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Plant–herbivore and plant–pollinator interactions are both well-studied, but largely independent of each other. It has become increasingly recognized, however, that pollination and herbivory interact extensively in nature, with consequences for plant fitness. Here, we explore the idea that trade-offs in investment in insect flight and reproduction may be a mechanistic link between pollination and herbivory. We first provide a general background on trade-offs between flight and fecundity in insects. We then focus on Lepidoptera; larvae are generally herbivores while most adults are pollinators, making them ideal to study these links. Increased allocation of resources to flight, we argue, potentially increases a Lepidopteran insect pollinator’s efficiency, resulting in higher plant fitness. In contrast, allocation of resources to reproduction in the same insect species reduces plant fitness, because it leads to an increase in herbivore population size. We examine the sequence of resource pools available to herbivorous Lepidopteran larvae (maternally provided nutrients to the eggs, as well as leaf tissue), and to adults (nectar and nuptial gifts provided by the males to the females), which potentially are pollinators. Last, we discuss how subsequent acquisition and allocation of resources from these pools may alter flight–fecundity trade-offs, with concomitant effects both on pollinator performance and the performance of larval herbivores in the next generation. Allocation decisions at different times during ontogeny translate into costs of herbivory and/or benefits of pollination for plants, mechanistically linking herbivory and pollination. 

1. Precise pollen placement on floral visitors can improve pollen transfer, but in many plant species, pollen is deposited onto the flexible proboscises of long-tongued insects. These proboscises are curled and uncurled between floral visits, potentially causing pollen to be lost or displaced. Rates of pollen movement and loss resulting from proboscis curling, and hence the potential quality of long-tongued insects as pollinators, are unknown. 2. Here, pollen loss and movement on the proboscises of Manduca sexta (Sphingidae) hawkmoths was experimentally measured. It was predicted that (i) proboscis curling causes pollen loss; (ii) pollen that is not lost is displaced from its deposition site; and (iii) repeated curls result in more displacement. Pollen from Datura wrightii, an important nectar plant for M. sexta, was placed distal to the knee bend on M. sexta proboscises, and the number and location of grains was recorded after proboscis curls. 3. Consistent with the hypotheses, proboscis curling caused significant pollen loss. (i) A single curl resulted in the loss of almost 75% of the pollen from the placement site; after repeated curling, 98% of grains were lost from this site. (ii) A single curl was also sufficient to displace pollen across all surfaces of the proboscis, but (iii) further curling did not affect its distribution across surfaces. 4. Together, these results suggest that precise pollen placement on the proboscises of hawkmoths would be unlikely to increase pollen transfer success. Strategies by which flowering plants might mitigate the effects of pollen loss from visitors with flexible pollen-pickup structures are discussed.