Bumblebees negotiate a trade-off between nectar quality and floral biomechanics.

How and why pollinators choose which flowers to visit are fundamental, multifaceted questions in pollination biology, yet most studies of floral traits measure simple relative preferences. Here, we used vertically and horizontally oriented slippery-surfaced artificial flowers to test whether bumblebees could make a trade-off between floral handling difficulty and nectar sucrose concentration. We quantified foraging energetics, thereby resolving the rationale behind the bees' foraging decisions. The bees chose flowers with either a high handling cost or low sucrose concentration, depending on which was the energetically favorable option. Their behavior agreed with the critical currency being the rate of energy return (net energy collected per unit time), not energetic efficiency (net energy collected per unit energy spent). This suggests that bumblebees prioritize immediate carbohydrate flow to the nest rather than energy gain over the working lifespan of each bee. Trade-off paradigms like these are a powerful approach for quantifying pollinator trait preferences.

Humans Share More Preferences for Floral Phenotypes With Pollinators Than With Pests.

Studies on the selection of floral traits usually consider pollinators and sometimes herbivores. However, humans also exert selection on floral traits of ornamental plants. We compared the preferences of bumblebees (Bombus terrestris), thrips (Frankliniella occidentalis), and humans for flowers of snapdragon. From a cross of two species, Antirrhinum majus and Antirrhinum linkianum, we selected four Recombinant Inbred Lines (RILs). We characterised scent emission from whole flowers and stamens, pollen content and viability, trichome density, floral shape, size and colour of floral parts. We tested the preferences of bumblebees, thrips, and humans for whole flowers, floral scent bouquets, stamen scent, and individual scent compounds. Humans and bumblebees showed preferences for parental species, whereas thrips preferred RILs. Colour and floral scent, in combination with other floral traits, seem relevant phenotypes for all organisms. Remarkably, visual traits override scent cues for bumblebees, although, scent is an important trait when bumblebees cannot see the flowers, and methyl benzoate was identified as a key attractant for them. The evolutionary trajectory of flowers is the result of multiple floral traits interacting with different organisms with different habits and modes of interaction.

The mechanics of nectar offloading in the bumblebee Bombus terrestris and implications for optimal concentrations during nectar foraging.

Nectar is a common reward provided by plants for pollinators. More concentrated nectar is more rewarding, but also more viscous, and hence more time-consuming to drink. Consequently, theory predicts an optimum concentration for maximizing energy uptake rate, dependent on the mechanics of feeding. For social pollinators such as bumblebees, another important but little-studied aspect of foraging is nectar offloading upon return to the nest. Studying the bumblebee Bombus terrestris, we found that the relationship between viscosity (µ) and volumetric transfer rates (Q) of sucrose solutions differed between drinking and offloading. For drinking, Q ∝ µ-0.180, in good agreement with previous work. Although offloading was quicker than drinking, offloading rate decreased faster with viscosity, with Q ∝ µ-0.502, consistent with constraints imposed by fluid flow through a tube. The difference in mechanics between drinking and offloading nectar leads to a conflict in the optimum concentration for maximizing energy transfer rates. Building a model of foraging energetics, we show that including offloading lowers the maximum rate of energy return to the nest and reduces the concentration which maximizes this rate by around 3%. Using our model, we show that published values of preferred nectar sugar concentrations suggest that bumblebees maximize the overall energy return rather than the instantaneous energy uptake during drinking.

Froghoppers jump from smooth plant surfaces by piercing them with sharp spines.

Attachment mechanisms used by climbing animals facilitate their interactions with complex 3D environments and have inspired novel types of synthetic adhesives. Here we investigate one of the most dynamic forms of attachment, used by jumping insects living on plants. Froghopper insects can perform explosive jumps with some of the highest accelerations known among animals. As many plant surfaces are smooth, we studied whether Philaenus spumarius froghoppers are able to take off from such substrates. When attempting to jump from smooth glass, the insects' hind legs slipped, resulting in weak, uncontrolled jumps with a rapid forward spin. By contrast, on smooth ivy leaves and smooth epoxy surfaces, Philaenus froghoppers performed strong jumps without any slipping. We discovered that the insects produced traction during the acceleration phase by piercing these substrates with sharp spines of their tibia and tarsus. High-speed microscopy recordings of hind legs during the acceleration phase of jumps revealed that the spine tips indented and plastically deformed the substrate. On ivy leaves, the spines of jumping froghoppers perforated the cuticle and epidermal cell walls, and wounds could be visualized after the jumps by methylene blue staining and scanning electron microscopy. Improving attachment performance by indenting or piercing plant surfaces with sharp spines may represent a widespread but previously unrecognized strategy utilized by plant-living insects. This attachment mechanism may also provide inspiration for the design of robotic grippers.

Scaling of claw sharpness: mechanical constraints reduce attachment performance in larger insects.

Claws are the most widespread attachment devices in animals, but comparatively little is known about the mechanics of claw attachment. A key morphological parameter in determining attachment ability is claw sharpness; however, there is a conflict between sharpness and fracture resistance. Sharper claws can interlock on more surfaces but are more likely to break. Body size interacts with this conflict such that larger animals should have much blunter claws and consequently poorer attachment ability than smaller animals. This expected size-induced reduction in attachment performance has not previously been investigated, and it is unclear how animals deal with this effect, and whether it indeed exists. We explored the scaling of claw sharpness with body size using four insect species (Nauphoeta cinerea, Gromphadorhina portentosa, Atta cephalotes and Carausius morosus) each covering a large size range. The scaling of claw sharpness varied significantly between species, suggesting that they face different pressures regarding claw function. Attachment forces were measured for A. cephalotes and G. portentosa (which had different scaling of claw sharpness) on several rough surfaces using a centrifuge setup. As expected, attachment performance was poorer in larger animals. Firstly, larger animals were more likely to slip, although this effect depended on the scaling of claw sharpness. Secondly, when they gripped, they attached with smaller forces relative to their weight. This size-induced reduction in attachment performance has significant implications for the attachment ability of larger animals on rough surfaces.

An analysis of the energetic reward offered by field bean (Vicia faba) flowers: Nectar, pollen, and operative force.

Global consumption of crops with a yield that is dependent on animal pollinators is growing, with greater areas planted each year. However, the floral traits that influence pollinator visitation are not usually the focus of breeding programmes, and therefore, it is likely that yield improvements may be made by optimizing floral traits to enhance pollinator visitation rates. We investigated the variation present in the floral reward of the bee-pollinated crop Vicia faba (field bean). We examined the genetic potential for breeding flowers with a greater reward into current commercial varieties and used bee behavioral experiments to gain insight into the optimal nectar concentration to maximize bee preference. There was a large range of variation in the amount of pollen and nectar reward of flowers in the genotypes investigated. Bee behavioral experiments using nectar sugar concentrations found in V. faba lines suggest that Bombus terrestris prefers 55% w/w sugar solution over 40% w/w, but has no preference between 55% w/w and 68% w/w sugar solution. We provide a first indication of the force required to open V. faba flowers. Our results provide a valuable starting point toward breeding for varieties with optimized floral reward. Field studies are now needed to verify whether the genetic potential for breeding more rewarding flowers can translate into higher yield and yield stability.

How can an understanding of plant-pollinator interactions contribute to global food security?

Pollination of crops by animals is an essential part of global food production, but evidence suggests that wild pollinator populations may be declining while a number of problems are besetting managed honey bee colonies. Animal-pollinated crops grown today, bred in an environment where pollination was less likely to limit fruit set, are often suboptimal in attracting and sustaining their pollinator populations. Research into plant-pollinator interactions is often conducted in a curiosity-driven, ecological framework, but may inform breeding and biotechnological approaches to enhance pollinator attraction and crop yield. In this article we review key topics in current plant-pollinator research that have potential roles in future crop breeding for enhanced global food security.

Bumblebee visual search for multiple learned target types.

Visual search is well studied in human psychology, but we know comparatively little about similar capacities in non-human animals. It is sometimes assumed that animal visual search is restricted to a single target at a time. In bees, for example, this limitation has been evoked to explain flower constancy, the tendency of bees to specialise on a single flower type. Few studies, however, have investigated bee visual search for multiple target types after extended learning and controlling for prior visual experience. We trained colour-naive bumblebees (Bombus terrestris) extensively in separate discrimination tasks to recognise two rewarding colours in interspersed block training sessions. We then tested them with the two colours simultaneously in the presence of distracting colours to examine whether and how quickly they were able to switch between the target colours. We found that bees switched between visual targets quickly and often. The median time taken to switch between targets was shorter than known estimates of how long traces last in bees' working memory, suggesting that their capacity to recall more than one learned target was not restricted by working memory limitations. Following our results, we propose a model of memory and learning that integrates our findings with those of previous studies investigating flower constancy.