absence of infection should decrease fitness. Third, infection should induce self-medication behavior. The few rigorous studies of self-medication in non-human animals have not used this theoretical framework and thus have not tested fitness costs of self-medication in the absence of disease or parasitism. Here we use manipulative experiments to test these predictions with the foraging behavior of woolly bear caterpillars (Grammia incorrupta; Lepidoptera: Arctiidae) in response to their lethal endoparasites (tachinid flies). Our experiments show that the ingestion of plant toxins called pyrrolizidine alkaloids improves the survival of parasitized caterpillars by conferring resistance against tachinid flies. Consistent with theoretical prediction, excessive ingestion of these toxins reduces the survival of unparasitized caterpillars. Parasitized caterpillars are more likely than unparasitized caterpillars to specifically ingest large amounts of pyrrolizidine alkaloids. This case challenges the conventional view that self-medication behavior is restricted to animals with advanced cognitive abilities, such as primates, and empowers the science of self-medication by placing it in the domain of adaptive plasticity theory.

Phytochemicals in animal health: diet selection and trade-offs between costs and benefits

“…nutritional and medicinal) against the ingestion of PSC as they benefit from selecting sainfoin over other tannin-free forages regardless of their level of parasitic burden. Thus, the inherent beneficial characteristics of some medicinal plants may not satisfy the second criterion described by Singer et al (30) needed to identify self-selection of PSC by parasitised individuals: a decrease in fitness by healthy animals. In a recent experiment, we offered parasitised and non-parasitised lambs a choice between two types of sainfoin pellets characterised by their level of tannin concentration (low, 2 % v. moderate, 4 %) (88) .…”

Integrating nutrition and immunology: A new frontier

“…The results of Lee et al (2006) and Povey et al (2009) indicate that dietary protein is a key nutritional component affecting immunity (see also (Alaux et al, 2010;Fellous and Lazzaro, 2010;Peck et al, 1992), and that caterpillars are able to self-medicate for infection by selecting a dietary composition that best supports immune defense (see also Singer et al, 2009). …”

Synergistic effects of floral phytochemicals against a bumble bee parasite

“…In addition to defending plants against their own pathogens, antimicrobial phytochemicals can also counteract infection in animals, including pollinators (Karban & English‐Loeb, 1997; de Roode, Lefèvre, Hunter, Lefevre, & Hunter, 2013; Singer, Mace, & Bernays, 2009). Medicinal effects of phytochemicals are especially relevant for bees, given that bees have abundant access to phytochemicals in nectar and pollen and that some species are threatened by parasite‐related population decline (Cameron et al., 2011; Goulson, Nicholls, Botías, & Rotheray, 2015).…”