Adding landscape genetics and individual traits to the ecosystem function paradigm reveals the importance of species functional breadth
Edited by Peter Kareiva, University of California, Los Angeles, CA, and approved October 16, 2017 (received for review November 22, 2016)
Significance
Pollinators mediate reproductive processes between plants; however, little is known about how plant and pollinator traits impact pollen dispersal and resulting genetic connectivity. Our study quantifies pollen-dispersal distances and pollination effectiveness for individual pollinator species. We demonstrate that seed set is positively driven by pollinator body size, but long-distance pollen dispersal is mediated by both large-bodied and small-bodied bees. We also reveal that individual plant and population attributes impact pollen-dispersal distances and seed production, respectively. Thus, we show that plant and pollinator traits mediate pollination function and that the entire pollinator community, large and small, plays an important role in the maintenance of genetic connectivity.
Abstract
Animal pollination mediates both reproduction and gene flow for the majority of plant species across the globe. However, past functional studies have focused largely on seed production; although useful, this focus on seed set does not provide information regarding species-specific contributions to pollen-mediated gene flow. Here we quantify pollen dispersal for individual pollinator species across more than 690 ha of tropical forest. Specifically, we examine visitation, seed production, and pollen-dispersal ability for the entire pollinator community of a common tropical tree using a series of individual-based pollinator-exclusion experiments followed by molecular-based fractional paternity analyses. We investigate the effects of pollinator body size, plant size (as a proxy of floral display), local plant density, and local plant kinship on seed production and pollen-dispersal distance. Our results show that while large-bodied pollinators set more seeds per visit, small-bodied bees visited flowers more frequently and were responsible for more than 49% of all long-distance (beyond 1 km) pollen-dispersal events. Thus, despite their size, small-bodied bees play a critical role in facilitating long-distance pollen-mediated gene flow. We also found that both plant size and local plant kinship negatively impact pollen dispersal and seed production. By incorporating genetic and trait-based data into the quantification of pollination services, we highlight the diversity in ecological function mediated by pollinators, the influential role that plant and population attributes play in driving service provision, and the unexpected importance of small-bodied pollinators in the recruitment of plant genetic diversity.
Data Availability
Data deposition: Data are available from the Dryad digital repository (https://doi.org/10.5061/dryad.1cm80).
Acknowledgments
We thank J. A. Ramirez, E. Sanchez, M. Ureña, A. G. Castillo, and numerous volunteers for their invaluable help in conducting the fieldwork; Jefferson Hall and Agua Salud team for help with planning, facilities, and logistics; and members of the S.J. laboratory, Justin W. Leung, and two anonymous reviewers for providing useful comments to improve the manuscript. This study was funded by the University of Texas at Austin and the National Science Foundation (NSF) (S.J.). M.O. and N.S.P. are funded by NSF Graduate Research Fellowships.
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Cover image: Pictured are the flowering tree Miconia affinis and a bee. Antonio R. Castilla et al. studied pollen dispersal of M. affinis across more than 690 ha of tropical forest in central Panama. By examining pollination events and the genotypes of reproductive trees, the authors found that large-bodied bee pollinators were associated with increased seed production, whereas small-bodied bee pollinators helped facilitate long-distance gene flow among the trees and accounted for nearly half of long-distance pollen-dispersal events. The study highlights the role of functionally diverse pollinator communities in conserving plant genetic diversity. See the article by Castilla et al. on pages 12761–12766. Image courtesy of Antonio R. Castilla.
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© 2017. Published under the PNAS license.
Data Availability
Data deposition: Data are available from the Dryad digital repository (https://doi.org/10.5061/dryad.1cm80).
Submission history
Published online: November 10, 2017
Published in issue: November 28, 2017
Keywords
Acknowledgments
We thank J. A. Ramirez, E. Sanchez, M. Ureña, A. G. Castillo, and numerous volunteers for their invaluable help in conducting the fieldwork; Jefferson Hall and Agua Salud team for help with planning, facilities, and logistics; and members of the S.J. laboratory, Justin W. Leung, and two anonymous reviewers for providing useful comments to improve the manuscript. This study was funded by the University of Texas at Austin and the National Science Foundation (NSF) (S.J.). M.O. and N.S.P. are funded by NSF Graduate Research Fellowships.
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This article is a PNAS Direct Submission.
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The authors declare no conflict of interest.
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