How high are the costs inflicted by an herbivorous pollinator?

Many adult Lepidoptera nectar at flowers of plant species on which they also deposit their eggs. As a consequence, the same partner may act as both a pollinator and herbivore. How high are the costs associated with such herbivorous pollinators, relative to the potential benefits they confer? We addressed this question in the association between Datura wrightii (Solanaceae) and Manduca sexta (Sphingidae), which in southern Arizona, USA is both the plant’s most important pollinator (as adults) and most significant herbivore (as larvae). We manually inflicted two biologically relevant levels of artificial folivory (33% and 66% leaf removal) at two points during the growing season, to nearly 200 D. wrightii plants established in a common-garden outdoor plot. We recorded plant survival, growth, and several components of reproduction (bud, flower, and fruit production). We found no detectable effect of damage on plant growth rate, fruit set in the same or the following growing season, or plant volume or survival in the same or the following three seasons. These results suggest that D. wrightii may be highly tolerant of leaf consumption by the herbivorous offspring of its specialized, nectar-feeding pollinators. We argue that this mechanism would likely foster persistence of the pollination mutualism more effectively than would resistance to, or deterrence of, herbivores. Tolerance to the costs of mutualism is an underexplored phenomenon that could contribute to the stability of these interactions.