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1.  Colour learning when foraging for nectar and pollen: bees learn two colours at once 
Biology Letters  2015;11(9):20150628.
Bees are model organisms for the study of learning and memory, yet nearly all such research to date has used a single reward, nectar. Many bees collect both nectar (carbohydrates) and pollen (protein) on a single foraging bout, sometimes from different plant species. We tested whether individual bumblebees could learn colour associations with nectar and pollen rewards simultaneously in a foraging scenario where one floral type offered only nectar and the other only pollen. We found that bees readily learned multiple reward–colour associations, and when presented with novel floral targets generalized to colours similar to those trained for each reward type. These results expand the ecological significance of work on bee learning and raise new questions regarding the cognitive ecology of pollination.
PMCID: PMC4614436  PMID: 26423070
Bombus; pollen; foraging; learning
3.  Long Frontal Projections Help Battus philenor (Lepidoptera: Papilionidae) Larvae Find Host Plants 
PLoS ONE  2015;10(7):e0131596.
Animals sometimes develop conspicuous projections on or near their heads as, e.g., weaponry, burrowing or digging tools, and probes to search for resources. The frontal projections that insects generally use to locate and assess resources are segmented appendages, including antennae, maxillary palps, and labial palps. There is no evidence to date that arthropods, including insects, use projections other than true segmental appendages to locate food. In this regard, it is noteworthy that some butterfly larvae possess a pair of long antenna-like projections on or near their heads. To date, the function of these projections has not been established. Larvae of pipevine swallowtail butterflies Battus philenor (Papilionidae) have a pair of long frontal fleshy projections that, like insect antennae generally, can be actively moved. In this study, we evaluated the possible function of this pair of long moveable frontal projections. In laboratory assays, both frontal projections and lateral ocelli were shown to increase the frequency with which search larvae found plants. The frontal projections increased finding of host and non-host plants equally, suggesting that frontal projections do not detect host-specific chemical cues. Detailed SEM study showed that putative mechanosensillae are distributed all around the frontal as well as other projections. Taken together, our findings suggest that the frontal projections and associated mechanosensillae act as vertical object detectors to obtain tactile information that, together with visual information from lateral ocelli and presumably chemical information from antennae and mouthparts, help larvae to find host plants. Field observations indicate that host plants are small and scattered in southern Arizona locations. Larvae must therefore find multiple host plants to complete development and face significant challenges in doing so. The frontal projections may thus be an adaptation for finding a scarce resource before starving to death. This is the first evidence that arthropods use projections other than true segmental appendages such as antennae, mouthparts and legs, to locate food resources.
PMCID: PMC4519131  PMID: 26222554
4.  Plasticity of the worker bumble bee brain in relation to age and rearing environment 
Brain, behavior and evolution  2013;82(4):250-261.
The environment experienced during development can dramatically affect the brain, with possible implications for sensory processing, learning and memory. Although the effects of single sensory modalities on brain development have been repeatedly explored, the additive or interactive effects of multiple modalities have been less thoroughly investigated. We asked how experience with multisensory stimuli affected brain development in the bumble bee, Bombus impatiens. First, to establish the timeline of brain development during early adulthood, we estimated regional brain volumes across a range of ages. We discovered significant age-related volume changes in nearly every region of the brain. Next, to determine whether these changes were dependent upon certain environmental stimuli, we manipulated the visual and olfactory stimuli available to newly emerged bumble bee workers in a factorial manner. Newly emerged bumble bees were maintained in the presence or absence of supplemental visual and/or olfactory stimuli for seven days, after which the volumes of several brain regions were estimated. We found that the volumes of the mushroom body lobes and calyces were larger in the absence of visual stimuli. Additionally, visual deprivation was associated with the expression of larger antennal lobes, the primary olfactory processing regions of the brain. In contrast, exposure to plant-derived olfactory stimuli did not have a significant effect on brain region volumes. This study is the first to explore the separate and interactive effects of visual and olfactory stimuli on bee brain development. Assessing the timing and sensitivity of brain development is a first step toward understanding how different rearing environments differentially affect regional brain volumes in this species. Our findings suggest that environmental factors experienced during the first week of adulthood can modify bumble brain development in many subtle ways.
PMCID: PMC3905614  PMID: 24281415
neuronal plasticity; Bombus; sensory environment; mushroom bodies; multimodal interactions
5.  Floral Nectar Guide Patterns Discourage Nectar Robbing by Bumble Bees 
PLoS ONE  2013;8(2):e55914.
Floral displays are under selection to both attract pollinators and deter antagonists. Here we show that a common floral trait, a nectar guide pattern, alters the behavior of bees that can act opportunistically as both pollinators and as antagonists. Generally, bees access nectar via the floral limb, transporting pollen through contact with the plant’s reproductive structures; however bees sometimes extract nectar from a hole in the side of the flower that they or other floral visitors create. This behavior is called “nectar robbing” because bees may acquire the nectar without transporting pollen. We asked whether the presence of a symmetric floral nectar guide pattern on artificial flowers affected bumble bees’ (Bombus impatiens) propensity to rob or access nectar “legitimately.” We discovered that nectar guides made legitimate visits more efficient for bees than robbing, and increased the relative frequency of legitimate visits, compared to flowers lacking nectar guides. This study is the first to show that beyond speeding nectar discovery, a nectar guide pattern can influence bees’ flower handling in a way that could benefit the plant.
PMCID: PMC3572167  PMID: 23418475
6.  Resource quality or competition: why increase resource acceptance in the presence of conspecifics? 
Behavioral Ecology  2011;22(4):730-737.
Some animal species increase resource acceptance rates in the presence of conspecifics. Such responses may be adaptive if the presence of conspecifics is a reliable indicator of resource quality. Similarly, these responses could represent an adaptive reduction in choosiness under high levels of scramble competition. Although high resource quality and high levels of scramble competition should both favor increased resource acceptance, the contexts in which the increase occurs should differ. In this paper, we tested the effect of social environment on egg-laying and aggressive behavior in the walnut fly, Rhagoletis juglandis, in multiple contexts to determine whether increased resource acceptance in the presence of conspecifics was better viewed as a response to increased host quality or increased competition. We found that grouped females oviposit more readily than isolated females when provided small (low-quality) artificial hosts but not when provided large (high-quality) artificial hosts, indicating that conspecific presence reduces choosiness. Increased resource acceptance was observed even when exposure to conspecifics was temporally or spatially separate from exposure to the resource. Finally, we found that individuals showed reduced aggression after being housed in groups, as expected under high levels of scramble competition. These results indicate that the pattern of resource acceptance in the presence of conspecifics may be better viewed as a response to increased scramble competition rather than as a response to public information about resource quality.
PMCID: PMC3117901  PMID: 22479135
conspecific attraction; experience; host choice; Rhagoletis; social facilitation; social information
7.  Multimodal signals enhance decision making in foraging bumble-bees 
Multimodal signals are common in nature and have recently attracted considerable attention. Despite this interest, their function is not well understood. We test the hypothesis that multimodal signals improve decision making in receivers by influencing the speed and the accuracy of their decisions. We trained bumble-bees (Bombus impatiens) to discriminate between artificial flowers that differed either in one modality, visual (specifically, shape) or olfactory, or in two modalities, visual plus olfactory. Bees trained on multimodal flowers learned the rewarding flowers faster than those trained on flowers that differed only in the visual modality and, in extinction trials, visited the previously rewarded flowers at a higher rate than bees trained on unimodal flowers. Overall, bees showed a speed–accuracy trade-off; bees that made slower decisions achieved higher accuracy levels. Foraging on multimodal flowers did not affect the slope of the speed–accuracy relationship, but resulted in a higher intercept, indicating that multimodal signals were associated with consistently higher accuracy across range of decision speeds. Our results suggest that bees make more effective decisions when flowers signal in more than one modality, and confirm the importance of studying signal components together rather than separately.
PMCID: PMC2596894  PMID: 18198150
Bombus; bumble-bees; decision making; multimodal signals; plant–pollinator interactions; speed–accuracy trade-off
8.  Big Genomes Facilitate the Comparative Identification of Regulatory Elements 
PLoS ONE  2009;4(3):e4688.
The identification of regulatory sequences in animal genomes remains a significant challenge. Comparative genomic methods that use patterns of evolutionary conservation to identify non-coding sequences with regulatory function have yielded many new vertebrate enhancers. However, these methods have not contributed significantly to the identification of regulatory sequences in sequenced invertebrate taxa. We demonstrate here that this differential success, which is often attributed to fundamental differences in the nature of vertebrate and invertebrate regulatory sequences, is instead primarily a product of the relatively small size of sequenced invertebrate genomes. We sequenced and compared loci involved in early embryonic patterning from four species of true fruit flies (family Tephritidae) that have genomes four to six times larger than those of Drosophila melanogaster. Unlike in Drosophila, where virtually all non-coding DNA is highly conserved, blocks of conserved non-coding sequence in tephritids are flanked by large stretches of poorly conserved sequence, similar to what is observed in vertebrate genomes. We tested the activities of nine conserved non-coding sequences flanking the even-skipped gene of the teprhitid Ceratis capitata in transgenic D. melanogaster embryos, six of which drove patterns that recapitulate those of known D. melanogaster enhancers. In contrast, none of the three non-conserved tephritid non-coding sequences that we tested drove expression in D. melanogaster embryos. Based on the landscape of non-coding conservation in tephritids, and our initial success in using conservation in tephritids to identify D. melanogaster regulatory sequences, we suggest that comparison of tephritid genomes may provide a systematic means to annotate the non-coding portion of the D. melanogaster genome. We also propose that large genomes be given more consideration in the selection of species for comparative genomics projects, to provide increased power to detect functional non-coding DNAs and to provide a less biased view of the evolution and function of animal genomes.
PMCID: PMC2650094  PMID: 19259274
9.  Flower choice copying in bumblebees 
Biology Letters  2005;1(4):504-507.
We tested a hypothesis originating with Darwin that bees outside the nest exhibit social learning in flower choices. Naive bumblebees, Bombus impatiens, were allowed to observe trained bees or artificial bees forage from orange or green flowers. Subsequently, observers of bees on green flowers landed more often on green flowers than non-observing controls or observers of models on orange flowers. These results demonstrate that bumblebees can change flower choice by observations of non-nest mates, a novel form of social learning in insects that could provide unique benefits to the colony.
PMCID: PMC1626359  PMID: 17148244
bumblebees; social learning; stimulus enhancement; social information
10.  A within-species warning function for an aposematic signal 
Aposematic, or warning, signals are generally interspecific in form: one species advertises noxiousness to a predator or parasite species. In a study of the pipevine swallowtail butterfly (Battus philenor), we show that a pattern of colouration in the caterpillars that is considered to be aposematic in the context of attack by natural enemies also deters oviposition by conspecific females. In field and laboratory assays, females avoided oviposition on plants bearing live conspecific larvae. Females avoided oviposition on plants bearing artificially constructed models identical to larvae in shape, size and colour pattern. Finally, oviposition on plants harbouring a model bearing the larval colour pattern was reduced relative to plants bearing a leaf-green model, suggesting that the larval colour pattern was essential for avoidance. We discuss how intraspecific and interspecific processes might interact in the evolution of an aposematic signal.
PMCID: PMC1599780  PMID: 16271978
aposematism; warning colouration; oviposition; crypsis; predator avoidance; host-marking behaviour

Results 1-10 (10)