The threat of parasitism impairs immune function in host caterpillars

Nonconsumptive effects (NCE) from natural enemy presence are known to change the behavior, morphology, and development of potential victims. However, the overwhelming majority of these studies focus on predation, documenting changes in prey behavior; far less is understood about parasitism risk and impacts on host physiology. We used the caterpillar Manduca sexta (Lepidoptera: Sphingidae) and two of its main natural enemies—a specialist parasitoid (wasp), Cotesia congregata (Hymenoptera: Braconidae), and a generalist predator (soldier bug), Podisus maculiventris (Hemiptera: Pentatomidae)—to determine how the threat of parasitism and predation during larval development alter prey growth and immunity. Caterpillars developing near female predators and parasitoids were ~ 85% larger compared to individuals without enemy exposure. Development time was not affected by natural enemies when compared to controls, but male P. maculiventris slowed M. sexta development compared to the other natural enemies. For immune functionality, phenoloxidase (PO) activity only responded to parasitoids, with wasp‐exposed caterpillars exhibiting 35% lower PO activity than all other treatments, while lysozyme activity was unaffected by any enemy treatment. This work emphasizes that parasites can induce changes to host immunity that potentially affect wasp development. More broadly, NCEs on victim immunity are likely given immunity's contribution to host defense but have been under‐appreciated compared to more easily observed phenotypes like behavior and morphology. In this study, we report how the threat of parasitism and predation during development alter prey growth and immunity using the caterpillar Manduca sexta and two of its main natural enemies—a specialist parasitoid (wasp), Cotesia congregata, and a generalist predator (soldier bug), Podisus maculiventris. We found that caterpillars developing near female predators and parasitoids were ~ 85% larger compared to individuals without enemy exposure. However, immune function (phenoloxidase; PO) only responded to parasitoids, with wasp‐exposed caterpillars exhibiting 35% lower PO activity than all other treatments. This study emphasizes that parasites can induce changes to host immunity that potentially affect wasp development.