Learning in the honey bee waggle dance.

The waggle dance of honey bees is a classic example of complex behavior and communication in animals. Despite long being considered a completely fixed and innate behavior, recent work is showing a role for social learning in tuning components of the waggle dance in naïve bees.

Spectral sensitivities of the orchid bee Euglossa dilemma.

Diurnal pollinators often rely on color cues to make decisions when visiting flowers. Orchid bees are major tropical pollinators, with most studies of their pollination behavior to date focusing on scent collection and chemical ecology. The objective of this study was to measure their spectral sensitivities to preliminarily characterize color vision in the orchid bee Euglossa dilemma and compare it to the known spectral sensitivity of other closely related bees. We compared E. dilemma's spectral sensitivities and opsin protein sequences to four closely related corbiculate bees. E. dilemma appears to have trichromatic vision, with spectral sensitivity peaks in the ultraviolet, blue, and green wavelengths (347 ± 0.957 (SE) nm, 429 ± 6.570 nm, and 537 ± 1.183 nm, respectively), similar to other measured bees. We found no differences between male and female E. dilemma visual systems despite neuroanatomical and behavioral differences reported in the literature. The lambda maxes of the ultraviolet-sensitive photoreceptors appeared to be the most conserved among the bees we compared. Meanwhile, both the lambda maxes of the blue photoreceptors and the blue opsin proteins sequences were the least conserved. Our results open up new possibilities for the study of color vision and color-mediated pollination behaviors in orchid bees.

Resource Availability Affects Seasonal Trajectories of Population-Level Learning.

AbstractEnvironmental effects on learning are well known, such as cognition that is mediated by nutritional consumption. Less known is how seasonally variable environments affect phenological trajectories of learning. Here, we test the hypothesis that nutritional availability affects seasonal trajectories of population-level learning in species with developmentally plastic cognition. We test this in bumble bees (Apidae: Bombus), a clade of eusocial insects that produce individuals at different time points across their reproductive season and exhibit organ developmental plasticity in response to nutritional consumption. To accomplish this, we develop a theoretical model that simulates learning development across a reproductive season for a colony parameterized with observed life history data. Our model finds two qualitative seasonal trajectories of learning: (1) an increase in learning across the season and (2) no change in learning across the season. We also find these two qualitative trajectories revealed by empirical learning data; the proportion of workers successfully completing a learning test increases across a season for two bumble bee species (Bombus auricomus, Bombus pensylvanicus) but does not change for another three (Bombus bimaculatus, Bombus griseocollis, Bombus impatiens). This study supports the novel consideration that resources affect seasonal trajectories of population-level learning in species with developmentally plastic cognition.

Memory and the value of social information in foraging bumble bees.

Not all information should be learned and remembered. The value of information is tied to the reliability and certainty of that information, which itself is determined by rates of environmental change, both within and across lifetimes. Theory of adaptive forgetting and remembering posits that memory should reflect the environment, with more valuable information remembered for longer amounts of time. Theory on biological preparedness predicts that rates of reliability through evolutionary time should influence what is learned and remembered. We use these ideas to predict that differential memory use will reflect the underlying value of the information being learned. We test this by comparing the learning and memory of social information versus floral information in foraging bumble bees. Bumble bees are extremely flexible in their use of both types of information and evidence suggests that social information is "special," reflecting biological preparedness. Our experiment tests how bumble bees learn and remember social and floral information when their reliabilities, and thus value, differ. We find that bees learn both types of information at a similar speed. Bees show a decrement of memory of the trained associations in both treatments, but retain trained socially reliable information for longer, at both 4-hour and 8-hour retention intervals. Both training treatments influence whether bees match or avoid the locations of demonstrators, and this interacts with retention interval. Bees trained under reliable floral cues and unreliable social cues avoid conspecifics after 8-hr and 24-hr retention intervals. Bees thus learn about the reliability or unreliability of social cues and use this to modify their choices across time.

Bumble bees exhibit body size clines across an urban gradient despite low genetic differentiation.

Environmental heterogeneity resulting from human-modified landscapes can increase intraspecific trait variation. However, less known is whether such phenotypic variation is driven by plastic or adaptive responses to local environments. Here, we study five bumble bee (Apidae: Bombus) species across an urban gradient in the greater Saint Louis, Missouri region in the North American Midwest and ask: (1) Can urban environments induce intraspecific spatial structuring of body size, an ecologically consequential functional trait? And, if so, (2) is this body size structure the result of plasticity or adaptation? We additionally estimate genetic diversity, inbreeding, and colony density of these species-three factors that affect extinction risk. Using ≥ 10 polymorphic microsatellite loci per species and measurements of body size, we find that two of these species (Bombus impatiens, Bombus pensylvanicus) exhibit body size clines across the urban gradient, despite a lack of population genetic structure. We also reaffirm reports of low genetic diversity in B. pensylvanicus and find evidence that Bombus griseocollis, a species thought to be thriving in North America, is inbred in the greater Saint Louis region. Collectively, our results have implications for conservation in urban environments and suggest that plasticity can cause phenotypic clines across human-modified landscapes.

Equivalent learning, but unequal participation: Male bumble bees learn comparably to females, but participate in cognitive assessments at lower rates.

Sex-specific cognitive abilities are well documented. These can occur when sexes engage in different ecological contexts. Less known is whether different ecological contexts can also drive sex-specific participation rates in behavioral tests. Here, we explore this question in bumble bees, a group of eusocial insects where worker females and males exhibit stark socioecological differences. Among myriad colony maintenance tasks, workers forage for themselves and developing brood, while males forage only for themselves while mate-searching. Following upon previous studies suggesting no sex differences in bumble bee learning, we test the hypothesis that despite having equivalent associative learning abilities, males participate in cognitive assessments offering nutritional rewards at lower rates. Testing > 500 bees from nine colonies in a differential conditioning protocol, we find support for our hypothesis. An equivalent proportion of workers and males successfully completed our cognitive assessment, while a significantly lower proportion of males participated in the entire protocol. Unequal participation is a perennial issue in the behavioral sciences, limiting sample size and potentially biasing results. Our results suggest that to understand the true range of variation in cognition, sex-differences in participation must be accounted for.

Teaching animal behavior online: A primer for the pandemic and beyond.

Behavior courses face numerous challenges when moving to an online environment, as has been made necessary by the COVID-19 pandemic. These challenges occur largely because behavior courses, like most organismal biology courses, often stress experiential learning through laboratories that involve live animals, as well as a lecture component that emphasizes formative assessment, discussion, and critical thinking. Although online behavior courses may be remote, they can still be interactive and social, and designed with inclusive pedagogy. Here, we discuss some of the key decisions that instructors should consider, provide recommendations, and point out new opportunities for student learning that stem directly from the move to online instruction. Specific topics include challenges related to generating an inclusive and engaging online learning environment, synchronous versus asynchronous formats, assignments that enhance student learning, testing format and execution, grade schemes, design of laboratory experiences including opportunities for community science, design of synthetic student projects, and workload balance for students and instructors. We designed this primer both for animal behavior instructors who need to quickly transition to online teaching in the midst of a pandemic, and for those facing such transitions in upcoming terms. Much of the manuscript's content should also be of general interest and value to instructors from all areas of organismal biology who are attempting to quickly transition to online teaching.

Intraspecific Variation in Worker Body Size Makes North American Bumble Bees (Bombus spp.) Less Susceptible to Decline.

Population declines have been documented in approximately one-third of bumble bee species. Certain drivers of these declines are known; however, less is known about the interspecific trait differences that make certain species more susceptible to decline. Two traits that have implications for responding to rapidly changed environments may be particularly consequential for bumble bee populations: intraspecific body size variation and brain size. Bumble bee body size is highly variable and is likely adaptive at the colony level, and brain size correlates with cognitive traits (e.g., behavioral plasticity) in many groups. Trait variation and plasticity may buffer species against negative effects of rapidly changed environments. Using phylogenetically controlled analyses of 31 North American bumble bee species, we find that higher intraspecific body size variation is associated with species having increased their relative abundance over time. However, this variation does not significantly interact with tongue length, another trait thought to influence bees' decline susceptibility. Head size, a proxy for brain size, is not correlated with change in relative abundance. Our results support the hypothesis that variation in body size makes species less susceptible to decline in rapidly altered environments and suggests that this variation is important to the success of bumble bee populations.

Sampling and tracking a changing environment: persistence and reward in the foraging decisions of bumblebees.

The question of when to collect new information and how to apply that information is central to much of behaviour. Theory suggests that the value of collecting information, or sampling, depends on environmental persistence and on the relative costs of making wrong decisions. However, empirical tests of how these variables interact are lacking. We tested whether bumblebee foraging decisions are indeed influenced by these two factors. We gave bees repeated choices between a resource providing a steady, mediocre reward and a resource fluctuating between a low reward and a high reward. In this paradigm, we manipulated environmental persistence by changing how long the quality of a fluctuating resource remained stable at one reward level. We manipulated the costs of decision errors by changing the relative values of the available rewards. Bees sampled the fluctuating resource more frequently when it changed quality more frequently, indicating that they measured environmental persistence and reacted to it as predicted by theory. Bees showed surprisingly suboptimal tracking, not reliably choosing the currently best resource except when the fluctuating resource was very persistent and the potential rewards high. While bees modify their choices in response to different levels of change and potential rewards, they do not always do so according to optimality predictions.

Foraging Bumble Bees Weigh the Reliability of Personal and Social Information.

Many animals, including insects, make decisions using both personally gathered information and social information derived from the behavior of other, usually conspecific, individuals [1]. Moreover, animals adjust use of social versus personal information appropriately under a variety of experimental conditions [2-5]. An important factor in how information is used is the information's reliability, that is, how consistently the information is correlated with something of relevance in the environment [6]. The reliability of information determines which signals should be attended to during communication [6-9], which types of stimuli animals should learn about, and even whether learning should evolve [10, 11]. Here, we show that bumble bees (Bombus impatiens) account for the reliability of personally acquired information (which flower color was previously associated with reward) and social information (which flowers are chosen by other bees) in making foraging decisions; however, the two types of information are not treated equally. Bees prefer to use social information if it predicts a reward at all, but if social information becomes entirely unreliable, flower color will be used instead. This greater sensitivity to the reliability of social information, and avoidance of conspecifics in some cases, may reflect the specific ecological circumstances of bee foraging. Overall, the bees' ability to make decisions based on both personally acquired and socially derived information, and the relative reliability of both, demonstrates a new level of sophistication and flexibility in animal, particularly insect, decision-making.

Experimental evolution of prepared learning.

Animals learn some things more easily than others. To explain this so-called prepared learning, investigators commonly appeal to the evolutionary history of stimulus-consequence relationships experienced by a population or species. We offer a simple model that formalizes this long-standing hypothesis. The key variable in our model is the statistical reliability of the association between stimulus, action, and consequence. We use experimental evolution to test this hypothesis in populations of Drosophila. We systematically manipulated the reliability of two types of experience (the pairing of the aversive chemical quinine with color or with odor). Following 40 generations of evolution, data from learning assays support our basic prediction: Changes in learning abilities track the reliability of associations during a population's selective history. In populations where, for example, quinine-color pairings were unreliable but quinine-odor pairings were reliable, we find increased sensitivity to learning the quinine-odor experience and reduced sensitivity to learning quinine-color. To the best of our knowledge this is the first experimental demonstration of the evolution of prepared learning.

Tracking a changing environment: optimal sampling, adaptive memory and overnight effects.

Foraging in a variable environment presents a classic problem of decision making with incomplete information. Animals must track the changing environment, remember the best options and make choices accordingly. While several experimental studies have explored the idea that sampling behavior reflects the amount of environmental change, we take the next logical step in asking how change influences memory. We explore the hypothesis that memory length should be tied to the ecological relevance and the value of the information learned, and that environmental change is a key determinant of the value of memory. We use a dynamic programming model to confirm our predictions and then test memory length in a factorial experiment. In our experimental situation we manipulate rates of change in a simple foraging task for blue jays over a 36 h period. After jays experienced an experimentally determined change regime, we tested them at a range of retention intervals, from 1 to 72 h. Manipulated rates of change influenced learning and sampling rates: subjects sampled more and learned more quickly in the high change condition. Tests of retention revealed significant interactions between retention interval and the experienced rate of change. We observed a striking and surprising difference between the high and low change treatments at the 24h retention interval. In agreement with earlier work we find that a circadian retention interval is special, but we find that the extent of this 'specialness' depends on the subject's prior experience of environmental change. Specifically, experienced rates of change seem to influence how subjects balance recent information against past experience in a way that interacts with the passage of time.

Components of change in the evolution of learning and unlearned preference.

Several phenomena in animal learning seem to call for evolutionary explanations, such as patterns of what animals learn and do not learn. While several models consider how evolution should influence learning, we have very little data testing these models. Theorists agree that environmental change is a central factor in the evolution of learning. We describe a mathematical model and an experiment, testing two components of change: reliability of experience and predictability of the best action. Using replicate populations of Drosophila we varied statistical patterns of change across 30 generations. Our results provide the first experimental demonstration that some types of environmental change favour learning while others select against it, giving the first experimental support for a more nuanced interpretation of the selective factors influencing the evolution of learning.

Why do animals make better choices in patch-leaving problems?

This study compares two procedures for the study of choices that differ in time and amount, namely the self-control and patch procedures. The self-control procedure offers animals a binary mutually exclusive choice between a smaller-sooner and larger-later option. This procedure dominates the choice literature. It seems to address the idea of choice in a general, but relatively abstract way. Animals in the self-control situation frequently prefer the smaller-sooner option even when the larger-later option yields a higher long-term intake rate. In contrast, the patch procedure poses an economically similar question, but simulates the naturally occurring problem of patch exploitation. In the patch procedure, animals choose between leaving and staying. Emerging evidence suggests that animals perform better and achieve higher long-term intake rates in the patch situation. This observation raises the question of how a single set of choice mechanisms could produce these different outcomes. The experiment presented here tests two hypotheses about the relationship between the patch and self-control situations. First, it asks whether the short-term rate rule can predict choice behavior in both situations. Second, it tests the second-delivery hypothesis which holds that the patch situation favors choosing the larger more delayed option (staying) because this option ultimately leads to two food deliveries. The results of this experiment convincingly reject both of these hypotheses. Indeed, our results suggest that none of the simple rules based on time and amount can explain the observed differences between the patch and self-control situations. This result challenges the generality of existing models of choice.

Female prairie voles do not choose males based on their frequency of scent marking.

We conducted an experiment to test three alternative hypotheses for the function of frequency of scent marking in male prairie voles, MICROTUS OCHROGASTER: (1) sexual attraction (to advertise male quality for mating); (2) reproductive competition; and (3) self-advertisement or individual identity. In laboratory experiments, males deposited scent on all areas of a bare substrate, and more in an area next to a stimulus animal than other areas, regardless of the stimulus animal's sex. Females did not choose mates based on their frequency of scent marking and scent marking did not antagonize or stimulate aggression between males. The frequency of scent marking by males supports the individual identity hypothesis, and is less consistent with the sexual attraction or reproductive competition hypotheses. Mate choice is likely based on a complex suite of characters, but at least in prairie voles, the frequency of scent marking by males does not appear to be one of them.

Multi-male mating, probability of conception, and litter size in the prairie vole (Microtus ochrogaster).

We conducted a mating experiment in the laboratory using prairie voles, Microtus ochrogaster, to document that multi-male mating (MMM) can occur in this supposedly monogamous species and to test two hypotheses for the advantages of MMM in female mammals. The two hypotheses are that MMM (1) increases the probability of pregnancy and (2) increases litter size. We also tested the hypothesis that multiple copulations, rather than multiple partners, increases litter size and/or probability of pregnancy. Females were given a choice of mating with any of three males, each of which was tethered in a separate compartment. The mate choice bouts were recorded on videotape. We recorded the number of copulations and number of males with which females mated over a 24 h period. Litter size and probability of pregnancy were not significantly different for females that mated with one, two or three males. Increasing numbers of copulations, independent from the number of males, also did not increase litter size but did significantly increase the probability of pregnancy. MMM, at least in prairie voles, must serve some function other than increasing litter size and probability of conception.