Mutualism has its limits: consequences of asymmetric interactions between a well-defended plant and its herbivorous pollinator

Concern for pollinator health has focused on social bees and their
agricultural services, but not all pollinators are bees, and their
ecosystem services also promote biodiversity and conservation. Pollinating
herbivores generate ecological conflicts when they utilize the same plant
as a nectar source and larval host. We tracked individual-level metrics of
pollinator health – growth, survivorship, fecundity – across the life
cycle of a pollinating herbivore, the hawkmoth Hyles lineata, through its
interactions with Oenothera harringtonii, a rare plant polymorphic for the
floral volatile (R)-(-)-linalool. Linalool had no impact on moth
attraction to O. harringtonii flowers but suppressed oviposition on
experimentally supplemented plants. Leaves of O. harringtonii showed
robust resistance against herbivory by H. lineata from leaf-disc to
wholeplant scales, through poor larval growth and survivorship. Higher
larval performance on other Oenothera species indicates that constitutive
herbivore resistance by O. harringtonii is not generic. Leaf volatiles
differed among populations of O. harringtonii but were not induced by
larval herbivory. Elagitannins and other phenolics varied among leaf, bud
and seed tissues but showed no evidence of herbivore induction. Our
findings highlight asymmetric plant-pollinator interactions and the
importance of third parties, such as alternative host plants, in
maintaining pollinator health.