Avery L. Russell

Investigating the impacts of field‐realistic exposure to a neonicotinoid pesticide on bumblebee foraging, homing ability and colony growth

Summary The ability to forage and return home is essential to the success of bees as both foragers and pollinators. Pesticide exposure may cause behavioural changes that interfere with these processes, with consequences for colony persistence and delivery of pollination services. We investigated the impact of chronic exposure (5–43 days) to field‐realistic levels of a neonicotinoid insecticide (2·4 ppb thiamethoxam) on foraging ability, homing success and colony size using radio frequency identification (RFID) technology in free‐flying bumblebee colonies. Individual foragers from pesticide‐exposed colonies carried out longer foraging bouts than untreated controls (68 vs. 55 min). Pesticide‐exposed bees also brought back pollen less frequently than controls indicating reduced foraging performance. A higher proportion of bees from pesticide‐exposed colonies returned when released 1 km from their nests; this is potentially related to increased orientation experience during longer foraging bouts. We measured no impact of pesticide exposure on homing ability for bees released from 2 km, or when data were analysed overall. Despite a trend for control colonies to produce more new workers earlier, we found no overall impacts of pesticide exposure on whole colony size. Synthesis and applications. This study shows that field‐realistic neonicotinoid exposure can have impacts on both foraging ability and homing success of bumblebees, with implications for the success of bumblebee colonies in agricultural landscapes and their ability to deliver crucial pollination services. Pesticide risk assessments should include bee species other than honeybees and assess a range of behaviours to elucidate the impact of sublethal effects. This has relevance for reviews of neonicotinoid risk assessment and usage policy world‐wide.

Concealed floral rewards and the role of experience in floral sonication by bees

Pollinators frequently use complex motor routines to find and extract floral rewards. Studies of pollinators foraging for nectar rewards indicate these routines are typically learned, and that constraints associated with learning and memory give pollinators incentive to continue foraging on these flowers. However, plants offer rewards besides nectar, including pollen, lipids and essential oils. In particular, bees use a complex motor routine termed floral sonication to extract pollen, their primary source of protein, from the more than 6% of flowering plant species (>22 000 species) that conceal pollen rewards within tube-like poricidal anthers. If floral sonication requires learning, this pollen extraction behaviour could contribute to floral fidelity. However, no studies have quantified the effect of experience on flower handling for bees extracting pollen from poricidal species. We therefore examined the degree to which floral sonication behaviour was modified by experience. We found that the key elements of the sonication motor routine appeared in full-blown form in a flower-naive bees first visit to a flower. We additionally found consistent, albeit modest, effects of experience on certain aspects of sonication behaviour. The latency to sonicate slightly decreased with experience. Bees also adjusted the length and amplitude of their sonication buzzes in response to pollen receipt. We conclude that the role of experience in foraging for concealed pollen rewards is different from that reported for nectar rewards. We offer an alternative explanation for its function in sonication. Finally, we discuss alternative hypotheses for the function of poricidal anthers and for how pollen-bearing plants may ensure floral fidelity even in the absence of a significant impact of experience on pollen extraction behaviour.

Patterns of pollen and nectar foraging specialization by bumblebees over multiple timescales using RFID

The ecological success of social insects is frequently ascribed to improvements in task performance due to division of labour amongst workers. While much research has focused on improvements associated with lifetime task specialization, members of colonies can specialize on a given task over shorter time periods. Eusocial bees in particular must collect pollen and nectar rewards to survive, but most workers appear to mix collection of both rewards over their lifetimes. We asked whether bumblebees specialize over timescales shorter than their lifetime. We also explored factors that govern such patterns, and asked whether reward specialists made more foraging bouts than generalists. In particular, we described antennal morphology and size of all foragers in a single colony and related these factors to each forager’s complete foraging history, obtained using radio frequency identification (RFID). Only a small proportion of foragers were lifetime specialists; nevertheless, >50% of foragers specialized daily on a given reward. Contrary to expectations, daily and lifetime reward specialists were not better foragers (being neither larger nor making more bouts); larger bees with more antennal olfactory sensilla made more bouts, but were not more specialized. We discuss causes and functions of short and long-term patterns of specialization for bumblebee colonies.

How a generalist bee achieves high efficiency of pollen collection on diverse floral resources

Lay SummaryLearning enables generalists to forage efficiently from diverse floral resources. Bees must collect nectar and pollen, but effective, flexible foraging behavior has been demonstrated only for nectar foragers. We demonstrate that flexible and effective pollen collection by bees is regulated by 2 ubiquitous floral cues. This mechanism of foraging flexibility likely facilitated the evolution of pollen concealment via poricidal floral morphology. We conclude that effective flexibility in pollen collection can occur without necessitating learning.

Division of labor of anthers in heterantherous plants: flexibility of bee pollen collection behavior may serve to keep plants honest

Heteranthery is thought to reflect a division of labor, with some anthers serving a pollinator-feeding function and others serving a pollinating function. Mutualism theory predicts that each participant should try to maximize the benefit it receives from its partner: plants should allocate more pollen to pollination, and pollinators should collect more pollen. Accordingly, plant and pollinator may engage in a ‘tug of war’ with respect to pollen from each anther type, resulting in incomplete division of labor. Here, we explored this idea by conducting a fully factorial manipulation of the availability of pollen in long and short anthers of staminate flowers of Solanum houstonii. We found the following: (1) Bumble bees (Bombus impatiens) preferred to sonicate (collect pollen from) short anthers over long anthers, consistent with a role as feeding and pollinating anthers, respectively; (2) Blocking short anther pores alone increased sonication of long anthers and resulted in collection of pollen from long anthers; (3) Blocking long anther pores alone did not influence sonication of short anthers; (4) The increase in sonication of long anthers, when short anther pores are blocked, was greater when pollen was available in long anthers; (5) Despite shifting sonication effort to long anthers, bees do not move their bodies closer to long anther pores where pollen could be collected more effectively; and (6) analysis of the growth of corbicular loads over time spent buzzing indicates that significant amounts of pollen are collected from long anthers as well as short anthers. We conclude that bees can flexibly increase pollen collection from pollinating anthers, but are constrained from fully exploiting this pollen. This results in checks and balances between plant and bee that may help maintain heteranthery.

White flowers finish last: pollen-foraging bumble bees show biased learning in a floral color polymorphism

Pollinator-driven selection is thought to drive much of the extraordinary diversity of flowering plants. Plants that produce floral traits preferred by particular pollinators are more likely to receive conspecific pollen and to evolve further adaptations to those pollinators that enhance pollination and ultimately generate floral diversity. Two mechanisms in particular, sensory bias and learning, are thought to explain how pollinator preference can contribute to divergence and speciation in flowering plants. While the preferences of pollinators, such as bees, flies, and birds, are frequently implicated in patterns of floral trait evolution, the role of learning in generating reproductive isolation and trait divergence for different floral types within plant populations is not well understood. Floral color polymorphism in particular provides an excellent opportunity to examine how pollinator behavior and learning might maintain the different floral morphs. In this study we asked if bumble bees showed innate preferences for different color morphs of the pollen-only plant Solanum tridynamum, whether bees formed preferences for the morphs with which they had experience collecting pollen from, and the strength of those learned preferences. Using an absolute conditioning protocol, we gave bees experience collecting pollen from a color polymorphic plant species that offered only pollen rewards. Despite initially-naïve bees showing no apparent innate bias toward human-white versus human-purple flower morphs, we did find evidence of a bias in learning. Specifically, bees learned strong preferences for purple corollas, but learned only weak preferences for hypochromic (human-white) corollas. We discuss how our results might explain patterns of floral display evolution, particularly as they relate to color polymorphisms. Additionally, we propose that the ease with which floral visual traits are learned—i.e., biases in learning—can influence the evolution of floral color as a signal to pollinators.

Linking components of complex signals to morphological part: the role of anther and corolla in the complex floral display

Signals used in communication are frequently complex, being composed of multiple signal components that in combination improve information transfer. A variety of morphological parts are typically used to transmit components of any given complex signal. Our understanding of why a given morphological part is used to transmit a given signal component is poor. We hypothesized that the function of a given signal component is improved by its association with its morphological part and that such parts interact functionally to transmit information. In a laboratory study we characterized the function of different floral signal components transmitted by associated floral parts and the interaction of those signal components. Using Solanum houstonii flowers, we focused on two major floral parts, corolla and anthers, involved in signalling bumblebee, Bombus impatiens , visitors. We further examined how experience affected the relationship between signal component and floral part. Floral visits involve a stepwise process in which bees approach, land and acquire pollen. We found that the corolla plays the dominant role in eliciting approaches by bees, whether naive or experienced. Landing is elicited by corolla signals and, to a lesser but additive degree, anther signals. Following experience, anther signals nearly completely dominate corolla signals in eliciting landing. The anthers convey signals mediating pollen acquisition, regardless of the bees experience level. Our findings suggest there is selection for specific relationships between signal components and morphological parts, which in turn might drive complex signal evolution.

Brawls Bring Buzz: Male Size Influences Competition and Courtship in Diadasia rinconis (Hymenoptera: Apidae)

Abstract Sexual selection on male body size in species with a female-biased sexual size dimorphism is common yet often poorly understood. In particular, in the majority of bee species, the relative contribution of intrasexual competition and female choice to patterns of male body size is unknown. In this field study, we examined two possible components of male mating success with respect to body size in the solitary bee Diadasia rinconis Cockerell (Hymenoptera: Apidae): 1) ability to procure a mate and 2) the duration of copulation. We found that larger males were better able to procure mates and copulated for shorter periods of time. Although consistent with sperm competition theory, differences in copulation duration were slight; possibly, the shorter copulations of larger males instead reflect in copulo female choice. Consistent with this notion, males engaged in complex courtship while mounted, characterized for the first time in any bee in such detail via audio recordings and high-speed, high-definition video. The number of pulses in male courtship behavior was also positively associated with copulation duration and may have stimulated females to continue copulating, thereby potentially allowing smaller males to transfer a full ejaculate. Females were shown to be potentially polyandrous and although we did not observe precopulatory rejection in the field, captive females frequently rejected copulation attempts by captive males. Our work indicates that intrasexual competition selects for increased body size in a solitary bee.