The widespread evolution of tube-like anthers releasing pollen from apical pores is associated wi... more The widespread evolution of tube-like anthers releasing pollen from apical pores is associated with buzz pollination, in which bees vibrate flowers to remove pollen. The mechanical connection among anthers in buzz-pollinated species varies from loosely held conformations, to anthers tightly held together with trichomes or bio-adhesives forming a functionally joined conical structure (anther cone). Joined anther cones in buzz-pollinated species have evolved independently across plant families and via different genetic mechanisms, yet their functional significance remains mostly untested. We used experimental manipulations to compare vibrational and functional (pollen release) consequences of joined anther cones in three buzz-pollinated species of Solanum (Solanaceae). We applied bee-like vibrations to focal anthers in flowers with (“joined”) and without (“free”) experimentally created joined anther cones, and characterised vibrations transmitted to other anthers and the amount of pol...
In buzz-pollinated plants, bees apply thoracic vibrations to the flower, causing pollen release f... more In buzz-pollinated plants, bees apply thoracic vibrations to the flower, causing pollen release from anthers, often through apical pores. Bees grasp one or more anthers with their mandibles, and vibrations are transmitted to this focal anther(s), adjacent anthers, and the whole flower. Pollen release depends on anther vibration, and thus it should be affected by vibration transmission through flowers with distinct morphologies, as found among buzz-pollinated taxa. We compare vibration transmission between focal and non-focal anthers in four species with contrasting stamen architectures: Cyclamen persicum, Exacum affine, Solanum dulcamara and S. houstonii. We used a mechanical transducer to apply bee-like vibrations to focal anthers, measuring the vibration frequency and displacement amplitude at focal and non-focal anther tips simultaneously using high-speed video analysis (6000 frames per second). In flowers in which anthers are tightly arranged (C. persicum and S. dulcamara), vibr...
How pollinators mediate microbiome assembly in the anthosphere is a major unresolved question of ... more How pollinators mediate microbiome assembly in the anthosphere is a major unresolved question of theoretical and applied importance in the face of anthropogenic disturbance. We addressed this question by linking visitation of diverse pollinator functional groups (bees, wasps, flies, butterflies, beetles, true bugs and other taxa) to the key properties of floral microbiome (microbial α- and β-diversity and microbial network) under agrochemical disturbance, using a field experiment of bactericide and fungicide treatments on cultivated strawberries that differ in flower abundance. Structural equation modeling was used to link agrochemical disturbance and flower abundance to pollinator visitation to floral microbiome properties. Our results revealed that (1) pollinator visitation influenced the α- and β-diversity and network centrality of floral microbiome, with different pollinator functional groups affecting different microbiome properties; (2) flower abundance influenced floral micro...
One of the reasons why flowering plants became the most diverse group of land plants is their ass... more One of the reasons why flowering plants became the most diverse group of land plants is their association with animals to reproduce. The earliest examples of this mutualism involved insects foraging for food from plants and, in the process, pollinating them. Vertebrates are latecomers to these mutualisms, but birds, in particular, present a wide variety of nectar-feeding clades that have adapted to solve similar challenges. Such challenges include surviving on small caloric rewards widely scattered across the landscape, matching their foraging strategy to nectar replenishment rate, and efficiently collecting this liquid food from well-protected chambers deep inside flowers. One particular set of convergent traits among plants and their bird pollinators has been especially well studied: the match between the shape and size of bird bills and ornithophilous flowers. Focusing on a highly specialized group, hummingbirds, we examine the expected benefits from bill–flower matching, with a ...
Philosophical Transactions of the Royal Society B: Biological Sciences
Mimicry is common in interspecies interactions, yet conditions maintaining Batesian mimicry have ... more Mimicry is common in interspecies interactions, yet conditions maintaining Batesian mimicry have been primarily tested in predator–prey interactions. In pollination mutualisms, floral mimetic signals thought to dupe animals into pollinating unrewarding flowers are widespread (greater than 32 plant families). Yet whether animals learn to both correctly identify floral models and reject floral mimics and whether these responses are frequency-dependent is not well understood. We tested how learning affected the effectiveness and frequency-dependence of imperfect Batesian mimicry among flowers using the generalist bumblebee, Bombus impatiens , visiting Begonia odorata , a plant species exhibiting intersexual floral mimicry. Unrewarding female flowers are mimics of pollen-rewarding male flowers (models), though mimicry to the human eye is imperfect. Flower-naive bees exhibited a perceptual bias for mimics over models, but rapidly learned to avoid mimics. Surprisingly, altering the freque...
learning multimodal cue pollen poricidal anther signal interaction Signals used in communication ... more learning multimodal cue pollen poricidal anther signal interaction 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 naïve 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 bee's 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.
Bees foraging for floral rewards are one of our most thoroughly studied examples of generalist fo... more Bees foraging for floral rewards are one of our most thoroughly studied examples of generalist foraging ecology. Generalist bees rely considerably on instrumental (associative) learning to acquire routines that allow them to collect nectar efficiently from diverse plant species. Although such bees must also collect pollen from diverse species, few studies have examined if and how high efficiency is achieved. We characterized how generalist bumble bees (Bombus impatiens) foraged effectively for pollen from diverse floral resources, by manipulating the presence of pollen and anther cues, in a series of experiments using pollen-bearing live flowers, flowers of a sterile pollen-less horticultural hybrid, and artificial flowers. We show that generalist bumble bees exhibit flexible and effective pollen collection by switching between 2 routines: " scrabbling " when pollen is abundant and " sonicating " when pollen is scarce. Efficient switching between these behaviors is regulated by the interplay of 2 ubiquitous floral cues: chemical anther cues stimulating pollen collection behavior and mechanical pollen cues suppressing sonication (and eliciting scrabbling). Flexible pollen collection behavior is functional: When pollen on anthers was scarce, bees collected it at a greater rate by sonicating than scrabbling. This mechanism of behavioral flexibility likely allows generalist bees to handle diverse anther morphologies efficiently and may have facilitated the recurrent evolution of plant species that conceal pollen rewards via pored floral morphology. Whereas effective nectar foraging relies heavily on associative learning of unique routines for each flower type, a weighing of 2 types of cues regulates the flexible pollen collection mechanism we describe.
Heteranthery is thought to reflect a division of labor, with some anthers serving a pollinator-fe... more 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.
The ecological success of social insects is frequently ascribed to improvements in task performan... more 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. Task specialization is a hallmark of insect societies 1,2. Eusocial bees, some of our most important pollinators, must engage in a variety of tasks over their lifetime, including nest construction, brood care, and foraging from flowers to feed themselves and their nest mates. Specialization on different foraging tasks in particular has been well studied (e.g., refs 3 and 4). Because switching between tasks can incur temporal, cognitive, and/or energetic costs, specialization is thought to maximize task efficiency 3–6. For instance, bees often have to learn new nectar collection routines each time they shift to a new plant species 3,7. Cognitive costs associated with learning and recalling such collection routines are thought to make it advantageous for foraging bees to specialize in the short term on a given plant species 3–8. In addition, individuals can vary in their task performance as a result of fixed physiological or morphological differences; for example, honeybees vary in their sucrose sensitivity 4,9. In fact, intrinsic differences among foragers are thought to explain lifetime patterns of specialization on the collection of nectar, water, and pollen in foraging honeybees 9,10. These and other studies suggest that patterns of foraging task specialization by individual worker bees might differ when we examine the short term (e.g., hours or days) versus the long-term (e.g., lifetime). Yet almost no research has examined specialization by the same foragers over different timescales. Patterns of foraging specialization over different timescales have important implications for how individuals and, for social bee species, colonies manage the collection of multiple floral rewards. The two most common floral rewards collected by bees are pollen and nectar 11,12. Flowering plants offer pollen and nectar in all combinations and qualities. For instance, the flowers of some plant species offer pollen and nectar, only pollen, only nectar, or even vary the availability of one or the other reward over the floral lifecycle or as a result of prior collection. Thus a forager might not always be able to collect pollen and nectar on a single floral visit (e.g., refs 13 and 14). Further, collecting both rewards during a single foraging bout may not be efficient if, for instance, the bee has to travel far to collect both rewards. In addition, colony needs vary over lifetime. Bees rely on nectar as their primary
Pollinators frequently use complex motor routines to find and extract floral rewards. Studies of ... more Pollinators frequently use complex motor routines to find and extract floral rewards. Studies of polli-nators 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 soni-cation motor routine appeared in full-blown form in a flower-naïve bee's 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.
1. The ability to forage and return home is essential to the success of bees as both foragers and... more 1. 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. 2. We investigated the impact of chronic exposure (5–43 days) to field-realistic levels of a neonicotinoid insecticide (2Á4 ppb thiamethoxam) on foraging ability, homing success and colony size using radio frequency identification (RFID) technology in free-flying bumblebee colonies. 3. 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. 4. 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. 5. Despite a trend for control colonies to produce more new workers earlier, we found no overall impacts of pesticide exposure on whole colony size. 6. 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 worldwide .
Pollinator-driven selection is thought to drive much of the extraordinary diversity of flowering ... more Pollinator-driven selection is thought to drive much of the extraordinary diversity of flowering plants. Plants that produce floral traits preferred by particular pol-linators 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-naı¨ve 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,
The study of foraging behaviour in plant-pollinator mutualisms has benefitted from the use of art... more The study of foraging behaviour in plant-pollinator mutualisms has benefitted from the use of artificial flowers to manipulate floral display traits and the delivery of floral rewards. The two most common floral rewards are pollen and nectar; some pollinators, such as bees, are obliged to collect both for survival and reproduction. While flexible designs for artificial flowers providing nectar rewards abound, useful designs for artificial flowers that dispense pollen are few. This disparity mirrors a heavy emphasis on nectar collection in the study of pollinator foraging behaviour. In this study we describe a novel, easily constructed and modifiable artificial flower that dispenses flexible amounts of pollen via an 'anther' composed of a chenille stem. Using controlled lab assays, we show that more pulverized honeybee pollen is collected by bumblebee (Bombus impatiens) workers at chenille stem feeders than at dish-type feeders. We suggest that the paucity of studies examining pollinator cognition in the context of pollen rewards might be partly remedied if researchers had access to inexpensive and easily adjustable pollen-offering surrogate flowers.
The widespread evolution of tube-like anthers releasing pollen from apical pores is associated wi... more The widespread evolution of tube-like anthers releasing pollen from apical pores is associated with buzz pollination, in which bees vibrate flowers to remove pollen. The mechanical connection among anthers in buzz-pollinated species varies from loosely held conformations, to anthers tightly held together with trichomes or bio-adhesives forming a functionally joined conical structure (anther cone). Joined anther cones in buzz-pollinated species have evolved independently across plant families and via different genetic mechanisms, yet their functional significance remains mostly untested. We used experimental manipulations to compare vibrational and functional (pollen release) consequences of joined anther cones in three buzz-pollinated species of Solanum (Solanaceae). We applied bee-like vibrations to focal anthers in flowers with (“joined”) and without (“free”) experimentally created joined anther cones, and characterised vibrations transmitted to other anthers and the amount of pol...
In buzz-pollinated plants, bees apply thoracic vibrations to the flower, causing pollen release f... more In buzz-pollinated plants, bees apply thoracic vibrations to the flower, causing pollen release from anthers, often through apical pores. Bees grasp one or more anthers with their mandibles, and vibrations are transmitted to this focal anther(s), adjacent anthers, and the whole flower. Pollen release depends on anther vibration, and thus it should be affected by vibration transmission through flowers with distinct morphologies, as found among buzz-pollinated taxa. We compare vibration transmission between focal and non-focal anthers in four species with contrasting stamen architectures: Cyclamen persicum, Exacum affine, Solanum dulcamara and S. houstonii. We used a mechanical transducer to apply bee-like vibrations to focal anthers, measuring the vibration frequency and displacement amplitude at focal and non-focal anther tips simultaneously using high-speed video analysis (6000 frames per second). In flowers in which anthers are tightly arranged (C. persicum and S. dulcamara), vibr...
How pollinators mediate microbiome assembly in the anthosphere is a major unresolved question of ... more How pollinators mediate microbiome assembly in the anthosphere is a major unresolved question of theoretical and applied importance in the face of anthropogenic disturbance. We addressed this question by linking visitation of diverse pollinator functional groups (bees, wasps, flies, butterflies, beetles, true bugs and other taxa) to the key properties of floral microbiome (microbial α- and β-diversity and microbial network) under agrochemical disturbance, using a field experiment of bactericide and fungicide treatments on cultivated strawberries that differ in flower abundance. Structural equation modeling was used to link agrochemical disturbance and flower abundance to pollinator visitation to floral microbiome properties. Our results revealed that (1) pollinator visitation influenced the α- and β-diversity and network centrality of floral microbiome, with different pollinator functional groups affecting different microbiome properties; (2) flower abundance influenced floral micro...
One of the reasons why flowering plants became the most diverse group of land plants is their ass... more One of the reasons why flowering plants became the most diverse group of land plants is their association with animals to reproduce. The earliest examples of this mutualism involved insects foraging for food from plants and, in the process, pollinating them. Vertebrates are latecomers to these mutualisms, but birds, in particular, present a wide variety of nectar-feeding clades that have adapted to solve similar challenges. Such challenges include surviving on small caloric rewards widely scattered across the landscape, matching their foraging strategy to nectar replenishment rate, and efficiently collecting this liquid food from well-protected chambers deep inside flowers. One particular set of convergent traits among plants and their bird pollinators has been especially well studied: the match between the shape and size of bird bills and ornithophilous flowers. Focusing on a highly specialized group, hummingbirds, we examine the expected benefits from bill–flower matching, with a ...
Philosophical Transactions of the Royal Society B: Biological Sciences
Mimicry is common in interspecies interactions, yet conditions maintaining Batesian mimicry have ... more Mimicry is common in interspecies interactions, yet conditions maintaining Batesian mimicry have been primarily tested in predator–prey interactions. In pollination mutualisms, floral mimetic signals thought to dupe animals into pollinating unrewarding flowers are widespread (greater than 32 plant families). Yet whether animals learn to both correctly identify floral models and reject floral mimics and whether these responses are frequency-dependent is not well understood. We tested how learning affected the effectiveness and frequency-dependence of imperfect Batesian mimicry among flowers using the generalist bumblebee, Bombus impatiens , visiting Begonia odorata , a plant species exhibiting intersexual floral mimicry. Unrewarding female flowers are mimics of pollen-rewarding male flowers (models), though mimicry to the human eye is imperfect. Flower-naive bees exhibited a perceptual bias for mimics over models, but rapidly learned to avoid mimics. Surprisingly, altering the freque...
learning multimodal cue pollen poricidal anther signal interaction Signals used in communication ... more learning multimodal cue pollen poricidal anther signal interaction 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 naïve 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 bee's 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.
Bees foraging for floral rewards are one of our most thoroughly studied examples of generalist fo... more Bees foraging for floral rewards are one of our most thoroughly studied examples of generalist foraging ecology. Generalist bees rely considerably on instrumental (associative) learning to acquire routines that allow them to collect nectar efficiently from diverse plant species. Although such bees must also collect pollen from diverse species, few studies have examined if and how high efficiency is achieved. We characterized how generalist bumble bees (Bombus impatiens) foraged effectively for pollen from diverse floral resources, by manipulating the presence of pollen and anther cues, in a series of experiments using pollen-bearing live flowers, flowers of a sterile pollen-less horticultural hybrid, and artificial flowers. We show that generalist bumble bees exhibit flexible and effective pollen collection by switching between 2 routines: " scrabbling " when pollen is abundant and " sonicating " when pollen is scarce. Efficient switching between these behaviors is regulated by the interplay of 2 ubiquitous floral cues: chemical anther cues stimulating pollen collection behavior and mechanical pollen cues suppressing sonication (and eliciting scrabbling). Flexible pollen collection behavior is functional: When pollen on anthers was scarce, bees collected it at a greater rate by sonicating than scrabbling. This mechanism of behavioral flexibility likely allows generalist bees to handle diverse anther morphologies efficiently and may have facilitated the recurrent evolution of plant species that conceal pollen rewards via pored floral morphology. Whereas effective nectar foraging relies heavily on associative learning of unique routines for each flower type, a weighing of 2 types of cues regulates the flexible pollen collection mechanism we describe.
Heteranthery is thought to reflect a division of labor, with some anthers serving a pollinator-fe... more 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.
The ecological success of social insects is frequently ascribed to improvements in task performan... more 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. Task specialization is a hallmark of insect societies 1,2. Eusocial bees, some of our most important pollinators, must engage in a variety of tasks over their lifetime, including nest construction, brood care, and foraging from flowers to feed themselves and their nest mates. Specialization on different foraging tasks in particular has been well studied (e.g., refs 3 and 4). Because switching between tasks can incur temporal, cognitive, and/or energetic costs, specialization is thought to maximize task efficiency 3–6. For instance, bees often have to learn new nectar collection routines each time they shift to a new plant species 3,7. Cognitive costs associated with learning and recalling such collection routines are thought to make it advantageous for foraging bees to specialize in the short term on a given plant species 3–8. In addition, individuals can vary in their task performance as a result of fixed physiological or morphological differences; for example, honeybees vary in their sucrose sensitivity 4,9. In fact, intrinsic differences among foragers are thought to explain lifetime patterns of specialization on the collection of nectar, water, and pollen in foraging honeybees 9,10. These and other studies suggest that patterns of foraging task specialization by individual worker bees might differ when we examine the short term (e.g., hours or days) versus the long-term (e.g., lifetime). Yet almost no research has examined specialization by the same foragers over different timescales. Patterns of foraging specialization over different timescales have important implications for how individuals and, for social bee species, colonies manage the collection of multiple floral rewards. The two most common floral rewards collected by bees are pollen and nectar 11,12. Flowering plants offer pollen and nectar in all combinations and qualities. For instance, the flowers of some plant species offer pollen and nectar, only pollen, only nectar, or even vary the availability of one or the other reward over the floral lifecycle or as a result of prior collection. Thus a forager might not always be able to collect pollen and nectar on a single floral visit (e.g., refs 13 and 14). Further, collecting both rewards during a single foraging bout may not be efficient if, for instance, the bee has to travel far to collect both rewards. In addition, colony needs vary over lifetime. Bees rely on nectar as their primary
Pollinators frequently use complex motor routines to find and extract floral rewards. Studies of ... more Pollinators frequently use complex motor routines to find and extract floral rewards. Studies of polli-nators 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 soni-cation motor routine appeared in full-blown form in a flower-naïve bee's 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.
1. The ability to forage and return home is essential to the success of bees as both foragers and... more 1. 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. 2. We investigated the impact of chronic exposure (5–43 days) to field-realistic levels of a neonicotinoid insecticide (2Á4 ppb thiamethoxam) on foraging ability, homing success and colony size using radio frequency identification (RFID) technology in free-flying bumblebee colonies. 3. 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. 4. 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. 5. Despite a trend for control colonies to produce more new workers earlier, we found no overall impacts of pesticide exposure on whole colony size. 6. 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 worldwide .
Pollinator-driven selection is thought to drive much of the extraordinary diversity of flowering ... more Pollinator-driven selection is thought to drive much of the extraordinary diversity of flowering plants. Plants that produce floral traits preferred by particular pol-linators 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-naı¨ve 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,
The study of foraging behaviour in plant-pollinator mutualisms has benefitted from the use of art... more The study of foraging behaviour in plant-pollinator mutualisms has benefitted from the use of artificial flowers to manipulate floral display traits and the delivery of floral rewards. The two most common floral rewards are pollen and nectar; some pollinators, such as bees, are obliged to collect both for survival and reproduction. While flexible designs for artificial flowers providing nectar rewards abound, useful designs for artificial flowers that dispense pollen are few. This disparity mirrors a heavy emphasis on nectar collection in the study of pollinator foraging behaviour. In this study we describe a novel, easily constructed and modifiable artificial flower that dispenses flexible amounts of pollen via an 'anther' composed of a chenille stem. Using controlled lab assays, we show that more pulverized honeybee pollen is collected by bumblebee (Bombus impatiens) workers at chenille stem feeders than at dish-type feeders. We suggest that the paucity of studies examining pollinator cognition in the context of pollen rewards might be partly remedied if researchers had access to inexpensive and easily adjustable pollen-offering surrogate flowers.
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Papers by Avery Russell