Pollinator Grooming Behavior Alters Pollen Landscapes on Bees’ Bodies and Increases Pollen Carryover to Other Flowers

Premise: Reproductive fitness in plants is often determined by the quantity and quality of pollen transferred by pollinators. However, many fitness studies measure only female fitness or rely on proxies for male fitness. Here we assessed how five bee taxon groups affect male fitness in a prairie plant by quantifying pollen removal, visitation, and siring success using paternity assignments and a unique pollinator visitation experiment. Methods: In Echinacea angustifolia, we measured per-visit pollen removal for each pollinator taxon and estimated the number of pollen grains needed for successful ovule fertilization. Additionally, we directly measured pollinator influence on siring by allowing only one bee taxon to visit each pollen-donor plant, while open-pollinated plants acted as unrestricted pollen recipients. We genotyped the resulting offspring, assigned paternity, and used aster statistical models to quantify siring success. Results: Siring success of pollen-donor plants differed among the five pollinator groups. Nongrooming male bees were associated with increased siring success. Bees from all taxa removed most of the flowering head's pollen in one visit. However, coneflower-specialist bee Andrena helianthiformis removed the most pollen per visit. Female fitness and proxy measures of male fitness, such as pollinator visitation and pollen removal, did not align with our direct quantifications of male fitness. Conclusions: Our results illustrate the need for more studies to directly quantify male fitness, and we caution against using male fitness proxy measures. In addition, conservation efforts that preserve a diverse pollinator community can benefit plants in fragmented landscapes.

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Pollinators differ in their contribution to the male fitness of a self‐incompatible composite

Pearson,

Zelman,

Hill

et al. 2023

“…Pollinator foraging and grooming behavior once on or after visiting a flower likely also impacts pollen-associated virus transmission because these behaviors determine pollen transfer from anther to stigma. For instance, Russell et al (2019Russell et al ( , 2021 found that bumble bees collecting pollen via "scrabbling" transferred more pollen grains and epiphytic bacterial cells to stigmas than bees only collecting nectar, and Marcelo et al (2023) predict that grooming allows bees to acquire more pollen grains and deposit a more diverse assemblage of pollen grains while foraging. Thus, withinflower foraging and grooming behaviors could mediate the transmission of epiphytic viruses and pollen-associated ones.…”

Section: Pollinator Traitsmentioning

confidence: 99%

The pollen virome: A review of pollen‐associated viruses and consequences for plants and their interactions with pollinators

Fetters

Ashman

2023

The movement of pollen grains from anthers to stigmas, often by insect pollinator vectors, is essential for plant reproduction. However, pollen is also a unique vehicle for viral spread. Pollen-associated plant viruses reside on the outside or inside of pollen grains, infect susceptible individuals through vertical or horizontal infection pathways, and can decrease plant fitness. These viruses are transferred with pollen between plants by pollinator vectors as they forage for floral resources; thus, pollenassociated viral spread is mediated by floral and pollen grain phenotypes and pollinator traits, much like pollination. Most of what is currently known about pollenassociated viruses was discovered through infection and transmission experiments in controlled settings, usually involving one virus and one plant species of agricultural or horticultural interest. In this review, we first provide an updated, comprehensive list of the recognized pollen-associated viruses. Then, we summarize virus, plant, pollinator vector, and landscape traits that can affect pollen-associated virus transmission, infection, and distribution. Next, we highlight the consequences of plant-pollinator-virus interactions that emerge in complex communities of coflowering plants and pollinator vectors, such as pollen-associated virus spread between plant species and viral jumps from plant to pollinator hosts. We conclude by emphasizing the need for collaborative research that bridges pollen biology, virology, and pollination biology.

“…The structures of these landscapes can theoretically affect the distance and timing of a flower's pollen dispersal (Harder and Wilson, 1998), with potentially far‐reaching effects on floral evolution and ecology. For example, layering may increase gene flow if pollen is not removed immediately from pollinators by stigmas, but is instead buried underneath subsequently deposited pollen, only to resurface much later (Lertzman and Gass, 1983; Morris et al, 1995; Marcelo et al 2022 [preprint]). Pollen landscapes may also generate variability in the ability of pollen grains to adhere to or leave the bodies of pollinators.…”

Section: Figurementioning

confidence: 99%

Pollen layering and male–male competition: Quantum dots demonstrate that pollen grains compete for space on pollinators

Moir

Anderson

2023

Premise: Almost nothing is known about what happens to pollen grains once they attach to pollinators, although some have postulated that pollen from different donors may form complex, two-or three-dimensional landscapes (e.g., layers or mosaics) that can facilitate male-male competition. For example, pollen that is already on pollinators may preclude the deposition of subsequent pollen grains. Methods: Using quantum dots to mark the pollen of individual flowers, we explored the possibilities of layering and preclusion in a fly-pollinated iris, Moraea lurida. Results and Conclusions:The proportion of labeled pollen from the last flower visited diminished in sequential pollen samples taken from the top to the bottom of the pollen load, representing the first empirical evidence for pollen layering. However, the consequences in terms of pollen preclusion were equivocal: Although the preexisting pollen load size was not a good predictor of new pollen receipt, labeled pollen loads from the last flower visited were significantly smaller than pollen loads from the previous flower visited. Thus, pollen from the previous flower may preclude pollen placement from a subsequently visited flower, and pollen from different flowers may compete for space on pollinators.