Herbivory and Time Since Flowering Shape Floral Rewards and Pollinator-Pathogen Interactions

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Herbivory and Time Since Flowering Shape Floral Rewards and Pollinator-Pathogen Interactions Luis A. Aguirre 1,2

&

Julie K. Davis 3

&

Philip C. Stevenson 4,5

&

Lynn S. Adler 1

Received: 5 May 2020 / Revised: 7 August 2020 / Accepted: 24 August 2020 # Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract Herbivory can induce chemical changes throughout plant tissues including flowers, which could affect pollinator-pathogen interactions. Pollen is highly defended compared to nectar, but no study has examined whether herbivory affects pollen chemistry. We assessed the effects of leaf herbivory on nectar and pollen alkaloids in Nicotiana tabacum, and how herbivory-induced changes in nectar and pollen affect pollinator-pathogen interactions. We damaged leaves of Nicotiana tabacum using the specialist herbivore Manduca sexta and compared nicotine and anabasine concentrations in nectar and pollen. We then pooled nectar and pollen by collection periods (within and after one month of flowering), fed them in separate experiments to bumble bees (Bombus impatiens) infected with the gut pathogen Crithidia bombi, and assessed infections after seven days. We did not detect alkaloids in nectar, and leaf damage did not alter the effect of nectar on Crithidia counts. In pollen, herbivory induced higher concentrations of anabasine but not nicotine, and alkaloid concentrations rose and then fell as a function of days since flowering. Bees fed pollen from damaged plants had Crithidia counts 15 times higher than bees fed pollen from undamaged plants, but only when pollen was collected after one month of flowering, indicating that both damage and time since flowering affected interaction outcomes. Within undamaged treatments, bees fed late-collected pollen had Crithidia counts 10 times lower than bees fed early-collected pollen, also indicating the importance of time since flowering. Our results emphasize the role of herbivores in shaping pollen chemistry, with consequences for interactions between pollinators and their pathogens. Keywords Bombus impatiens . Crithidia bombi . Floral chemistry . Multitrophic interactions . Pollinators

Introduction Plant defenses modify species interactions, and induced defenses in response to herbivory can mediate interactions over Electronic supplementary material The online version of this article (https://doi.org/10.1007/s10886-020-01213-2) contains supplementary material, which is available to authorized users. * Luis A. Aguirre [email protected] 1

Department of Biology, University of Massachusetts, Amherst, MA 01003, USA

2

Graduate Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, MA 01003, USA

3

Department of Entomology, Cornell University, Ithaca, NY 14850, USA

4

Jodrell Laboratory, Royal Botanic Gardens, Kew, Surrey TW9 3AB, UK

5

Natural Resources Institute, University of Greenwich, Chatham, Kent ME4 4TB, UK

three or even four trophic levels (Harvey et al. 2003; Soler et al. 2005). Induced plant defenses typically are stu