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Approach direction prior to landing explains patterns of colour learning in bees

Gaze direction is closely coupled with body movement in insects and other animals. If movement patterns interfere with the acquisition of visual information, insects can actively adjust them to seek relevant cues. Alternatively, where multiple visual cues are available, an insects movements may influence how it perceives a scene. We show that the way a foraging bumblebee approaches a floral pattern could determine what it learns about the pattern. When trained to vertical bicoloured patterns, bumblebees consistently approached from below centre in order to land in the centre of the target where the reward was located. In subsequent tests, the bees preferred the colour of the lower half of the pattern that they predominantly faced during the approach and landing sequence. A predicted change of learning outcomes occurred when the contrast line was moved up or down off-centre: learned preferences again reflected relative frontal exposure to each colour during the approach, independent of the overall ratio of colours. This mechanism may underpin learning strategies in both simple and complex visual discriminations, highlighting that morphology and action patterns determines how animals solve sensory learning tasks. The deterministic effect of movement on visual learning may have substantially influenced the evolution of floral signals, particularly where plants depend on fine-scaled movements of pollinators on flowers.

animal behavior and cognition

An Ishihara-style test of animal colour vision

O_LIColour vision mediates ecologically relevant tasks for many animals, such as mate choice, foraging and predator avoidance. However, our understanding of animal colour perception is largely derived from human psychophysics, even though animal visual systems differ from our own. Behavioural tests of non-human animals are required to understand how colour signals are perceived by them.\nC_LIO_LIHere we introduce a novel test of colour vision in animals inspired by the Ishihara colour charts, which are widely used to identify human colour deficiencies. These charts consist of dots that vary in colour, brightness and size, and are designed so that a numeral or letter is distinguishable from distractor dots for humans with normal colour vision. In our method, distractor dots have a fixed chromaticity (hue and saturation) but vary in luminance. Animals can be trained to find single target dots that differ from distractor dots in chromaticity. We provide Matlab code for creating these stimuli, which can be modified for use with different animals.\nC_LIO_LIWe demonstrate the success of this method with triggerfish, Rhinecanthus aculeatus, and highlight behavioural parameters that can be measured, including success of finding the target dot, time to detect dot and error rate. Triggerfish quickly learnt to select target dots that differed from distractors dots regardless of the particular hue or saturation, and proved to use acute colour vision. We measured discrimination thresholds by testing the detection of target colours that were of increasing colour distances ({Delta}S) from distractor dots in different directions of colour space. At least for some colours, thresholds indicated better discrimination than expected from the Receptor Noise Limited (RNL) model assuming 5% Weber fraction for the long-wavelength cone.\nC_LIO_LIThis methodology seems to be highly effective because it resembles natural foraging behavior for the triggerfish and may well be adaptable to a range of other animals, including mammals, birds, bees and freshwater fish. Other questions may be addressed using this methodology, including luminance thresholds, sensory bias, effects of sensory noise in detection tasks, colour categorization and saliency.\nC_LI

animal behavior and cognition

Quantitative analysis reveals the basic behavioural repertoire of the urochordate Ciona intestinalis.

Quantitative analysis of animal behaviour in model organisms is becoming an increasingly essential approach for tackling the great challenge of understanding how activity in the brain gives rise to behaviour. In addition, behavioural analysis can provide insight on the molecular basis of nervous system development and function as demonstrated by genetic screens focused on behavioural phenotyping in some genetically tractable model organisms. The progress in building low-cost automated tracking setups, together with advances in computer vision machine learning have expanded the repertoire of organisms which are amenable to quantitative behavioural analysis. Here we used automated image-based tracking to extract behavioural features from an organism of great importance in understanding the evolution of chordates, the free swimming larval form of the tunicate Ciona intestinalis which has a compact and fully mapped nervous system composed of only 231 neurons. We analysed hundreds of videos of larvae and we extracted basic geometric and physical descriptors of larval behaviour. Most importantly, we used machine learning methods to create an objective ontology of behaviours for C. intestinalis larvae. We identified eleven behavioural modes using agglomerative clustering. This approach enabled us to produce a quantitative description of the basic larval behavioural repertoire. Furthermore, we tested the robustness of this repertoire by comparing different rearing conditions and ages. Using our pipeline for quantitative behavioural analysis, we successfully reproduced the known photoresponsive behaviour and the first demonstration to our knowledge that C. intestinalis larvae exhibit sensory arousal and thigmotaxis, both of which can be modulated by the anxiotropic drug modafinil. Remarkably, by comparing the behaviour between animals assayed individually or in small groups, we found that crowd size influences larval behaviour. This study shows that C. intestinalis larval behaviour can be broken down to a set of stereotyped behaviours that are used to different extents in a context-dependent manner. Furthermore, it raises exciting possibilities such as mapping behaviour to specific neurons of this compact chordate nervous system and it paves the way for comparative quantitative behavioural studies as a means to reconstruct the evolution of behaviour, especially in the chordate lineage.

animal behavior and cognition

Brood-holding causes workers to pay attention to the queen in the carpenter ant Camponotus japonicus

[Abstract]Brood accumulation, a fundamental behavior of offspring care in the carpenter ant Camponotus japonicus, is driven by alternation of holding run and empty-handed run behaviors. In the holding run, a worker holds a brood with her mandibles and carries it to the queen (holding run). After releasing it beside the queen, she hurries back to another brood (empty-handed run). To address the motivation for the brood-accumulation task, in this study, I observed these behaviors under experimental conditions. When workers performed the task in a situation that involved selection between their own and unfamiliar queens, they ran in significantly more restrictive ways during the holding run than during the empty-handed run. Hence, holding represents a different motivational state than empty-handed. In a second experiment, the workers were suddenly presented with an unfamiliar floor during the task. Regardless of whether they were holding or empty-handed, their running traces on the familiar floor were simple, whereas on the unfamiliar floor they were more complex. These results show that holding workers would pay attention to the queen, exploiting cues on the floor to restrict their responses to the queen.

animal behavior and cognition

Manipulation of the social and spatial organization of the vector of Chagas disease, Triatoma infestans, by the parasite Trypanosoma cruzi

Insects of Triatominae subfamily are vectors of the parasite Trypanosoma cruzi, the etiological agent of Chagas disease affecting millions of people in Latin America. Some of these vector species, like Triatoma infestans, live in the human neighborhood, aggregating in walls or roof cracks during the day and going out to feed on animal or human blood at night. Except for their feeding specialization, these insects share this cycle of activities with many gregarious arthropod species. The understanding of how sex and T. cruzi infection affect their aggregation and geotaxis behavior is essential for understanding the spatial organization of the insects and the parasite dispersion. Experiments with non-infected and infected adults of T. infestans show that the insects presented a high negative geotaxis and aggregative behavior. Males had a higher negative geotaxis and a higher aggregation level than females. The aggregation level and the negative geotaxis were stronger in infected insects than in non-infected ones, the difference between sexes being maintained. The importance of these results is discussed in term of parasitic manipulation, dispersion of the vector and strategy of its monitoring.

animal behavior and cognition

Familiarity increases aggressiveness among clonal fish.

Understanding how animal groups form and function is a major goal in behavioural ecology. Both genetic relatedness and familiarity among group mates have been shown to be key mediators of group composition. However, disentangling the two in most species is challenging as the most familiar individuals are often the most related, and vice versa. In order to gain a complete understanding of how individual interactions shape group behaviour it is crucial to understand the role each of this social relationship factors plays individually. To this end, we manipulated the level of familiarity among groups of the naturally clonal, and genetically identical fish, the Amazon molly (Poecilia formosa) and monitored group behaviour in an open-field and when given the opportunity to forage. Contrary to our predictions, fish that were the most familiar with each other showed the highest levels of aggression. Additionally, fish that were less familiar with each other exhibited the highest group cohesion and took the longest to begin feeding, compared to the more familiar fish. These results suggest that familiarity may socially buffer individuals from the perception of risk in novel environments, such as is common in most behavioural tests designed to test group behaviour. Increases in aggression that are associated with increasing familiarity as shown here might be a mechanism by which fish maintain a fission-fusion society with important consequences for the patterns of associations in group living animals.

animal behavior and cognition

Domain-general enhancements of metacognitive ability through adaptive training

The metacognitive ability to introspect about self-performance varies substantially across individuals. Given that effective monitoring of performance is deemed important for effective behavioural control, intervening to improve metacognition may have widespread benefits, for example in educational and clinical settings. However, it is unknown whether and how metacognition can be systematically improved through training independently of task performance, or whether metacognitive improvements generalize across different task domains. Across 8 sessions, here we provided feedback to two groups of participants in a perceptual discrimination task: an experimental group (N = 29) received feedback on their metacognitive judgments, while an active control group (N = 32) received feedback on their decision performance only. Relative to the control group, adaptive training led to increases in metacognitive calibration (as assessed by Brier scores) which generalized both to untrained stimuli and an untrained task (recognition memory). Leveraging signal detection modeling we found that metacognitive improvements were driven both by changes in metacognitive efficiency (meta-d/d) and confidence level, and that later increases in metacognitive efficiency were positively mediated by earlier shifts in confidence. Our results reveal a striking malleability of introspection and indicate the potential for a domain-general enhancement of metacognitive abilities.

animal behavior and cognition

Homing and egg discrimination in the Western Slimy Salamander, Plethodon albagula (Caudata: Plethodontidae)

In some species of vertebrates egg brooding is a costly form of parental care. Therefore, misdirection of parental care can significantly lower a females fitness. Because of the maternal investment and increased survivorship to offspring from egg guarding, a brooding female should home to her nest site after being displaced a short distance and discriminate between her own eggs and eggs from other females. In this study, we experimentally tested, in the field, alternative hypotheses concerning homing ability and egg discrimination in a population of nesting western slimy salamanders (Plethodon albagula). Fourteen brooding females were displaced 1 m to the left or right of their nest sites (determined randomly) for the homing experiment. Furthermore, brooding females (n = 13) were presented with their own clutches, which were displaced 50 cm to the left or right (determined randomly), and unfamiliar egg clutches at their original nest sites. The females were released at an equal distance from both egg clutches. After 24 hours, 12 displaced females (86%) had returned to their own nest sites and were brooding their egg clutches. Also, after 24 hours, nine test females had returned to their own nest sites and were brooding the unfamiliar egg clutches. No control or test females were present at the other new nest site locations. Therefore, we suggest that brooding female P. albagula do home to their nest sites and exhibit indirect egg discrimination.

animal behavior and cognition

Effects of the anesthetic MS-222 on silver pomfret (Pampus argenteus) juveniles under aquaculture treatment stresses

The silver pomfret (Pampus argenteus) is a major economically important marine fish in China. However, P. argenteus is sensitive to many stress factors and susceptible to injury. This problem could be resolved using anesthesia. We determined the lowest effective dose (LED) of tricaine methanesulfonate (MS-222) and assessed the longest safe deep anesthesia time and effect after aquaculture treatment stresses. P. argenteus juveniles were exposed to six concentrations of MS-222 (10, 25, 50, 75, 100, and 125 mg L-1); LED was established at 75 mg L-1. The juveniles were exposed to different deep anesthesia times (4, 7, 10, 12, and 15 min) at 75 mg L-1; the longest safe deep anesthesia time under LED was 10 min. Finally, the juveniles were randomly divided into four groups: control group (CG), draining group (DG, drain), anesthetic group (AG, drain + MS-222 + aquaculture treatment); and non-anesthetic group (NAG, drain + aquaculture treatment). Plasma cortisol levels in the NAG, AG, DG, and CG groups were 38.739 {+/-} 1.065 (highest), 25.083 {+/-} 0.587, 28.644 {+/-} 0.612, and 22.620 {+/-} 0.836 ng mL-1 (lowest). The AG group showed significant differences in superoxide dismutase, catalase, and malondialdehyde activities, except for glutathione. HSP70, HSP90, GR1, and GR2 mRNA levels in the NAG group increased sharply in response to stressors. GR1 and GR2 mRNA levels in the AG group also increased significantly, whereas HSP70 and HSP90 mRNA levels showed no significant differences. Thus, MS-222 can reduce oxidative damage, stress reaction, and resistance to aquaculture treatment stresses in P. argenteus.

animal behavior and cognition

Powerful and interpretable behavioural features for quantitative phenotyping of C. elegans

Behaviour is a sensitive and integrative readout of nervous system function and therefore an attractive measure for assessing the effects of mutation or drug treatment on animals. Video data provides a rich but high-dimensional representation of behaviour and so the first step of analysis is often some form of tracking and feature extraction to reduce dimensionality while maintaining relevant information. Modern machine learning methods are powerful but notoriously difficult to interpret, while handcrafted features are interpretable but do not always perform as well. Here we report a new set of handcrafted features to compactly quantify C. elegans behaviour. The features are designed to be interpretable but to capture as much of the phenotypic differences between worms as possible. We show that the full feature set is more powerful than a previously defined feature set in classifying mutant strains. We then use a combination of automated and manual feature selection to define a core set of interpretable features that still provides sufficient power to detect behavioural differences between mutant strains and the wild type. Finally, we apply the new features to detect time-resolved behavioural differences in a series of optogenetic experiments targeting different neural subsets.

animal behavior and cognition

Using Drosophila behavioral assays to characterize terebrid venom-peptide bioactivity

The number of newly discovered peptides from the transcriptomes and proteomes of animal venom arsenals is rapidly increasing, resulting in an abundance of uncharacterized peptides. There is a pressing need for a systematic, cost effective, and scalable approach to identify physiological effects of venom peptides. To address this discovery-to-function gap, we developed a sequence driven:activity-based hybrid approach for screening venom peptides that is amenable to large-venom peptide libraries with minimal amounts of peptide. Using this approach, we characterized the physiological and behavioral phenotypes of two peptides from the venom of predatory terebrid marine snails, teretoxins Tv1 from Terebra variegata and Tsu1.1 from Terebra subulata. Our results indicate that Tv1 and Tsu1.1 have distinct bioactivity. Tv1 (100 M) had an antinociceptive effect in adult Drosophila using a thermal nociception assay to measure heat avoidance. Alternatively, Tsu1.1 (100 M) increased food intake. These findings describe the first functional bioactivity of terebrid venom peptides in relation to pain and diet and indicate that Tv1 and Tsu1.1 may, respectively, act as antinociceptive and orexigenic agents. Tv1 and Tsu1.1 are distinct from previously identified venom peptides, expanding the toolkit of peptides that can potentially be used to investigate the physiological mechanisms of pain and diet.

animal behavior and cognition

Trajectory changes are susceptible to change blindness manipulations

People routinely fail to notice that things have changed in a visual scene if they do not perceive the changes in the process of occurring, a phenomenon known as change blindness (1,2). The majority of lab-based change blindness studies use static stimuli and require participants to identify simple changes such as alterations in stimulus orientation or scene composition. This study uses a flicker paradigm adapted for dynamic stimuli which allowed for both simple orientation changes and more complex trajectory changes. Participants were required to identify a moving rectangle which underwent one of these changes against a background of moving rectangles which did not. The results demonstrated that participants ability to correctly identify the target deteriorated with the presence of a visual mask and a larger number of distractor objects, consistent with findings in previous change blindness work.\n\nThe study provides evidence that the flicker paradigm can be used to induce change blindness with dynamic stimuli, and that changes to predictable trajectories are detected or missed in the similar way as orientation changes.

animal behavior and cognition

Demography and behavior of polygyne nests of the supercolonial Cataglyphis niger: Does kinship matter?

The basic ant colony is presumed to have evolved through kin selection. However, ants show a remarkable diversity in their social organization, from a monogynous-monandrous queen to the more derived states of polygyny with polyandrous queens. The existence of polygyny is an evolutionary enigma, since kin selection theory predicts that while queens should strive for reproductive monopoly, workers are predicted to favor their own matriline in rearing gynes. Using a barcoding system that enables tracking of individual interactions, along with polymorphic DNA microsatellite markers that indicate the matriline and patriline of all individuals, we demonstrate the complex social interactions in polygyne nests of Cataglyphis niger. C. niger is not only polygyne but also constitutes a supercolony at the study site. Our pioneering findings that both queens and workers are not necessarily related to each other support the supercolony structure of the population. Also in line with supercoloniality, we demonstrate that the workers contribute equally to the nest production and rearing of the queens. Unlike invasive supercolonial species, C. niger is native to Israel, raising questions about the driving forces, apart from kin selection, that stabilize this society.

animal behavior and cognition

Density-dependent changes in neophobia and stress-coping styles in the worlds oldest farmed fish

Farmed fish are typically reared at densities much higher than those observed in the wild, but to what extent crowding results in abnormal behaviours that can impact welfare and stress coping styles is subject to debate. Neophobia (i.e. fear of the new) is thought to be adaptive under natural conditions by limiting risks, but it is potentially maladapted in captivity, where there are no predators or novel foods. We reared juvenile Nile tilapia (Oreochromis niloticus) for six weeks at either high (50g/L) or low density (14g/L), assessed the extent of skin and eye darkening (two proxies of chronic stress), and exposed them to a novel object in an open-test arena, with and without cover, to assess the effects of density on neophobia and stress coping styles. Fish reared at high density were darker, more neophobic, less aggressive, less mobile and less likely to take risks than those reared at low density, and these effects were exacerbated when no cover was available. Thus, the reactive coping style shown by fish at high density was very different from the proactive coping style shown by fish at low density. Our findings provide novel insights into the plasticity of fish behaviour and the effects of aquaculture intensification on one of the worlds oldest farmed and most invasive fish, and highlight the importance of considering context. Crowding could have a positive effect on the welfare of tilapia by reducing aggressive behaviour, but it can also make fish chronically stressed and more fearful, which could make them less invasive.

animal behavior and cognition

Identity domains in complex behavior: Toward a biology of personality

Personality traits offer considerable insight into the biological basis of individual differences. However, existing approaches toward understanding personality across species rely on subjective criteria and limited sets of behavioral readouts, resulting in noisy and often inconsistent outcomes. Here, we introduce a mathematical framework for studying individual differences along dimensions with maximum consistency and discriminative power. We validate this framework in mice, using data from a system for high-throughput longitudinal monitoring of group-housed mice that yields a variety of readouts from all across an individuals behavioral repertoire. We describe a set of stable traits that capture variability in behavior and gene expression in the brain, allowing for better informed mechanistic investigations into the biology of individual differences.

animal behavior and cognition

Rapid environmental change in games: complications and curiosities

Human-induced rapid environmental change (HIREC) has recently led to alterations in the fitness and behavior of many organisms. Game theory is an important tool of behavioral ecology for analyzing evolutionary situations involving multiple individuals. However, game theory bypasses the details by which behavioral phenotypes are determined, taking the functional perspective straight from expected payoffs to predicted frequencies of behaviors. In contrast with optimization approaches, we identify that to use existing game theoretic models to predict HIREC effects, additional mechanistic details (or assumptions) will often be required. We illustrate this in relation to the hawk-dove game by showing that three different mechanisms, each of which support the same ESS prior to HIREC (fixed polymorphism, probabilistic choice, or cue dependency), can have a substantial effect on behavior (and success) following HIREC. Surprisingly, an increase in the value of resources can lead to a reduction in payoffs (and vice versa), both in the immediate- and long-term following HIREC. An increase in expected costs also increases expected payoffs. Along with these counter-intuitive findings, this work shows that simply understanding the behavioral payoffs of existing games is insufficient to make predictions about the effects of HIREC.\n\nIts the little details that are vital. Little things make big things happen.\n\nJohn Wooden

animal behavior and cognition

The geometry of dependence: solitary bee larvae prioritize carbohydrate over protein in parentally provided pollen

O_LIMost organisms must regulate their nutritional intake in an environment full of complex food choices. While this process is well understood for self-sufficient organisms, dependent offspring, such as bee larvae, in practice have limited food choices because food is provided by parents. Nutrient balancing may therefore be achieved by offspring, by parents on offsprings behalf, or by both, whether cooperatively or in conflict. C_LIO_LIWe used the Geometric Framework to investigate the capacity of dependent larval mason bees (Osmia bicornis) to regulate their intake of protein and carbohydrate. Female Osmia seal eggs individually inside cells they have provisioned with pollen, and have no contact with developing offspring, allowing offspring choices to be studied in isolation. Herbivorous insect larvae are typically expected to balance protein and carbohydrate to maximise growth and reproduction. C_LIO_LIContrary to prediction, carbohydrate and not protein mediated both growth and survival to pupation. Accordingly, larvae prioritised maintaining a constant intake of carbohydrate and self-selected a relatively carbohydrate biased diet compared to other hymenopterans, while tolerating wide excesses and deficiencies of protein, rendering them potentially vulnerable to dietary change or manipulation. Reasons for prioritising carbohydrate may include (1) the relative abundance of protein in their normal pollen diet, (2) the relative paucity of nectar in parental provisions making carbohydrate a scarce resource, or (3) the requirement for diapause for all O. bicornis larvae. Larvae were intolerant of moderate dietary dilution, likely reflecting an evolutionary history of nutrient-dense food. C_LIO_LIOur results demonstrate that dependent offspring can remain active participants in balancing their own nutrients even when sedentary, and, moreover, even in mass provisioning systems where parents and offspring have no physical contact. Research should now focus on whether and how evolutionary interests of parent and dependent offspring coincide or conflict with respect to food composition, and the implications for species resilience to changing environments. C_LI

animal behavior and cognition

Markerless tracking suggests a tactile sensing role for forelegs of Dolomedes spiders during locomotion

Summary statementWe developed a machine vision technique for markerless tracking of locomotion in the spider Dolomedes aquaticus. Gait analysis suggests that each pair of legs plays a specific role in locomotion.\n\nAbstractBecause of their rigid exoskeleton with relatively simple joint mechanics, arthropods can provide useful models for studying the sensory-neural and mechanical design principles of agile animal locomotion. Gait analysis usually requires attaching markers or manually identifying reference points in video frames, which can be time consuming and inaccurate, especially with small animals. Here we describe a markerless motion capture technique and its application to gait analysis in the New Zealand semi-aquatic hunting spider, Dolomedes aquaticus. Our machine vision approach uses a model of the spiders skeleton to infer the location of the centre of mass and the configuration of the skeleton in successive video frames. We found that stride length and frequency are correlated with running speed. Inter-limb coordination during the gait cycle suggests that different legs have specialized roles in locomotion. Phase relationships among the six hindmost legs exhibit an alternating tripod gait, as in hexapod insects. The middle two leg pairs appear to be primarily responsible for generating thrust, while the hind legs contribute more to stability. The front legs are not phase-coupled to the other legs and appear to be used as tactile probes during locomotion. Our machine vision approach has the potential to automate arthropod gait analysis, making it faster and easier. Our results indicate how specialization of limb function may contribute to locomotor efficiency and agility of a specialized hunting spider, and how arthropod design principles may contribute to developing efficient, agile legged robots.

animal behavior and cognition