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Exaggerated estrous swellings and male mate choice in primates: testing the reliable indicator hypothesis in the Amboseli baboons.

INTRODUCTION INTRODUCTION METHODS RESULTS DISCUSSION LITERATURE CITED The evolution of male mate choice in sex-role reversed species can easily be understood according to the general principles of sexual selection. That is, when females are mate-limited they are expected to compete for access to males and those males, in turn, are expected to be choosy. This phenomenon is well described in some sex-role reversed species of pipefish (Berglund et al. 1989; Vincent et al. 1992) and shorebirds (Szekely & Reynolds 1995). In contrast, when the sex roles are conventional, choosy males will be at a competitive disadvantage and, therefore, male mate choice should be selected against. Of course, exceptions to this prediction have been demonstrated, most notably in those cases where fe ...

Animal Behavior and Cognition

Ontogeny of aerial righting and wing flapping in juvenile birds

Mechanisms of aerial righting in juvenile Chukar Partridge (Alectoris chukar) were studied from hatching through 14 days-post-hatching (dph). Asymmetric movements of the wings were used from 1-8 dph to effect progressively more successful righting behaviour via body roll. Following 8 dph, wing motions transitioned to bilaterally symmetric flapping that yielded aerial righting via nose-down pitch, along with substantial increases in vertical force production during descent. Ontogenetically, the use of such wing motions to effect aerial righting precedes both symmetric flapping and a previously documented behaviour in chukar (i.e., wing-assisted incline running) hypothesized to be relevant to incipient flight evolution in birds. These findings highlight the importance of asymmetric wing activation and controlled aerial manoeuvres during bird development, and are potentially relevant to understanding the origins of avian flight.

Animal Behavior and Cognition

A quantitative analysis of objective feather colour assessment: measurements in the lab are more reliable than in the field

The evolution of animal colouration is importantly driven by sexual selection operating on traits used to transmit information to rivals and potential mates, which therefore, have major impacts on fitness. Reflectance spectrometry has become a standard colour-measuring tool, especially after the discovery of tetrachromacy in birds and their ability to detect UV. Birds plumage patterns may be invisible to humans, necessitating a reliable and objective way of assessing colouration not dependent on human vision. Plumage colouration measurements can be taken directly on live birds in the field or in the lab (e.g. on collected feathers). Therefore, it is essential to determine which sampling method yields more repeatable and reliable measures, and which of the available quantitative approaches best assess the repeatability of these measures. Using a spectrophotometer, we measured melanin-based colouration in barn swallows (Hirundo rustica) plumage. We assessed the repeatability of measures obtained with both traditional sampling methods separately to quantitatively determine their reliability. We used the ANOVA-based method for calculating the repeatability of measurements from two years separately, and the GLMM-based method to calculate overall adjusted repeatabilities for both years. We repeated the assessment for the whole reflectance spectrum range and only the human-visible part, to assess the influence of the UV component on the reliabilities of sampling methodologies. Our results reveal very high repeatability for lab measurements and a lower, still moderate to high repeatability, for field measurements. Both increased when limited to only the human-visible part, for all plumage patches except the throat, where we observed the opposite trend. Repeatability between sampling methods was quite low including the whole spectrum, but moderate including only the human-visible part. Our results suggest higher reliability for measurements in the lab and higher power and accuracy of the GLMM-based method. They also suggest UV reflectance differences amongst different plumage patches.

Animal Behavior and Cognition

Amino acid and carbohydrate tradeoffs by honey bee nectar foragers and their implications for plant-pollinator interactions

Honey bees are important pollinators, requiring floral pollen and nectar for nutrition. Nectar is rich in sugars, but contains additional nutrients, including amino acids (AAs). We tested the preferences of free-flying foragers between 20 AAs at 0.1% w/w in sucrose solutions in an artificial meadow. We found consistent preferences amongst AAs, with essential AAs preferred over nonessential AAs. The preference of foragers correlated negatively with AA induced deviations in pH values, as compared to the control. Next, we quantified tradeoffs between attractive and deterrent AAs at the expense of carbohydrates in nectar. Bees were attracted by phenylalanine, willing to give up 84 units sucrose for 1 unit AA. They were deterred by glycine, and adding 100 or more units of sucrose could resolve to offset 1 unit AA. In addition, we tested physiological effects of AA nutrition on forager homing performance. In a no-choice context, caged bees showed indifference to 0.1% proline, leucine, glycine or phenylanaline in sucrose solutions. Furthermore, flight tests gave no indication that AA nutrition affected flight capacity directly. In contrast, low carbohydrate nutrition reduced the performance of bees, with important methodological implications for homing studies that evaluate the effect of substances that may affect imbibition of sugar solution. In conclusion, low AA concentrations in nectar relative to pollen suggest a limited role in bee nutrition. Most of the 20 AAs evoked a neutral to a mild deterrent response in bees, thus it seems unlikely that bees respond to AAs in nectar as a cue to assess nutritional quality. Nonetheless, free choice behavior of foraging bees is influenced, for instance by phenylalanine and glycine. Thus, AAs in nectar may affect plant-pollinator interactions and thereby exhibit a selective pressure on the flora in the honey bee habitat.\n\nO_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=83 SRC=\"FIGDIR/small/008516_ufig1.gif\" ALT=\"Figure 1\">\nView larger version (31K):\norg.highwire.dtl.DTLVardef@8fde04org.highwire.dtl.DTLVardef@138fdd3org.highwire.dtl.DTLVardef@a05775org.highwire.dtl.DTLVardef@cde793_HPS_FORMAT_FIGEXP M_FIG C_FIG HIGHLIGHTS- Amino acids in artificial nectar elicit preferences from honey bee foragers\n- Amino acid identity, pH, and essentiality explain preferences of bees\n- A honey bee forager is willing to pay a premium of carbohydrates for amino acids\n- Carbohydrate nutritional state affects flight performance of foraging bees

Animal Behavior and Cognition

SPOILS OF WAR AND PEACE: ENEMY ADOPTION AND QUEEN-RIGHT COLONY FUSION FOLLOW COSTLY INTRASPECIFIC CONFLICT IN ACACIA ANTS

Intraspecific conflict over vital limited resources can lead to costly fights. How winners compensate for costs and minimize the threat of Pyrrhic victory is not well known. This study tracked the outcomes of experimentally induced field conflicts between highly territorial Acacia ant Crematogaster mimosae colonies using molecular genetics, and discovered that fatal fights significantly decrease within-colony worker relatedness. We find that reduced relatedness can be explained by colonies increasing worker number via 1) non-kin enemy adoption or 2) queen-right colony fusion. We hypothesize that incorporating non-kin enemies can speed recovery from conflict when resource defense is paramount. In the case of queen-right colony fusion, territorial defense benefits could outweigh fitness costs. We provide evidence that winners of colony fights have reduced worker forces to defend larger territories. Field assays indicate that post-fight colonies are more vulnerable to heavy browsing of host trees by mega-herbivores and takeover by competitors following conflict. We discuss the implications of our findings for ant colony cohesion and recognition systems.

Animal Behavior and Cognition

How predator hunting-modes affect prey behaviour: Capture deterrence in Drosophila melanogaster

Hunting mode, the distinct set of behavioural strategies that a predator employs while hunting, can be an important determinant of the prey organisms behavioural response. However, few studies have considered how a predators hunting mode influences anti-predatory behaviours of a prey species. Here we document the influence of active hunters (zebra jumping spiders, Salticus scenicus) and ambush predators (Chinese praying mantids, Tenodera aridifolia sinensis) on the capture deterrence anti-predatory behavioural repertoire of the model organism, Drosophila melanogaster. We hypothesized that D. melanogaster would reduce overall locomotory activity in the presence of ambush predators, and increase activity with active hunters. First we observed and described the behavioural repertoire of D. melanogaster in the presence of the predators. We documented three previously undescribed behaviours-abdominal lifting, stopping and retreat-which were performed at higher frequency by D. melanogaster in the presence of predators, and may aid in capture deterrence. Consistent with our predictions, we observed an increase in the overall activity of D. melanogaster in the presence of jumping spiders (active hunter). However, counter to our prediction, mantids (ambush hunter) had only a modest influence on activity. We also observed considerable intra and inter-individual variation in response to both predator types. Given these new insights into Drosophila behaviour, and with the genetic tools available, dissecting the molecular mechanisms of anti-predator behaviours may now be feasible in this system.

Animal Behavior and Cognition

Social communication in mice – Are there optimal cage conditions?

Social communication is heavily affected in patients with neuropsychiatric disorders. Accordingly, mouse models designed to study the mechanisms leading to these disorders are tested for this phenotypic trait. Test conditions vary between different models, and the effect of these test conditions on the quantity and quality of social interactions and ultrasonic communication is unknown. The present study examines to which extent the habituation time to the test cage as well as the shape / size of the cage influence social communication in freely interacting mice. We tested 8 pairs of male mice in free dyadic social interactions, with two habituation times (20 min and 30 min) and three cage formats (rectangle, round, square). We tested the effect of these conditions on the different types of social contacts, approach-escape sequences, follow behavior, and the time each animal spent in the vision field of the other one, as well as on the emission of ultrasonic vocalizations and their contexts of emission. We provide for the first time an integrated analysis of the social interaction behavior and ultrasonic vocalizations. Surprisingly, we did not highlight any significant effect of habituation time and cage shape / size on the behavioral events examined. There was only a slight increase of social interactions with the longer habituation time in the round cage. Remarkably, we also showed that vocalizations were emitted during specific behavioral sequences especially during close contact or approach behaviors. The present study provides a protocol reliably eliciting social contacts and ultrasonic vocalizations in male mice. This protocol is therefore well adapted for standardized investigation of social interactions in mouse models of neuropsychiatric disorders.

Animal Behavior and Cognition

Division of Labor: A Democratic Approach to Understanding Manual Asymmetries in Non-Human Primates

A consequence of the gold rush like hunch for human-like handedness in non-human primates has been that researchers have been continually analyzing observations at the level of the population, ignoring the analysis at the level of an individual and, consequently, have potentially missed revelations on the forms and functions of manual asymmetries. Recently, consecutive studies on manual asymmetries in bonnet macaques, Macaca radiata [Mangalam et al., 2014a; Mangalam et al., 2014b] revealed both the functional and the adaptive significance of manual asymmetries respectively, and pointed towards the division of labor as being the general principle underlying the observed hand-usage patterns. We review the studies on manual asymmetries in capuchin monkeys, Cebus spp. and argue that the observed hand-usage patterns might reflect specialization of the two hands for accomplishing tasks that require different dexterity types (i.e., maneuvering in three dimensional space or physical strength). To this end, we do a step-by-step analysis of the various tasks used in the studies on manual asymmetries in capuchin monkeys, wherein we: (a) analyze the different manual tasks that have been used to study manual asymmetries in non-human primates on the basis of the attributes such as the number of hands required to solve a given task (i.e., unimanual, pseudo unimanual, or bimanual) and the spatiotemporal progression of manual actions (i.e., sequential or concurrent). (b) Determine the forms and functions of manual asymmetries that these tasks can potentially elicit within the broader scope of the behavioral repertoire of an individual, a population, or a species. (c) Qualify the scope of the inter-individual, -population, or -species comparisons. We then describe the division of labor as a general principle underlying manual asymmetries in non-human primates, and propose experimental designs that would elaborate the forms and functions of manual asymmetries in non-human primates, and the associated adaptive value.

Animal Behavior and Cognition

Retrieval-extinction within the memory reconsolidation window does not influence appetitive choice

Influencing choice behavior is key to achieving behavioral change. Traditional means to influence choice behavior rely on effortful self control, which is known to be fragile under several circumstances, rendering these methods ineffectual in maintaining any change in behavior over time. Behavioral maintenance efforts are likely more effective over the long term if they target more automatic processes such as attention or memory. Memories are not set in stone and are vulnerable to change and updating under certain circumstances when retrieved. It is possible to target specific memories for updating. In two studies, we sought to update the memory for an appetitive choice by way of reversal learning following retrieval of the targeted choice behavior. We found that targeting memories of a choice behavior for updating shortly after a reminder did not significantly attenuate the renewal of the targeted choice under extinction conditions. Possible explanations and suggested future directions are discussed.

Animal Behavior and Cognition

Large-scale assessment of olfactory preferences and learning in Drosophila melanogaster: behavioral and genetic measures

In the Evolve and Resequence method (E&R), experimental evolution and genomics are combined to investigate evolutionary dynamics and the genotype-phenotype link. This approach requires many replicates with large population sizes, which imposes severe restrictions on the analysis of behavioral phenotypes. Aiming to use E&R for investigating the evolution of behavior in Drosophila, we have developed a simple and effective method to assess spontaneous olfactory preferences and learning in large samples of fruit flies using a T-maze. We tested this procedure on (a) a large wild-caught population and (b) 11 isofemale lines of Drosophila melanogaster. Compared to previous methods, this procedure reduces the environmental noise and allows for the analysis of large population samples. Consistent with previous results, we show that flies have a spontaneous preference for orange vs. apple odor. With our procedure wild-derived flies exhibit olfactory learning in the absence of previous laboratory selection. Furthermore, we find genetic differences in the olfactory learning with relatively high heritability. We propose this large-scale method as an effective tool for E&R and genome-wide association studies on olfactory preferences and learning.

Animal Behavior and Cognition

Changes in postural syntax characterize sensory modulation and natural variation of C. elegans locomotion

Locomotion is driven by shape changes coordinated by the nervous system through time; thus, enumerating an animals complete repertoire of shape transitions would provide a basis for a comprehensive understanding of locomotor behaviour. Here we introduce a discrete representation of behaviour in the nematode C. elegans. At each point in time, the worms posture is approximated by its closest matching template from a set of 90 postures and locomotion is represented as sequences of postures. The frequency distribution of postural sequences is heavy-tailed with a core of frequent behaviours and a much larger set of rarely used behaviours. Responses to optogenetic and environmental stimuli can be quantified as changes in postural syntax: worms show different preferences for different sequences of postures drawn from the same set of templates. A discrete representation of behaviour will enable the use of methods developed for other kinds of discrete data in bioinformatics and language processing to be harnessed for the study of behaviour.\n\nAuthor SummaryTechnology for recording neural activity is advancing rapidly and whole-brain imaging with single neuron resolution has already been demonstrated for smaller animals. To interpret such complex neural recordings, we need comprehensive characterizations of behaviour, which is the principal output of the brain. Animal tracking can increasingly be performed automatically but an outstanding challenge is finding ways to represent these behavioural data. We have focused on the movement of the nematode worm C. elegans to develop a quantitative representation of behaviour as a series of distinct postures. Each posture is analogous to a word in a language and so we can directly count the number of phrases that makes up the C. elegans behavioural repertoire. C. elegans has a very small nervous system but we find that its behavioural repertoire is still complex. As with human languages, there is a large number of possible phrases, but most are rarely used. When comparing different populations of worms or worms in different environments, we find that the difference between their behaviour is due to a subset of their entire repertoire. In the language analogy, these would correspond to idiomatic phrases that distinguish groups of speakers. A quantitative understanding of the nature of behavioural variation will inform research on the function and evolution of neural circuits.

Animal Behavior and Cognition

Intensity matching in cuttlefish

For efficient background matching it is essential that animals closely match a set of salient visual statistics of their visual surroundings. The mean intensity of a background is a key statistic, because it can be estimated across a large range of viewing distances by a simple computation. We investigated how the dynamic neuromuscular camouflage system of the cuttlefish Sepia offcinalis responds to changes in the mean background intensity of uniform backgrounds. We find that cuttlefish adapt their body intensity in response to variations in the mean background intensity, yet show biases in their body intensity beyond what can be predicted from the limited dynamic range of their camouflage system. On sandy backgrounds of various reflectance values their uniform body patterns maintain a constant yellow hue. This color constancy may represent an example of a color prior in a colorblind animal because a yellow body color would be the optimal hue for camouflage on sands typically encountered in their natural environment. Cuttlefish adapt their appearance to the background via a dynamic process composed of a complex mixture of intensity transients spanning timescales from the subsecond to the minute range. In very young animals camouflaging on dark sands the masquerade strategy is preferred over background matching. Masquerade is implemented by combining partial background matching with frequent expression of disruptive components. We furthermore provide an objective definition of disruptive components using hierarchical clustering and automated image analysis thus highlighting the role of chromatophore activity correlations in structuring the motor output of S.officinalis.

Animal Behavior and Cognition

Social feedback and the emergence of rank in animal society

Dominance hierarchies are group-level properties that emerge from the aggressions of individuals. Although individuals can gain critical benefits from their position in a hierarchy, we do not understand how real-world hierarchies form, or what signals and decision-rules individuals use to construct and maintain them in the absence of simple cues. A study of aggression in two groups of captive monk parakeets (Myiopsitta monachus) found a transition to large-scale ordered aggression occurred in newly-formed groups after one week, with individuals thereafter preferring to direct aggression against those nearby in rank. We describe two mechanisms by which individuals may determine rank order: inference based on overall levels of aggression, or on subsets of the aggression network. Both pathways were predictive of individual decisions to aggress. Based on these results, we present a new theory, of a feedback loop between knowledge of rank and consequent behavior, that explains the transition to strategic aggression, and the formation and persistence of dominance hierarchies in groups capable of both social memory and social inference.

Animal Behavior and Cognition

BEEtag : a low-cost, image-based tracking system for the study of animal behavior and locomotion

A fundamental challenge common to studies of animal movement, behavior, and ecology is the collection of high-quality datasets on spatial positions of animals as they change through space and time. Recent innovations in tracking technology have allowed researchers to collect large and highly accurate datasets on animal spatiotemporal position while vastly decreasing the time and cost of collecting such data. One technique that is of particular relevance to the study of behavioral ecology involves tracking visual tags that can be uniquely identified in separate images or movie frames. These tags can be located within images that are visually complex, making them particularly well suited for longitudinal studies of animal behavior and movement in naturalistic environments. While several software packages have been developed that use computer vision to identify visual tags, these software packages are either (a) not optimized for identification of single tags, which is generally of the most interest for biologist, or (b) suffer from licensing issues, and therefore their use in the study of animal behavior has been limited. Here, we present BEEtag, an open-source, image-based tracking system in Matlab that allows for unique identification of individual animals or anatomical markers. The primary advantages of this system are that it (a) independently identifies animals or marked points in each frame of a video, limiting error propagation, (b) performs well in images with complex background, and (c) is low-cost. To validate the use of this tracking system in animal behavior, we mark and track individual bumblebees (Bombus impatiens) and recover individual patterns of space use and activity within the hive. Finally, we discuss the advantages and limitations of this software package and its application to the study of animal movement, behavior, and ecology.

Animal Behavior and Cognition

Concordance and incongruence in preclinical anxiety models: systematic review and meta-analyses

Rodent defense behavior assays have been widely used as preclinical models of anxiety to study possibly therapeutic anxiety-reducing interventions. However, some proposed anxiety-modulating factors--genes, drugs and stressors--have had discordant effects across different studies. To reconcile the effect sizes of purported anxiety factors, we conducted systematic review and meta-analyses of the literature on ten anxiety-linked interventions, as examined in the elevated plus maze, open field and light-dark box assays. Diazepam, 5-HT1A receptor gene knockout and overexpression, SERT gene knockout and overexpression, pain, restraint, social isolation, corticotropin-releasing hormone and Crhr1 were selected for review. Eight interventions had statistically significant effects on rodent anxiety, while Htr1a overexpression and Crh knockout did not. Evidence for publication bias was found in the diazepam, Htt knockout, and social isolation literatures. The Htr1a and Crhr1 results indicate a disconnect between preclinical science and clinical research. Furthermore, the meta-analytic data confirmed that genetic SERT anxiety effects were paradoxical in the context of the clinical use of SERT inhibitors to reduce anxiety.\n\nHighlightsO_LIMeta-analysis shows eight rodent anxiety factors have at least moderate effects.\nC_LIO_LIPublication bias affects four of the anxiety interventions.\nC_LIO_LIPreclinical rodent anxiety results appear disconnected from clinical efforts.\nC_LIO_LISerotonin transporter gene lesion effects are paradoxical with reuptake inhibitors clinical use.\nC_LI

Animal Behavior and Cognition

A decision underlies phototaxis in an insect.

Like a moth into the flame - Phototaxis is an iconic example for innate preferences. Such preferences likely reflect evolutionary adaptations to predictable situations and have traditionally been conceptualized as hard-wired stimulus-response links. Perhaps therefore, the century-old discovery of flexibility in Drosophila phototaxis has received little attention. Here we report that across several different behavioral tests, light/dark preference tested in walking is dependent on various aspects of flight. If we temporarily compromise flying ability, walking photopreference reverses concomitantly. Neuronal activity in circuits expressing dopamine and octopamine, respectively, plays a differential role in photopreference, suggesting a potential involvement of these biogenic amines in this case of behavioral flexibility. We conclude that flies monitor their ability to fly, and that flying ability exerts a fundamental effect on action selection in Drosophila. This work suggests that even behaviors which appear simple and hard-wired comprise a value-driven decision-making stage, negotiating the external situation with the animals internal state, before an action is selected.

Animal Behavior and Cognition

Pollen contaminated with field-relevant levels of cyhalothrin affects honey bee survival, nutritional physiology, and pollen consumption behavior

Honey bees are exposed to a variety of environmental stressors that impact their health, including nutritional stress, pathogens, and chemicals in the environment. In particular, there has been increasing evidence that sublethal exposure to pesticides can cause subtle, yet important effects on honey bee health and behavior. Here, we add to this body of knowledge by presenting data on bee-collected pollen containing sublethal levels of cyhalothrin, a pyrethroid insecticide, which, when fed to young honey bees, results in significant changes in lifespan, nutritional physiology, and behavior. For the first time, we show that when young, nest-aged bees are presented with pollen containing field-relevant levels of cyhalothrin, they reduce their consumption of contaminated pollen. This indicates that, at least for some chemicals, young bees are able to detect contamination in pollen and change their behavioral response, even if the contamination levels do not prevent foraging honey bees from collecting the contaminated pollen.

Animal Behavior and Cognition

Social inheritance can explain the structure of animal social networks

The social network structure of animal populations has major implications for survival, reproductive success, sexual selection, and pathogen transmission of individuals. But as of yet, no general theory of social network structure exists that can explain the diversity of social networks observed in nature, and serve as a null model for detecting species and population-specific factors. Here we propose a simple and generally applicable model of social network structure. We consider the emergence of network structure as a result of social inheritance, in which newborns are likely to bond with maternal contacts, and via forming bonds randomly. We compare model output to data from several species, showing that it can generate networks with properties such as those observed in real social systems. Our model demonstrates that important observed properties of social networks, including heritability of network position or assortative associations, can be understood as consequences of social inheritance.

Animal Behavior and Cognition