Kessler et al. 2010 Changing Pollinators as a Means of Escaping Herbivores (1)

Summary

Overview

  • Animal-pollinated plants face the challenge of attracting pollinators without attracting herbivores.

  • This dilemma is heightened when larval-stage herbivores also serve as important pollinators.

Nicotiana attenuata

  • Nicotiana attenuata is a night-flowering tobacco that typically opens flowers at night to attract nocturnal hawkmoth pollinators (e.g., Manduca quinquemaculata, Manduca sexta).

  • When infested by hawkmoth larvae, these plants change their floral characteristics.

Herbivore Impact on Flower Phenology

  • Upon larval attack, N. attenuata produces morning-opening flowers (MoFs) instead of night-opening flowers (NoFs).

  • MoFs exhibit reduced emissions of floral volatiles (like benzyl acetone) and attract diurnal pollinators, specifically hummingbirds.

  • This shift in flowering time is regulated by oral secretions from the feeding larvae and requires jasmonate (JA) signaling.

Experimental Observations

Field Studies

  • During a Manduca quinquemaculata outbreak, plants shifted from producing primarily NoFs to MoFs in response to herbivore attack.

  • Experiments showed that infested plants produced significantly more MoFs under herbivore pressure compared to uninfested plants.

Flower Characteristics

  • MoFs have:

    • Lower benzyl acetone emissions.

    • Reduced nectar concentrations.

    • Smaller corolla diameter compared to NoFs.

  • The shift from NoFs to MoFs affects the community of pollinators visiting the plants, facilitating greater pollination by hummingbirds.

Pollinator Dynamics

Hummingbird Visits

  • Hummingbirds preferentially visit MoFs over NoFs, likely due to nectar availability that is undisturbed by nocturnal pollinators.

  • Observational data highlighted that visits to MoFs increased overall pollination rates of infested plants.

Fitness Consequences

  • Infested plants benefited from enhanced outcrossing rates despite emitting lower floral volatiles overall.

  • Hummingbirds’ preferences contributed to a greater capsule production from MoFs compared to NoFs.

Mechanisms of Change

Signaling Pathways

  • Feeding by Manduca larvae activates a MAP kinase cascade, leading to increased jasmonic acid production and resulting in the herbivory-induced production of MoFs.

  • Genetic experiments confirmed that JA signaling is essential for this change in flower phenology.

Conclusion

  • The shift from MoFs to NoFs serves as a defensive strategy against herbivore attack while optimizing pollination services from specific pollinators such as hummingbirds.

  • This herbivory-elicited change in flower phenology accentuates the complex interactions between plants, herbivores, and pollinators, representing an adaptation for reducing herbivore loads while maximizing reproductive success.