Honey bee colonies change their foraging decisions after in-hive experiences with unsuitable pollen.

Pollen is the protein resource for Apis mellifera and its selection affects colony development and productivity. Honey bee foragers mainly lose their capacity to digest pollen, so we expect that those pollen constituents that can only be evaluated after ingestion will not influence their initial foraging preferences at food sources. We predicted that pollen composition may be evaluated in a delayed manner within the nest, for example, through the effects that the pollen causes on the colony according to its suitability after being used by in-hive bees. To address whether pollen foraging is mediated by in-hive experiences, we conducted dual-choice experiments to test the avoidance of pollen adulterated with amygdalin, a deterrent that causes post-ingestion malaise. In addition, we recorded pollen selection in colonies foraging in the field after being supplied or not with amygdalin-adulterated pollen from one of the dominant flowering plants (Diplotaxis tenuifolia). Dual-choice experiments revealed that foragers did not avoid adulterated pollens at the foraging site; however, they avoided pollen that had been offered adulterated within the nest on the previous days. In field experiments, pollen samples from colonies supplied with amygdalin-adulterated pollen were more diverse than controls, suggesting that pollen foraging was biased towards novel sources. Our findings support the hypothesis that pollen assessment relies on in-hive experiences mediated by pollen that causes post-ingestive malaise.

Altered nociceptive behavior and emotional contagion of pain in mouse models of autism.

Individuals with autism spectrum disorder (ASD) have altered sensory processing but may ineffectively communicate their experiences. Here, we used a battery of nociceptive behavioral tests to assess sensory alterations in two commonly used mouse models of ASD, BTBR T+ Itpr3tf /J (BTBR), and fragile-X mental retardation-1 knockout (Fmr1-KO) mice. We also asked whether emotional contagion, a primitive form of empathy, was altered in BTBR and Fmr1 KO mice when experiencing pain with a social partner. BTBR mice demonstrated mixed nociceptive responses with hyporesponsivity to mechanical/thermal stimuli and intraplantar injections of formalin and capsaicin while displaying hypersensitivity on the acetic acid test. Fmr1-KO mice were hyposensitive to mechanical stimuli and intraplantar injections of capsaicin and formalin. BTBR and Fmr1-KO mice developed significantly less mechanical allodynia following intraplantar injections of complete Freund's adjuvant, while BTBR mice developed slightly more thermal hyperalgesia. Finally, as measured by the formalin and acetic acid writhing tests, BTBR and Fmr1-KO mice did not show emotional contagion of pain. In sum, our findings indicate that depending on the sensation, pain responses may be mixed, which reflects findings in ASD individuals.

Acoustic particle motion detection in the snapping shrimp (Alpheus richardsoni).

Many crustaceans produce sounds that might be used in communication. However, little is known about sound detection in crustaceans, hindering our understanding of crustacean acoustic communication. Sound detection has been determined only for a few species, and for many species, it is unclear how sound is perceived: as particle motion or sound pressure. Snapping shrimp are amongst the loudest and most pervasive marine sound sources. They produce snaps during interactions with conspecifics, and they also interact with soniferous heterospecifics. If they can hear, then sound could facilitate key behavioral interactions. We measured the auditory sensitivity of the snapping shrimp, Alpheus richardsoni, using auditory evoked potentials in response to a shaker table that generated only particle motion and an underwater speaker that generated both particle motion and sound pressure. Auditory detection was most sensitive between 80 and 100 Hz, and auditory evoked potentials were detected up to 1500 Hz. Snapping shrimp responded to both the shaker table and the underwater speaker, demonstrating that they detect acoustic particle motion. Crushing the statocyst reduced or eliminated hearing sensitivity. We conclude that snapping shrimp detect acoustic particle motion using the statocyst, they might detect conspecifics and heterospecifics, and hearing could facilitate key behavioral interactions.

Local Axonal Conduction Shapes the Spatiotemporal Properties of Neural Sequences.

Sequential activation of neurons has been observed during various behavioral and cognitive processes, but the underlying circuit mechanisms remain poorly understood. Here, we investigate premotor sequences in HVC (proper name) of the adult zebra finch forebrain that are central to the performance of the temporally precise courtship song. We use high-density silicon probes to measure song-related population activity, and we compare these observations with predictions from a range of network models. Our results support a circuit architecture in which heterogeneous delays between sequentially active neurons shape the spatiotemporal patterns of HVC premotor neuron activity. We gauge the impact of several delay sources, and we find the primary contributor to be slow conduction through axonal collaterals within HVC, which typically adds between 1 and 7.5 ms for each link within the sequence. Thus, local axonal "delay lines" can play an important role in determining the dynamical repertoire of neural circuits.

Noise-Sensitive But More Precise Subcortical Representations Coexist with Robust Cortical Encoding of Natural Vocalizations.

Humans and animals maintain accurate sound discrimination in the presence of loud sources of background noise. It is commonly assumed that this ability relies on the robustness of auditory cortex responses. However, only a few attempts have been made to characterize neural discrimination of communication sounds masked by noise at each stage of the auditory system and to quantify the noise effects on the neuronal discrimination in terms of alterations in amplitude modulations. Here, we measured neural discrimination between communication sounds masked by a vocalization-shaped stationary noise from multiunit responses recorded in the cochlear nucleus, inferior colliculus, auditory thalamus, and primary and secondary auditory cortex at several signal-to-noise ratios (SNRs) in anesthetized male or female guinea pigs. Masking noise decreased sound discrimination of neuronal populations in each auditory structure, but collicular and thalamic populations showed better performance than cortical populations at each SNR. In contrast, in each auditory structure, discrimination by neuronal populations was slightly decreased when tone-vocoded vocalizations were tested. These results shed new light on the specific contributions of subcortical structures to robust sound encoding, and suggest that the distortion of slow amplitude modulation cues conveyed by communication sounds is one of the factors constraining the neuronal discrimination in subcortical and cortical levels.SIGNIFICANCE STATEMENT Dissecting how auditory neurons discriminate communication sounds in noise is a major goal in auditory neuroscience. Robust sound coding in noise is often viewed as a specific property of cortical networks, although this remains to be demonstrated. Here, we tested the discrimination performance of neuronal populations at five levels of the auditory system in response to conspecific vocalizations masked by noise. In each acoustic condition, subcortical neurons better discriminated target vocalizations than cortical ones and in each structure, the reduction in discrimination performance was related to the reduction in slow amplitude modulation cues.

Do honey bee (Apis mellifera) foragers recruit their nestmates to native forbs in reconstructed prairie habitats?

Honey bee (Apis mellifera) colonies are valued for the pollination services that they provide. However, colony mortality has increased to unsustainable levels in some countries, including the United States. Landscape conversion to monocrop agriculture likely plays a role in this increased mortality by decreasing the food sources available to honey bees. Many land owners and organizations in the Upper Midwest region of the United States would like to restore/reconstruct native prairie habitats. With increasing public awareness of high bee mortality, many landowners and beekeepers have wondered whether these restored prairies could significantly improve honey bee colony nutrition. Conveniently, honey bees have a unique communication signal called a waggle dance, which indicates the locations of the flower patches that foragers perceive as highly profitable food sources. We used these communication signals to answer two main questions: First, is there any part of the season in which the foraging force of a honey bee colony will devote a large proportion of its recruitment efforts (waggle dances) to flower patches within prairies? Second, will honey bee foragers advertise specific taxa of native prairie flowers as profitable pollen sources? We decoded 1528 waggle dances in colonies located near two large, reconstructed prairies. We also collected pollen loads from a subset of waggle-dancing bees, which we then analyzed to determine the flower taxon advertised. Most dances advertised flower patches outside of reconstructed prairies, but the proportion of dances advertising nectar sources within prairies increased significantly in the late summer/fall at one site. Honey bees advertised seven native prairie taxa as profitable pollen sources, although the three most commonly advertised pollen taxa were non-native. Our results suggest that including certain native prairie flower taxa in reconstructed prairies may increase the chances that colonies will use those prairies as major food sources during the period of greatest colony growth and honey production.

The structure of species discrimination signals across a primate radiation.

Discriminating conspecifics from heterospecifics can help avoid costly interactions between closely related sympatric species. The guenons, a recent primate radiation, exhibit high degrees of sympatry and form multi-species groups. Guenons have species-specific colorful face patterns hypothesized to function in species discrimination. Here, we use a machine learning approach to identify face regions most essential for species classification across fifteen guenon species. We validate these computational results using experiments with live guenons, showing that facial traits critical for accurate classification influence selective attention toward con- and heterospecific faces. Our results suggest variability among guenon species in reliance on single-trait-based versus holistic facial characteristics for species discrimination, with behavioral responses and computational results indicating variation from single-trait to whole-face patterns. Our study supports a role for guenon face patterns in species discrimination, and shows how complex signals can be informative about differences between species across a speciose and highly sympatric radiation.

Acoustic behaviour of male European lobsters (Homarus gammarus) during agonistic encounters.

Previous studies have demonstrated that male European lobsters (Homarus gammarus) use chemical and visual signals as a means of intraspecific communication during agonistic encounters. In this study, we show that they also produce buzzing sounds during these encounters. This result was missed in earlier studies because low-frequency buzzing sounds are highly attenuated in tanks, and are thus difficult to detect with hydrophones. To address this issue, we designed a behavioural tank experiment using hydrophones, with accelerometers placed on the lobsters to directly detect their carapace vibrations (i.e. the sources of the buzzing sounds). While we found that both dominant and submissive individuals produced carapace vibrations during every agonistic encounter, very few of the associated buzzing sounds (15%) were recorded by the hydrophones. This difference is explained by their high attenuation in tanks. We then used the method of algorithmic complexity to analyse the carapace vibration sequences as call-and-response signals between dominant and submissive individuals. Even though some intriguing patterns appeared for closely size-matched pairs (<5 mm carapace length difference), the results of the analysis did not permit us to infer that the processes underlying these sequences could be differentiated from random ones. Thus, such results prevented any conclusions about acoustic communication. This concurs with both the high attenuation of the buzzing sounds during the experiments and the poor understanding of acoustic perception by lobsters. New approaches that circumvent tank acoustic issues are now required to validate the existence of acoustic communication in lobsters.

Early genistein exposure of California mice and effects on the gut microbiota-brain axis.

Human offspring encounter high amounts of phytoestrogens, such as genistein (GEN), through maternal diet and soy-based formulas. Such chemicals can exert estrogenic activity and thereby disrupt neurobehavioral programming. Besides inducing direct host effects, GEN might cause gut dysbiosis and alter gut metabolites. To determine whether exposure to GEN affects these parameters, California mice (Peromyscus californicus) dams were placed 2 weeks prior to breeding and throughout gestation and lactation on a diet supplemented with GEN (250 mg/kg feed weight) or AIN93G phytoestrogen-free control diet (AIN). At weaning, offspring socio-communicative behaviors, gut microbiota and metabolite profiles were assayed. Exposure of offspring to GEN-induced sex-dependent changes in gut microbiota and metabolites. GEN exposed females were less likely to investigate a novel female mouse when tested in a three-chamber social test. When isolated, GEN males and females exhibited increased latency to elicit their first call, suggestive of reduced motivation to communicate with other individuals. Correlation analyses revealed interactions between GEN-induced microbiome, metabolome and socio-communicative behaviors. Comparison of GEN males with AIN males revealed the fraction of calls above 20 kHz was associated with daidzein, α-tocopherol, Flexispira spp. and Odoribacter spp. Results suggest early GEN exposure disrupts normal socio-communicative behaviors in California mice, which are otherwise evident in these social rodents. Such effects may be due to GEN disruptions on neural programming but might also be attributed to GEN-induced microbiota shifts and resultant changes in gut metabolites. Findings indicate cause for concern that perinatal exposure to GEN may detrimentally affect the offspring microbiome-gut-brain axis.

Honey bee waggle dance communication increases diversity of pollen diets in intensively managed agricultural landscapes.

The benefits of honey bee dance communication for colony performance in different resource environments are still not well understood. Here, we test the hypothesis that directional dance communication enables honey bee colonies to maintain a diverse pollen diet, especially in landscapes with low resource diversity. To test this hypothesis, we placed 24 Apis mellifera L. colonies with either intact or experimentally disrupted dance communication in eight agricultural landscapes that differed in the diversity of flowering plants and in the dominance of mass-flowering crops. Pollen from incoming foragers was collected and identified via DNA metabarcoding. Disrupting dance communication affected the way the diversity of honey bee pollen diets was impacted by the dominance of mass-flowering crops in available flower resources (p = .04). With increasing dominance of mass-flowering crops in resource environments, foragers of colonies with intact communication foraged on an increasing proportion of available plant genera (p = .01). This was not the case for colonies with disrupted dance communication (p = .5). We conclude that the honey bee dance communication benefits pollen foraging on diverse plant resources and thereby contributes to high quality nutrition in environments with low-resource diversity.

Honey bees increase their foraging performance and frequency of pollen trips through experience.

Honey bee foragers must supply their colony with a balance of pollen and nectar to sustain optimal colony development. Inter-individual behavioural variability among foragers is observed in terms of activity levels and nectar vs. pollen collection, however the causes of such variation are still open questions. Here we explored the relationship between foraging activity and foraging performance in honey bees (Apis mellifera) by using an automated behaviour monitoring system to record mass on departing the hive, trip duration, presence of pollen on the hind legs and mass upon return to the hive, during the lifelong foraging career of individual bees. In our colonies, only a subset of foragers collected pollen, and no bee exclusively foraged for pollen. A minority of very active bees (19% of the foragers) performed 50% of the colony's total foraging trips, contributing to both pollen and nectar collection. Foraging performance (amount and rate of food collection) depended on bees' individual experience (amount of foraging trips completed). We argue that this reveals an important vulnerability for these social bees since environmental stressors that alter the activity and reduce the lifespan of foragers may prevent bees ever achieving maximal performance, thereby seriously compromising the effectiveness of the colony foraging force.

Adaptation and spectral enhancement at auditory temporal perceptual boundaries - Measurements via temporal precision of auditory brainstem responses.

In human and animal auditory perception the perceived quality of sound streams changes depending on the duration of inter-sound intervals (ISIs). Here, we studied whether adaptation and the precision of temporal coding in the auditory periphery reproduce general perceptual boundaries in the time domain near 20, 100, and 400 ms ISIs, the physiological origin of which are unknown. In four experiments, we recorded auditory brainstem responses with five wave peaks (P1 -P5) in response to acoustic models of communication calls of house mice, who perceived these calls with the mentioned boundaries. The newly introduced measure of average standard deviations of wave latencies of individual animals indicate the waves' temporal precision (latency jitter) mostly in the range of 30-100 µs, very similar to latency jitter of single neurons. Adaptation effects of response latencies and latency jitter were measured for ISIs of 10-1000 ms. Adaptation decreased with increasing ISI duration following exponential or linear (on a logarithmic scale) functions in the range of up to about 200 ms ISIs. Adaptation effects were specific for each processing level in the auditory system. The perceptual boundaries near 20-30 and 100 ms ISIs were reflected in significant adaptation of latencies together with increases of latency jitter at P2-P5 for ISIs < ~30 ms and at P5 for ISIs < ~100 ms, respectively. Adaptation effects occurred when frequencies in a sound stream were within the same critical band. Ongoing low-frequency components/formants in a sound enhanced (decrease of latencies) coding of high-frequency components/formants when the frequencies concerned different critical bands. The results are discussed in the context of coding multi-harmonic sounds and stop-consonants-vowel pairs in the auditory brainstem. Furthermore, latency data at P1 (cochlea level) offer a reasonable value for the base-to-apex cochlear travel time in the mouse (0.342 ms) that has not been determined experimentally.

Honey bee foraging ecology: Season but not landscape diversity shapes the amount and diversity of collected pollen.

The availability of pollen in agricultural landscapes is essential for the successful growth and reproduction of honey bee colonies (Apis mellifera L.). The quantity and diversity of collected pollen can influence the growth and health of honey bee colonies, but little is known about the influence of landscape structure on pollen diet. In a field experiment, we rotated 16 honey bee colonies across 16 agricultural landscapes, used traps to collect samples of collected pollen and observed intra-colonial dance communication to gain information about foraging distances. DNA metabarcoding was applied to analyze mixed pollen samples. Neither the amount of collected pollen nor pollen diversity was related to landscape diversity. However, we found a strong seasonal variation in the amount and diversity of collected pollen in all sites independent of landscape diversity. The observed increase in foraging distances with decreasing landscape diversity suggests that honey bees compensated for lower landscape diversity by increasing their pollen foraging range in order to maintain pollen amount and diversity. Our results underscore the importance of a diverse pollen diet for honey bee colonies. Agri-environmental schemes aiming to support pollinators should focus on possible spatial and temporal gaps in pollen availability and diversity in agricultural landscapes.

Dietary constraints can preclude the expression of an honest chemical sexual signal.

Identifying the factors that underlie signal divergences remains challenging in studies of animal communication. Regarding the chemical signalling, different compounds can be found in some species but be absent in others. We hypothesized that if the costs that are associated with the expression of some compounds are too high, their presence in the signal may be restricted. However, these compounds may be expressed and be functional when those costs are relaxed. Vitamin E (α-tocopherol), a dietary compound with metabolic relevancy, acts as an honest chemical sexual signal in many lizards but no in others such as the Carpetan Rock lizard (Iberolacerta cyreni). We investigated whether dietary supplementation favours the expression of this vitamin in scents of I. cyreni. We show that dietary constraints can preclude the expression of vitamin E in chemical secretions of wild males because was expressed when it was experimentally provided in the diet. Vitamin E supplementation also heightened the immune response of males and increased the interest of their scent for females, highlighting the vitamin E as a chemical sexual signal in this species. We suggest that diet could decisively act as a driver of intra- and interspecific divergences in the chemical signalling of lizards.

Monoaminergic integration of diet and social signals in the brains of juvenile spadefoot toads.

Social behavior often includes the production of species-specific signals (e.g. mating calls or visual displays) that evoke context-dependent behavioral responses from conspecifics. Monoamines are important neuromodulators that have been implicated in context-dependent social behavior, yet we know little about the development of monoaminergic systems and whether they mediate the effects of early life experiences on adult behavior. We examined the effects of diet and social signals on monoamines early in development in the plains spadefoot toad (Spea bombifrons), a species in which diet affects the developmental emergence of species recognition and body condition affects the expression of adult mating preferences. To do so, we manipulated the diet of juveniles for 6 weeks following metamorphosis and collected their brains 40 min following the presentation of either a conspecific or a heterospecific call. We measured levels of monoamines and their metabolites using high pressure liquid chromatography from tissue punches of the auditory midbrain (i.e. torus semicircularis), hypothalamus and preoptic area. We found that call type affected dopamine and noradrenaline signaling in the auditory midbrain and that diet affected dopamine and serotonin in the hypothalamus. In the preoptic area, we detected an interaction between diet and call type, indicating that diet modulates how the preoptic area integrates social information. Our results suggest that the responsiveness of monoamine systems varies across the brain and highlight preoptic dopamine and noradrenaline as candidates for mediating effects of early diet experience on later expression of social preferences.

Phenotypes associated with psychiatric disorders are sex-specific in a mutant mouse line.

Wnt1-Cre- and Wnt1-GAL4 double transgenic (dTg) mice are used to study neural crest cell lineages by utilizing either the Cre/loxP or the GAL4/UAS system. We have previously shown that these mice exhibit behavioral abnormalities that resemble certain behaviors of psychiatric disorders and histologic alterations in the cholinergic and glutamatergic systems in the brain. The objective of the current study was to extend the behavioral analyses in these mice and to determine whether there were any sex-specific differences in the prevalence or severity of these behaviors. In the present study, we demonstrate additional behavioral abnormalities in dTg mice, such as increased locomotor activity, decreased social behavior, and an increased frequency in vertical jumping. Of these, the proclivity for vertical jumping was observed only in male dTg mice. In contrast, MK-801 administration induced increased locomotion in only female dTg mice. Furthermore, the concentrations of prolactin in the sera and oxytocin in the hypothalamus were both reduced only in female dTg mice, compared to controls. These sex-dependent behavioral and hormonal abnormalities in the dTG mice suggest that the phenotype of certain psychiatric disorders may be influenced by both genetic and sex-specific factors.

Nectar loads as fuel for collecting nectar and pollen in honeybees: adjustment by sugar concentration.

When honeybee foragers leave the nest, they receive nectar from nest mates for use as fuel for flight or as binding material to build pollen loads. We examined whether the concentration of nectar carried from the nest changes with the need for sugar. We found that pollen foragers had more-concentrated nectar (61.8 %) than nectar foragers (43.8 %). Further analysis revealed that the sugar concentration of the crop load increased significantly with waggle duration, an indicator of food-source distance, in both groups of foragers. Crop volume also increased with waggle duration. The results support our argument that foragers use concentrated nectar when the need for sugar is high and suggest that they precisely adjust the amount of sugar in the crop by altering both volume and nectar concentrations. We also investigated the impact of the area where foragers receive nectar on the crop load concentration at departure. Although nectar and pollen foragers tend to load nectar at different areas in the nest, area did not have a significant effect on crop load concentration. Departing foragers showed an average of 2.2 momentary (<1 s) begging trophallactic contacts before leaving the nest. They might be rejecting nectar with inappropriate concentrations during these contacts.

Studying Socio-Affective Communication in Rats through Playback of Ultrasonic Vocalizations.

Rats are able to produce ultrasonic vocalizations (USVs). Such USVs are an important component of the rat social behavior repertoire and serve distinct communicative functions as socio-affective signals. Depending on the emotional valence of the situation, juvenile and adult rats utter (1) aversive 22-kHz USVs conveying an appeasing and/or alarming function; or (2) appetitive 50-kHz USVs, which act as social contact calls, amongst others. A 50-kHz USV radial maze playback paradigm that allows assessment of the behavioral responses displayed by the recipients in a highly standardized manner has been developed. In this newly developed paradigm, a rat is exposed individually to playback of natural 50-kHz USVs and appropriate acoustic control stimuli using an acoustic presentation system for ultrasound. By this means, it has been consistently shown that 50-kHz USVs lead to social approach behavior in the recipient, supporting the notion that they serve an affiliative function as social contact calls.

Distribution and Abundance of Glucocorticoid and Mineralocorticoid Receptors throughout the Brain of the Great Tit (Parus major).

The glucocorticoid stress response, regulated by the hypothalamic-pituitary-adrenal (HPA) axis, enables individuals to cope with stressors through transcriptional effects in cells expressing the appropriate receptors. The two receptors that bind glucocorticoids-the mineralocorticoid receptor (MR) and glucocorticoid receptor (GR)-are present in a variety of vertebrate tissues, but their expression in the brain is especially important. Neural receptor patterns have the potential to integrate multiple behavioral and physiological traits simultaneously, including self-regulation of glucocorticoid secretion through negative feedback processes. In the present work, we quantified the expression of GR and MR mRNA throughout the brain of a female great tit (Parus major), creating a distribution map encompassing 48 regions. This map, the first of its kind for P. major, demonstrated a widespread but not ubiquitous distribution of both receptor types. In the paraventricular nucleus of the hypothalamus (PVN) and the hippocampus (HP)-the two brain regions that we sampled from a total of 25 birds, we found high GR mRNA expression in the former and, unexpectedly, low MR mRNA in the latter. We examined the covariation of MR and GR levels in these two regions and found a strong, positive relationship between MR in the PVN and MR in the HP and a similar trend for GR across these two regions. This correlation supports the idea that hormone pleiotropy may constrain an individual's behavioral and physiological phenotype. In the female song system, we found moderate GR in hyperstriatum ventrale, pars caudalis (HVC), and moderate MR in robust nucleus of the arcopallium (RA). Understanding intra- and interspecific patterns of glucocorticoid receptor expression can inform us about the behavioral processes (e.g. song learning) that may be sensitive to stress and stimulate future hypotheses concerning the relationships between receptor expression, circulating hormone concentrations and performance traits under selection, including behavior.

Effects of Phenibut and Citrocard on Non-Competitive and Competitive Behavior during Provoked Aggression in Animals.

Anti-aggressive effects of phenibut (25 mg/kg) and its structural analogue citrocard (50 mg/kg) were revealed in rats under condition of provoked intraspecific aggression. These substances significantly decreased manifestations of aggression in animals: they increased the latency of attacks and reduced their number. Anti-aggressive effects of citrocard were more pronounced than effects of phenibut under conditions of non-competitive aggression induced by fear of inescapable painful exposure or under conditions of competitive aggression reflecting the ability of animals to reveal adaptive social communicative skills in aversive situation.