Learning stimulus-response associations helps animals to adjust to changing environments. Sequentially learned associations may interact with each other, either reinforcing memory, a process referred to as 'transfer', or hindering memory, a process referred to as 'interference'. According to Osgood's (1949, Psychological Review, 56(3), 132-143) model, close similarity between new and previously learned stimuli can enhance the transfer of memory through a process of stimulus generalization. In contrast, the model proposes that if responses are different from those previously learned, generalizing stimuli may lead to confusion, resulting in the interference of memory. This model has primarily been applied in the context of human verbal learning. However, the interaction between stimulus similarity and response similarity is poorly documented in nonhuman animals, despite a growing body of literature suggesting that both vertebrate and invertebrate species share complex cognitive abilities similar to those found in humans. Here, we tested Osgood's model using bumble bees (Bombus impatiens) foraging for sucrose on artificial flowers with varied colours (= stimuli) that required either legitimate visits or nectar robbing (= responses). Bees were first allowed to forage on one type of flower, then switched to another type of flower and finally returned to the initial flower type. We measured learning performance via flowerhandling time and the number of failed visits. Consistent with Osgood's model, bees made more failed visits when they switched between similarly coloured flowers requiring different foraging techniques but made fewer failed visits when switching between similarly coloured flowers with the same technique. Regardless of similarities in stimuli or responses, however, experienced bees were faster in handling flowers than were na & iuml;ve bees. Results taken together thus provide mixed support for Osgood's model. Possible explanations for the mixed results are discussed. (c) 2024 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights are reserved, including those for text and data mining, AI training, and similar technologies.

Nectar-foraging bees change their use of floral resources as plant species appear in the environment and disappear over their lifetimes. The new flowers used may involve different cues and different nectar extraction tactics. Although bumble bees can adapt to changes in floral cues and required tactics, little is known about whether bees prioritize switching tactics or floral cues when deciding which plant species to switch to. In a laboratory assay, we forced common eastern bumble bee, Bombus impatiens, workers either to switch the handling tactic they were using or to continue using the tactic but to switch the colour of artificial flowers foraged on. We examined whether bees' tendency to change their tactics was influenced by how similar in colour novel flowers were to familiar ones. We conducted a 2 x 2 factorial experiment using artificial flowers, manipulating the handling tactic that bees were initially trained to use (legitimate visit or nectar robbing) and the similarity between novel and trained colours (similar or distinct). We found that under most conditions bees preferred to switch flower colours and retain handling tactics. However, when given experience with legitimate visits and when novel flowers were markedly different in colour from those they had experienced previously, bees tended to switch tactics while continuing to forage on flowers of the same colour. These findings suggest that the similarity in colour of a new floral resource to the currently exploited resource and the flower-handling tactic used by bees both play an important role in decision making by foraging bumble bees. (c) 2024 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights are reserved, including those for text and data mining, AI training, and similar technologies.

AbstractIntraspecific variation in camouflage is common in animals. Sexual dimorphism in camouflage is less common and, where observed, attributed to trade-offs between natural selection for predator avoidance and sexual selection for conspicuous mating signals. Here we report on variation in putatively cryptic ventral hindwing patterns in the American snout butterfly, Libytheana carinenta. We use field surveys and crowdsourced data to characterize three morphs. One is found in both sexes, one is male specific, and one is female specific. The sex-specific morphs constitute a sexually dimorphic set whose frequencies change together in time. Field surveys indicate that butterflies in southern Arizona transition from midsummer dominance of the sexually monomorphic pattern to early-fall dominance of the sexually dimorphic set. Crowdsourced data indicate that the sexually dimorphic set dominates in early spring, transitioning later into a mixture of morphs dominated by the monomorphic pattern, with the dimorphic set rising in frequency again in late fall. We discuss this unique pattern of camouflage variation with respect to contemporary theory on animal coloration.

The evolution of flowers that offer oils as rewards and are pollinated by specialized bees represents a distinctive theme in plant-pollinator co-diversification. Some plants that offer acetylated glycerols as floral oils emit diacetin, a volatile by-product of oil metabolism, which is utilized by oil-collecting bees as an index signal for the presence of floral oil. However, floral oils in the genus Krameria (Krameriaceae) contain β-acetoxy-substituted fatty acids instead of acetylated glycerols, making them unlikely to emit diacetin as an oil-bee attractant. We analyzed floral headspace composition from K. bicolor and K. erecta, native to the Sonoran Desert of southwestern North America, in search of alternative candidates for volatile index signals. Using solid-phase microextraction, combined with gas chromatography-mass spectrometry, we identified 26 and 45 floral volatiles, respectively, from whole flowers and dissected flower parts of these two Krameria species. As expected, diacetin was not detected. Instead, β-ionone emerged as a strong candidate for an index signal, as it was uniquely present in dissected oil-producing floral tissues (elaiophores) of K. bicolor, as well as the larval cells and provisions from its oil-bee pollinator, Centris cockerelli. This finding suggests that the floral oil of K. bicolor is perfused with β-ionone in its tissue of origin and retains the distinctive raspberry-like scent of this volatile after being harvested by C. cockerelli bees. In contrast, the elaiophores of K. erecta, which are not thought to be pollinated by C. cockerelli, produced a blend of anise-related oxygenated aromatics not found in the elaiophores of K. bicolor. Our findings suggest that β-ionone has the potential to impact oil-foraging by C. cockerelli bees through several potential mechanisms, including larval imprinting on scented provisions or innate or learned preferences by foraging adults.

This article is a Commentary on Barman et al. (2024), 244: 1013–1023.

It seems self-evident that generalist foragers switch more between resources than specialists but despite diverse ecological and evolutionary implications, how variation in switching relates to variation in preference warrants additional study. Here we tested predictions based on a simple probability model, using flower-foraging bees as a model system. In laboratory assays, we presented bumble bee (Bombus impatiens) workers with flowers of two species, Tecoma stans and T. alata, from which they could collect nectar and/or pollen. We quantified landing preference and occurrence of switching between species in successive visits. Bees varied greatly in floral preference. Almost half showed statistically significant preferences for one or the other species, while the rest were generalists in preference. As expected, generalists using both flower species switched more in successive visits than bees that were more specialized, a pattern fit to a quadratic function. However, generalist individuals switched more than expected based on null expectation. A Modified Jacob’s Index (MJI) of switching was significantly positively correlated with degree of preference: generalist bees had more negative MJI’s than specialist bees, indicating that even after the expected statistical effect of preference on switching was accounted for, they switched more than specialists. A simulation ruled out the possibility that the pattern was due to bias in MJI. Generalist-specialist differences in which food was collected (nectar versus pollen) were also ruled out. We offer possible explanations for our observed pattern and advocate consideration of preference and switching throughout behavioral ecology. Behavioral preference is the subject of a large literature in areas such as foraging, mating and communication. However, a preference measure alone does not necessarily tell us if choices for one alternative are made in runs or intermingled with choices for another alternative. The distinction between preference and the sequential pattern of choices is relevant in many contexts in behavioral ecology but has been a particular focus of study in flower foraging by pollinators. Even in that literature, the relationship between preference and sequential pattern in switching warrants further examination. In our study, bees were shown to vary in preference for flowers of two species. Some were generalists; some were specialists on one or the other species. Generalist bees switched more than specialist bees, even after controlling for statistical effects of preference on switching frequency. The report of this generalist-specialist pattern in switching may be novel and has far-reaching implications throughout the field of behavioral ecology.

Previous articleNext article No AccessZoologyThe Mind of a Bee. By Lars Chittka. Princeton (New Jersey): Princeton University Press. $29.95. vii + 260 p.; ill.; index. ISBN: 978-0-691-18047-2 (hc); 978-0-691-23624-7 (eb). 2022.Daniel R. PapajDaniel R. PapajEcology & Evolutionary Biology, University of Arizona, Tucson, Arizona Search for more articles by this author PDFPDF PLUSFull Text Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinkedInRedditEmail SectionsMoreDetailsFiguresReferencesCited by The Quarterly Review of Biology Volume 98, Number 1March 2023 Published in association with Stony Brook University Article DOIhttps://doi.org/10.1086/723936 Views: 15Total views on this site For permission to reuse, please contact [email protected]PDF download Crossref reports no articles citing this article.

The ontogeny of nectar robbing by pollinators is not well understood. In this study, we investigated the interplay of pre-existing biases and experience in the expression of nectar-robbing behavior by common eastern bumble bee (Bombus impatiens) workers. Flower-naïve bees were released individually into an arena containing six live Tecoma stans flowers in one of two treatments. One treatment consisted of open flowers bearing a single artificial slit, allowing the bee to rob or enter legitimately for nectar, while the other consisted of flowers bearing slits, whose corollas were plugged with cotton, requiring the bee to rob for nectar. A subset of bees was tested twice, once on each treatment; the order of treatments was balanced across bees. Results showed that first attempts by flower-naïve bees were biased nearly absolutely towards legitimate visitation regardless of flower treatment. Most bees in both treatment groups robbed over the course of a trial, but plugged flowers were robbed significantly more. Previous experience affected robbing frequency on subsequent visits, suggestive of learning; bees induced to rob on plugged flowers tended to continue to rob even when legitimate access was restored. We speculate that the initial bias towards legitimate visits is due to the flower corolla’s distinctive odor and nectar guides, to which bees respond innately. Bees nevertheless readily learn to rob, particularly when it is the only option for extracting nectar. Our findings support the view that studies of cognition are essential to understanding the pattern of cooperation and conflict in plant-pollinator mutualism. Nectar-robbing behavior is widely observed among pollinators in nature. Unlike visitation of flowers through the floral entrance, nectar robbing often does not transfer pollen. However, despite the importance of nectar robbing on plant fitness, little is known about the ontogeny of nectar-robbing behavior. In this study, we found that naïve Bombus impatiens workers strongly preferred legitimate visits over nectar robbing on their first visits to live flowers. However, bees quickly switched to nectar robbing when nectar could not be accessed legitimately and continued robbing even when legitimate access is restored. Our results suggest that flowers may take advantage of their pollinators’ innate responses for their own or mutual gain, but also that pollinators can overcome this manipulation through learning.

Within-species variation in pollinator behavior is widely observed, but its causes have been minimally investigated. Pollinator sex is associated with large differences in behavior that may lead to predictable differences in flower foraging, but this expectation has not been explicitly tested. We investigate sex-associated differences in nectar-foraging behavior of the hawkmoth Hyles lineata, using pollen on the proboscis as a proxy for flower visitation. We tested two predictions emerging from the literature: (1) the sexes differ in the flower species they visit, (2) females are more specialized in flower choice. We also examined potential drivers underlying these predictions by performing field and laboratory experiments to test whether males (3) switch among flower species more frequently, or (4) fly farther and therefore encounter more species than females. Consistent with prediction (1), pollen load composition differed between the sexes, indicative of visitation differences. Contrary to prediction (2), females consistently carried more species-rich pollen loads than males. (3) Both sexes switched between flower species at similar rates, suggesting that differences in floral fidelity are unlikely to explain why females are less specialized than males. (4) Males flew longer distances than females; coupled with larger between-site differences in pollen composition for females, this result suggests that sex differences in mobility influence foraging, and that females may forage more frequently and in smaller areas than males. Together, our results demonstrate that sex-associated foraging differences can be large and consistent over time, and highlight the importance of sex as a driver of variation in pollinator behavior.

Animals sometimes have prominent projections on or near their heads serving diverse functions such as male combat, mate attraction, digging, capturing prey, sensing or defence against predators. Some butterfly larvae possess a pair of long frontal projections; however, the function of those projections is not well known. Hestina japonica butterfly larvae have a pair of long hard projections on their heads (i.e., horns). Here we hypothesized that they use these horns to protect themselves from natural enemies (i.e., predators and parasitoids). Field surveys revealed that the primary natural enemies of H. japonica larvae were Polistes wasps. Cage experiments revealed that larvae with horns intact and larvae with horns removed and fitted with horns of other individuals succeeded in defending themselves against attacks of Polistes wasps significantly more often than larvae with horns removed. We discuss that the horns counter the paper wasps' hunting strategy of first biting the larvae's 'necks' and note that horns evolved repeatedly only within the Nymphalidae in a phylogeny of the Lepidoptera. This is the first demonstration that arthropods use head projections for physical defence against predators.

Organisms can often respond adaptively to a change in their environment through phenotypic plasticity in multiple traits, a phenomenon termed as multivariate plasticity. These different plastic responses could interact and affect each other's development as well as selection on each other, but the causes and consequences of these interactions have received relatively little attention. Here, we propose a new conceptual framework for understanding how different plastic responses can affect each other's development and why organisms should have multiple plastic responses. A plastic change in one trait could alter the phenotype of a second plastic trait by changing either the cue received by the organism (cue-mediated effect) or the response to that cue (response-mediated effect). Multivariate plasticity could benefit the organism either because the plastic responses work better when expressed together (synergy) or because each response is more effective under different environmental circumstances (complementarity). We illustrate these hypotheses with case studies, focusing on interactions between behavior and morphology, plastic traits that differ in their reversibility. Future empirical and theoretical research should investigate the consequences of these interactions for additional factors important for the evolution of plasticity, such as the limits and costs of plasticity.

We describe the nesting biology of Centris (Paracentris) burgdorfi, a solitary bee that nests in sandstone in northeastern Brazil. The nest consists of a shallow tunnel with access to the brood cells. Females of C. burgdorfi made 1-7 brood cells per nest with each cell requiring 2.58 +/- 0.40 ( +/- SD) days to construct. The average cell-building construction time was longer when compared to other Centris species. Females were larger than males, and this difference was reflected in the size of their respective emergence cells. The temperature within C. burgdorfi nests was lower when compared to ambient temperature. Our study is the first to report the nesting biology of C. burgdorfi. The detailed behavior of the female inside the nest was also described, which is unusual in the study of solitary bee nesting biology.

Mutualisms involve cooperation, but also frequently involve conflict. Plant-pollinator mutualisms are no exception. To facilitate animal pollination, flowering plants often offer pollen (their male gametes) as a food reward. Since plants benefit by maximizing pollen export to conspecific flowers, we might expect plants to cheat on pollen rewards. In intersexual floral mimicry, rewarding pollen-bearing male flowers (models) are mimicked by rewardless female flowers (mimics) on the same plant. Pollinators should therefore learn to avoid the unrewarding mimics. Plants might impede such learning by producing phenotypically variable flowers that cause bees to generalize among models and mimics during learning. In this laboratory study, we used partially artificial flowers (artificial petals, live reproductive parts) modeled after Begonia odorata to test whether variation in the size of rewarding male flowers (models) and unrewarding female flowers (mimics) affected how quickly bees learned both to recognize models and to reject mimics. Live unrewarding female flowers have 33% longer petals and have 31% greater surface area than live rewarding male flowers, which bees should easily discriminate. Yet while bees rapidly learned to reduce foraging effort on mimics, learning was not significantly affected by the degree to which flower size varied. Additionally, we found scant evidence that this was a result of bees altering response speed to maintain decision accuracy. Our study failed to provide evidence that flower size variation in intersexual floral mimicry systems exploits pollinator cognition, though we cannot rule out that other floral traits that are variable may be important. Furthermore, we propose that contrary to expectation, phenotypic variability in a Batesian mimicry system may not necessarily have significant effects on whether receivers effectively learn to discriminate models and mimics.

Animals foraging from flowers must assess their environment and make critical decisions about which patches, plants, and flowers to exploit to obtain limiting resources. The cognitive ecology of plant-pollinator interactions explores not only the complex nature of pollinator foraging behavior and decision making, but also how cognition shapes pollination and plant fitness. Floral visitors sometimes depart from what we think of as typical pollinator behavior and instead exploit floral resources by robbing nectar (bypassing the floral opening and instead consuming nectar through holes or perforations made in floral tissue). The impacts of nectar robbing on plant fitness are well-studied; however, there is considerably less understanding, from the animal’s perspective, about the cognitive processes underlying nectar robbing. Examining nectar robbing from the standpoint of animal cognition is important for understanding the evolution of this behavior and its ecological and evolutionary consequences. In this review, we draw on central concepts of foraging ecology and animal cognition to consider nectar robbing behavior either when individuals use robbing as their only foraging strategy or when they switch between robbing and legitimate foraging. We discuss sensory and cognitive biases, learning, and the role of a variable environment in making decisions about robbing vs. foraging legitimately. We also discuss ways in which an understanding of the cognitive processes involved in nectar robbing can address questions about how plant-robber interactions affect patterns of natural selection and floral evolution. We conclude by highlighting future research directions on the sensory and cognitive ecology of nectar robbing.

Learning plays an important role in food acquisition in a wide range of insect species. However, few studies have explored differences in the ability to learn floral cues among pollinator species across insect orders. In this study, we examined associative learning of flower color with nectar rewards for females or female workers in two bee species (an eusocial bumblebee [Bombus ignitus] and a solitary mason bee [Osmia orientalis]) and two hoverfly species (Eristalis cerealis and E. tenax). Prior data for females of four butterfly species (Idea leuconoe, Argyreus hyperbius, Pieris rapae, and Lycaena phlaeas) were included for analyses of flower color-learning rate in a total of eight species of three insect orders (Hymenoptera, Diptera, and Lepidoptera). All eight species learned flower colors associated with food. Flower color-learning rate was highest in B. ignitus, followed by the two larger butterflies (I. leuconoe and A. hyperbius), the two smaller butterflies (P. rapae and L. phlaeas), and the remaining species (E. cerealis, E. tenax, and O. orientalis). These results represent the first evidence that the ability to learn floral cues differs among flower-visiting insects of different orders. We discuss the adaptive significance of superior learning abilities in bumblebees and butterflies and that of inferior learning abilities in the two hoverflies and mason bees.

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 frequency of models and mimics only marginally shaped responses by naive bees and by bees experienced with the distribution and frequency of models and mimics. Our results provide evidence both of exploitation by the plant of signal detection trade-offs in bees and of resistance by the bees, via learning, to this exploitation. Critically, we provide experimental evidence that imperfect Batesian mimicry can be adaptive and, in contrast with expectations of signal detection theory, functions largely independently of the model and mimic frequency. This article is part of the theme issue ‘Signal detection theory in recognition systems: from evolving models to experimental tests’.

Similar to animal communication displays, flowers emit complex signals that attract pollinators. Signal complexity could lead to higher cognitive load for pollinators, impairing performance, or might benefit them by facilitating learning, memory and decision making. Here, we evaluated learning and memory in foragers of the bumble bee Bombus impatiens trained to simple (unimodal) versus complex (bimodal) signals under restrained conditions. Use of a proboscis extension response protocol enabled us to control the timing and duration of stimuli presented during absolute and differential learning tasks. Overall, we observed broad variation in performance under the two conditions, with bees trained to compound bimodal signals learning and remembering as well as, better than or more poorly than bees trained to unimodal signals. Interestingly, the outcome of training was affected by the specific colour-odour combination. Among unimodal stimuli, the performance with odour stimuli was higher than with colour stimuli, suggesting that olfactory signals played a more significant role in the compound bimodal condition. This was supported by the fact that after 24 h, most bimodal-treatment bees responded to odour but not visual stimuli. We did not observe differences in latency of response, suggesting that signal composition affected decision accuracy, not speed. We conclude that restrained bumble bee workers exhibit broad variation of responses to bimodal stimuli and that components of the bimodal signal may not be used equivalently. The analysis of bee performance under restrained conditions enables accurate control of the multimodal stimuli provided to individuals and to study the interaction of individual components within a compound.