FITNESS IMPACTS OF HERBIVORY THROUGH INDIRECT EFFECTS ON PLANT–POLLINATOR INTERACTIONS IN OENOTHERA MACROCARPA

The negative impacts of herbivores on plant fitness may include both direct and indirect effects. Direct effects on female plant fitness occur when decreased seed production is due to decreased resource availability from loss of leaf area and its attendant photosynthesis or through consumption of reproductive structures. Indirect effects occur when folivore‐ and florivore‐mediated changes in floral traits influence pollinator preference and/or pollinator efficiency, thus reducing pollen receipt. We examined the effects of both leaf and floral herbivory (bud damage) and determined the relative contribution of direct and indirect effects of damage on female fitness through changes in floral traits for Oenothera macrocarpa (Onagraceae). The experiment was a two‐factorial design that manipulated both leaf damage (∼25% leaf area removed by hand) and pollen receipt (supplemental hand pollination). We then measured effects of leaf damage on floral traits (corolla diameter, floral tube length, and flower number) and fruit and seed set. Because herbivores damaged corollas in the bud stage in this experiment, we were also able to determine the effect of florivores on subsequent female reproduction. Plants in the increased leaf damage treatment (33.4% leaf area loss) produced fewer flowers than natural leaf damage plants (6.5% leaf area loss), and their flowers had smaller corolla diameters and shorter floral tube lengths. Experimentally damaged plants also had 18% lower fruit set and produced 33% fewer seeds compared with natural leaf damage plants. Hand pollination increased fruit set by 60% and total seed number by 38% above that of naturally pollinated plants, demonstrating that female fitness was pollen‐limited. Bud damage significantly decreased corolla diameter and floral tube length, and it led to a 68% reduction in fruit set. Hawk moths were observed preferentially visiting flowers with larger corollas, and study flowers with larger corollas had significantly increased probability of setting fruit. Additionally, seed number per fruit was positively related to floral tube length. In path analysis, we found no significant path between percentage leaf damage and female reproduction, suggesting that herbivores did not reduce seed production directly through decreased resource availability. Instead, we found a significant indirect path from percentage leaf damage to seed number through corolla diameter. We conclude that decreased female reproduction was due to changes in floral traits from both leaf and floral bud damage, which affected hawk moth preference (flowers with smaller corollas received fewer visits) and hawk moth efficiency of pollen delivery (flowers with shorter floral tubes had fewer seeds). This study demonstrates that herbivores can mitigate the mutualistic relationship between plants and pollinators through their effects on floral traits.