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bioRxiv2017

Taking a semi-local dynamic snapshot as a possibility for local homing in initially naive bumblebees

For central place foragers, such as bumblebees, it is essential to return reliably to their nest. Instead of just flying away to forage, bumblebees, leaving their inconspicuous nest hole for the first time, need to gather and learn sufficient information about the surroundings to allow them to return to the nest at the end of their trip. Therefore, we assume an intrinsic learning program that manifests itself in the flight structure immediately after leaving the nest for the first time.\n\nIn this study, we recorded and analysed the first outbound flight of individually marked naive bumblebees in an indoor environment. We found characteristic loop-like features in the flight pattern that appear to be necessary for the bees to acquire environmental information and might be relevant for finding the nest hole after a foraging trip.\n\nDespite common features in their spatio-temporal organisation, the first departure flights from the nest are characterised by a high level of variability in their loop-like flight structure across animals. Changes in turn direction of body orientation, for example, are distributed evenly across the entire area used for the flights without any systematic relation to the nest location. By considering the common flight motifs as well as this variability, we came to the hypothesis, that a kind of dynamic snapshot is taken during the early phase of departure flights in the close vicinity of the nest location. The quality of this snapshot is hypothesised to be tested during the later phases of the departure flights concerning its usefulness for local homing.

animal behavior and cognition↗

bioRxiv2017

Development of honeybee waggle dance and its differences between recruits and scouts

The lifetime development of the waggle dance of 14 honeybees was automatically recorded just after the imaginal molt using high-definition camera modules connected with a Raspberry Pi computer and numbered radio-frequency identification tags fitted to the back of each bee. For most honeybees, waggle dance follow preceded the appearance of the first waggle dance from 1 week after the imaginal molt. The duration per trip increased just after waggle dance follow. Before the appearance of the first waggle dance, the honeybee repeatedly follows waggle dances that indicate a limited number (2-6) of food source locations. We discriminated between two types of foragers with different roles, recruits and novice scouts, by comparing the vectors indicated by the bees first waggle dance (sending vectors) with dances they had previously followed (received vectors). Of 14 tagged honeybees, 11 were categorized as recruits and 2 as novice scouts. For recruits (but not for novice scouts), the duration per trip increased significantly after waggle dances follow and substantially increased just before the appearance of the first waggle dance. Moreover, recruits increased the number of times they followed waggle dances indicating the same location, and their first waggle dance indicated this location. These results suggest that the differentiation of these two types of foragers is partly related to behavioral differences after waggle dance follows: whether trip is activated or not by follows a waggle dance.\n\nSummary statementBecause of technological difficulties, there are no studies comparing the development of recruit and scout waggle dances. Using miniature radio frequency identification tags, we observed and clarified these developmental processes.\n\nList of Abbreviations

animal behavior and cognition↗

bioRxiv2017

Helpers increase daily survival rate of Southern Lapwing (Vanellus chilensis) nests during the incubation stage

Cooperative breeding is characterized by reproduction in the presence of helpers. What impact these helpers have on the reproductive success of group members is one of the long-standing questions in the cooperative breeding literature. In cooperative species, helpers are known to provide benefits during multiple stages or at a particular stage of the reproductive cycle. The aim of this study was to investigate whether helpers increased the daily survival rate of nests during the incubation stage in the Southern Lapwing (Vanellus chilensis), a crested plover with a cooperative breeding system. Southern Lapwings have a variable mating system, with some breeding groups composed of unassisted pairs, and others that breed in the presence of helpers. Our best supported model indicated a positive effect of the presence of helpers on the daily survival rate of nests, leading to a probability of nest success (i.e., survival until hatching) of 83%, compared to 51% for nests of unassisted pairs. But a null model had a similar model weight as the best supported model and was the second-best model. Our study provides evidence that helpers influence egg survival during the egg-incubation stage, which could influence the fitness of breeders.

animal behavior and cognition↗

bioRxiv2017

Odor source localization in complex visual environments by fruit flies

Flying insects routinely forage in complex and cluttered sensory environments. Their search for a food or a pheromone source typically begins with a whiff of odor, which triggers a flight response, eventually bringing the insect in the vicinity of the odor source. The precise localization of an odor source, however, requires the use of both visual and olfactory modalities, aided by air currents that trap odor molecules into turbulent plumes, which the insects track. Here, we investigated odor tracking behavior in fruit flies (Drosophila melanogaster) presented with low- or high-contrast visual landmarks, which were either paired with or separate from an attractive odor cue. These experiments were conducted either in a gentle air stream which generated odor plumes, or in still air in which odor dissipates uniformly in all directions. The trajectories of the flies revealed several novel features of their odor-tracking behavior in addition to those that have been previously documented (e.g. cast- and-surge maneuvers). First, in both moving and still air, odor-seeking flies rely on the co-occurrence of visual landmarks with olfactory cues to guide them to putative odorant objects in the decisive phase before landing. Second, flies abruptly decelerate when they encounter an odor plume, and thereafter steer towards nearby visual objects that had no inherent salience in the absence of odor. This indicates that the interception of an attractive odor increases their salience to nearby high-contrast visual landmarks. Third, flies adopt distinct odor tracking strategies during flight in moving vs. still air. Whereas they weave in and out of plumes towards an odor source when airflow is present, their approach is more gradual and incremental in still air. Both strategies are robust and flexible, and can ensure that the flies reliably find the odor source under diverse visual and airflow environments. Our experiments also indicate the possibility of an olfactory \" working memory\" that enables flies to continue their search even when the olfactory feedback is reduced or absent. Together, these results provide insights into how flies determine the precise location of an odor source.

animal behavior and cognition↗

bioRxiv2017

SwarmSight: Real-Time Tracking of Insect Antenna Movements and Proboscis Extension Reflex using a Common Preparation and Conventional Hardware

Many scientifically and agriculturally important insects use antennae to detect the presence of volatile chemical compounds and extend their proboscis during feeding. The ability to rapidly obtain high-resolution measurements of natural antenna and proboscis movements and assess how they change in response to chemical, developmental, and genetic manipulations can aid the understanding of insect behavior. By extending our previous work on assessing aggregate insect swarm or animal group movements from natural and laboratory videos using video analysis software SwarmSight, we developed a novel, free, and open-source software module, SwarmSight Appendage Tracking (SwarmSight.org) for frame-by-frame tracking of insect antenna and proboscis positions from conventional web camera videos using conventional computers. The software processes frames about 120 times faster than humans, performs at better than human accuracy, and, using 30 frames-per-second videos, can capture antennal dynamics up to 15 Hz. We used the software to track the antennal response of honey bees to two odors and found significant mean antennal retractions away from the odor source about 1 s after odor presentation. We observed antenna position density heat map cluster formation and cluster and mean angle dependence on odor concentration.

animal behavior and cognition↗

bioRxiv2017

A Rescorla-Wagner Drift-Diffusion Model of Conditioning and Timing

Computational models of classical conditioning have made significant contributions to the theoretic understanding of associative learning, yet they still struggle when the temporal aspects of conditioning are taken into account. Interval timing models have contributed a rich variety of time representations and provided accurate predictions for the timing of responses, but they usually have little to say about associative learning. In this article we present a unified model of conditioning and timing that is based on the influential Rescorla-Wagner conditioning model and the more recently developed Timing Drift-Diffusion model. We test the model by simulating 10 experimental phenomena and show that it can provide an adequate account for 8, and a partial account for the other 2. We argue that the model can account for more phenomena in the chosen set than these other similar in scope models: CSC-TD, MS-TD, Learning to Time and Modular Theory. A comparison and analysis of the mechanisms in these models is provided, with a focus on the types of time representation and associative learning rule used.\n\nAuthor SummaryHow does the time of events affect the way we learn about associations between these events? Computational models have made great contributions to our understanding of associative learning, but they usually do not perform very well when time is taken into account. Models of timing have reached high levels of accuracy in describing timed behaviour, but they usually do not have much to say about associations. A unified approach would involve combining associative learning and timing models into a single framework. This article takes just this approach. It combines the influential Rescorla-Wagner associative model with a timing model based on the Drift-Diffusion process, and shows how the resultant model can account for a number of learning and timing phenomena. The article also compares the new model to others that are similar in scope.

animal behavior and cognition↗

bioRxiv2017

Filtering Methods to Improve the Accuracy of Indoor Positioning Data for Dairy Cows

Several indoor positioning systems for livestock buildings have been developed to be used as a tool in automated animal welfare monitoring. In many environments the measurements from positioning systems still contain unwanted noise and the quality of the measurement data can be enhanced using filters.\n\nThe aim of this study was to develop an efficient filter for positioning data measured from dairy cows with UWB-based indoor positioning system in a free stall barn. We developed and tested a heuristic jump filter combined with median filter and extended Kalman filter. The performance of the filters were compared against reference data collected from Insentec Roughage intake feeders and scan sampling of animal presence in a specific lying stall with over 1500 reference observations from both methods.\n\nWe were able to improve the quality of the positioning data significantly using filtering. The 9th order median filter provided best estimates for cow position when the cows were not moving with median 100% of measurements located in correct stall and 84% in correct feeding trough when compared to the reference observations and measurements. The extended Kalman filter also improved the positioning accuracy significantly when compared to raw data and provides better of estimates of the trajectory of moving cows.

animal behavior and cognition↗

bioRxiv2017

Positional encoding in cotton-top tamarins (Saguinus oedipus)

Strategies used in artificial grammar learning can shed light into the abilities of different species to extract regularities from the environment. In the A(X)nB rule, A and B items are linked but assigned to different positional categories and separated by distractor items. Open questions are how widespread is the ability to extract positional regularities from A(X)nB patterns, which strategies are used to encode positional regularities and whether individuals exhibit preferences for absolute or relative position encoding. We used visual arrays to investigate whether cotton-top tamarins (Saguinus oedipus) can learn this rule and which strategies they use. After training on a subset of exemplars, half of the tested monkeys successfully generalized to novel combinations. These tamarins discriminated between categories of tokens with different properties (A, B, X) and detected a positional relationship between non-adjacent items even in the presence of novel distractors. Generalization, though, was incomplete, since we observed a failure with items that during training had always been presented in reinforced arrays. The pattern of errors revealed that successful subjects used visual similarity with training stimuli to solve the task, and that tamarins extracted the relative position of As and Bs rather than their absolute position, similarly to what observed in other species. Relative position encoding appears to be the default strategy in different tasks and taxa.

animal behavior and cognition↗

bioRxiv2017

Elastase-2 knockout mice display anxiogenic- and antidepressant-like phenotype: putative role for BDNF metabolism in prefrontal cortex

Several pieces of evidence indicate that elastase-2 (ELA2; chymotrypsin-like ELA2) is an alternative pathway to the generation of angiotensin II (ANG II). Elastase-2 knockout mice (ELA2KO) exhibit alterations in the arterial blood pressure and heart rate. However, there is no data on the behavioral consequences of ELA2 deletion. In this study we addressed this question, submitting ELA2KO and wild-type (WT) mice to several models sensitive to anxiety- and depression-like, memory, and repetitive behaviors. Our data indicates a higher incidence of barbering behavior in ELA2KO compared to WT, as well as an anxiogenic phenotype, evaluated in the elevated plus maze (EPM). While a decrease in locomotor activity was observed in ELA2KO in EPM, this feature was not the main source of variation in the other parameters analyzed. The marble burying test (MBT) indicated increase in repetitive behavior, observed by a higher number of buried marbles. The actimeter test indicated a decrease in total activity and confirmed the increase in repetitive behavior. The spatial memory was tested by repeated exposure to the actimeter in a 24h interval. Both ELA2KO and WT exhibited decreased activity compared to the first exposure, without any distinction between the genotypes. However, when submitted to the cued fear conditioning, ELA2KO displayed lower levels of freezing behavior in the extinction session when compared to WT, but no difference was observed during the conditioning phase. Increased levels of BDNF were found in the prefrontal cortex but not in the hippocampus of ELA2KO mice compared to WT. Finally, in silico analysis indicates that ELA2 is putatively able to cleave BDNF, and incubation of the purified enzyme with BDNF led to the degradation of the later. Our data suggested an anxiogenic- and antidepressant-like phenotype of ELA2KO, possibly associated with increased levels of BDNF in the prefrontal cortex.

animal behavior and cognition↗

bioRxiv2017

Collective mechanical adaptation of honeybee swarms

Honeybee Apis mellifera swarms form clusters made solely of bees attached to each other, forming pendant structures on tree branches (1). These clusters can be hundreds of times the size of a single organism. How these structures are stably maintained under the influence of static gravity and dynamic stimuli (e.g. wind) is unknown. To address this, we created pendant conical clusters attached to a board that was shaken with varying amplitude, frequency and total duration. Our observations show that horizontally shaken clusters spread out to form wider, flatter cones, i.e. the cluster adapts to the dynamic loading conditions, but in a reversible manner - when the loading is removed, the cluster recovers its original shape, slowly. Measuring the response of a cluster to a sharp pendular excitation before and after it adapted shows that the flattened cones deform less and relax faster than the elongated ones, i.e. they are more stable mechanically. We use particle-based simulations of a passive assemblage to suggest a behavioral hypothesis that individual bees respond to local variations in strain. This behavioral response improves the collective stability of the cluster as a whole at the expense of increasing the average mechanical burden experienced by the individual. Simulations using this rule explain our observations of adaptation to horizontal shaking. The simulations also suggest that vertical shaking will not lead to significant differential strains and thus no adaptation. To test this, we shake the cluster vertically and find that indeed there is no response to this stimulus. Altogether, our results show how an active, functional super-organism structure can respond adaptively to dynamic mechanical loading by changing its morphology to achieve better load sharing.

animal behavior and cognition↗

bioRxiv2017

Effect of vertical slit turbulence on metabolism and swimming behavior of juvenile grass carp (ctenopharyngodon idella)

Baffles were incorporated into the swim chamber of a flume-type swimming respirometer, and the effect of vertical slit turbulence on the swimming behavior and metabolism of juvenile grass carp were investigated. Results showed a significant lower TBF in turbulent flow than in laminar flow (p< 0.05). However, differences in TBF at different inlet velocities were not significant (p> 0.05), whether the fish passed through the baffles or not. In turbulent flow, the residence time ratios of test fish at different flow zone were low water velocity > medium velocity > high velocity. Oxygen consumption rate (MO2) increased with flow velocity and was higher in turbulent flow than in laminar flow. Further, the speed exponent c, in turbulent flow, was significantly higher than in laminar flow, indicated a decrease swimming efficiency. This study of fish swimming in turbulent flow extends knowledge of fish ecology and provides data for guiding the design of hydrokinetic turbulent where needed, so preventing ecological impacts.

animal behavior and cognition↗

bioRxiv2017

Precopulatory behavior and sexual conflict in the desert locust

Studies of mating and reproductive behavior have contributed much to our understanding of various animals ecological success. The desert locust, Schistocerca gregaria, is an important agricultural pest. However, knowledge of locust courtship and precopulatory behavior is surprisingly limited. Here we provide a comprehensive study of the precopulatory behavior of both sexes of the desert locust in the gregarious phase, with particular emphasis on the conflict between the sexes. Detailed HD-video monitoring of courtship and mating of 20 locust pairs, in a controlled environment, enabled both qualitative and quantitative descriptions of the behavior. A comprehensive list of behavioral elements was used to generate an eight-step ethogram, depicting from first encounter between the sexes to actual copulation. Further analyses included the probability of each element occurring, and a kinematic diagram based on a transitional matrix. Eleven novel behavioral elements are described in this study, and two potential points of conflict between the sexes are identified. Locust sexual interaction was characterized by the dominance of the males during the pre-mounting stage, and an overall stereotypic male courtship behavior. In contrast, females displayed no clear courtship-related behavior and an overall less organized behavioral sequence. Central elements in the sexual behavior of the females were low-amplitude hind-leg vibration, as well as rejecting males by jumping and kicking. Intricate reciprocal interactions between the sexes were evident mostly at the mounting stage. The reported findings contribute important insights to our knowledge of locust mating and reproductive behavior, and may assist in confronting this devastating agricultural pest.

animal behavior and cognition↗

bioRxiv2017

Genetic differences in the behavioral organization of binge eating, conditioned food reward, and compulsive-like eating in C57BL/6J and DBA/2J strains

Binge eating (BE) is a heritable symptom of eating disorders associated with anxiety, depression, malnutrition, and obesity. Genetic analysis of BE could facilitate therapeutic discovery. We used an intermittent, limited access BE paradigm involving sweetened palatable food (PF) to examine genetic differences in BE, conditioned food reward, and compulsive-like eating between C57BL/6J (B6J) and DBA/2J (D2J) inbred mouse strains. D2J mice showed a robust escalation in intake and conditioned place preference for the PF-paired side. D2J mice also showed a unique style of compulsive-like eating in the light/dark conflict test where they rapidly hoarded and consumed PF in the preferred unlit environment. BE and compulsive-like eating exhibited narrow-sense heritability estimates between 56 and 73 percent. To gain insight into the genetic basis, we phenotyped and genotyped a small cohort of 133 B6J x D2J-F2 mice at the peak location of three quantitative trait loci (QTL) previously identified in F2 mice for sweet taste (chromosome 4: 156 Mb), bitter taste (chromosome 6: 133 Mb) and behavioral sensitivity to drugs of abuse (chromosome 11: 50 Mb). The D2J allele on chromosome 6 was associated with greater PF intake on training days and greater compulsive-like PF intake, but only in males, suggesting that decreased bitter taste may increase BE in males. The D2J allele on chromosome 11 was associated with an increase in final PF intake and slope of escalation across days. Future studies employing larger crosses and genetic reference panels comprising B6J and D2J alleles will identify causal genes and neurobiological mechanisms.

animal behavior and cognition↗

bioRxiv2017

Neuronal rhythms orchestrate cell assembles to distinguish perceptual categories

Categories are reflected in the spiking activity of neurons. However, how neurons form ensembles for categories is unclear. To address this, we simultaneously recorded spiking and local field potential (LFP) activity in the lateral prefrontal cortex (lPFC) of monkeys performing a delayed match to category task with two independent category sets (Animals: Cats vs Dogs; Cars: Sports Cars vs Sedans). We found stimulus and category information in alpha and beta band oscillations. Different category distinctions engaged different frequencies. There was greater spike field coherence (SFC) in alpha ([~]8-14 Hz) for Cats and in beta ([~]16-22 Hz) for Dogs. Cars showed similar differences, albeit less pronounced: greater alpha SFC for Sedans and greater beta SFC for Sports Cars. Thus, oscillatory rhythms can help coordinate neurons into different ensembles. Engagement of different frequencies may help differentiate the categories.

animal behavior and cognition↗

bioRxiv2017

Hormonal regulation of women’s prosocial, but not sexual, responses to kinship cues

Mate preferences and mating-related behaviors are hypothesized to change over the menstrual cycle in ways that function to increase reproductive fitness. Results of recent large-scale studies suggest that many of these hormone-linked behavioral changes are less robust than was previously thought. One hypothesis that has not yet been subject to a large-scale test is the proposal that womens preference for associating with male kin is down-regulated during the ovulatory (high-fertility) phase of the menstrual cycle. Consequently, we used a longitudinal design to investigate the relationship between changes in womens steroid hormone levels and their perceptions of faces experimentally manipulated to possess kinship cues. Analyses suggested that women viewed mens faces displaying kinship cues more positively (i.e., more attractive and trustworthy) when estradiol-to-progesterone ratio was high. Since estradiol-to-progesterone ratio is positively associated with conception risk during the menstrual cycle, these results directly contradict the hypothesis that womens preference for associating with male kin is down-regulated during the ovulatory (high-fertility) phase of the menstrual cycle. Data and code are publicly available at https://osf.io/wnhma/.

animal behavior and cognition↗

bioRxiv2017

Behavioral diversity assisting obstacle navigation during group transportation in ant

Cooperative transportation behavior in ants has attracted attention from a wide range of researchers, from behavioral biologists to roboticists. Ants can accomplish complex tasks as a group whereas individual ants are not intelligent (in the context of thisstudys tasks). In this study, group transportation and obstacle navigation in Formica japonica, an ant species exhibiting uncoordinated transportation (primitive group transportation), are observed using two differently conditioned colonies. Analysesfocus on the effect of group size on two key quantities: transportation speed and obstacle navigation period. Additionally, this study examines how these relationships differ between colonies. The tendencies in transportation speed differ between colonies whereas the obstacle navigation period is consistently reduced irrespective of the colony. To explain this seemingly inconsistent result in transportation speed, we focus on behavioral diversity in directivity, defined as the tendency of individual ants totransport a food item toward their own preferential direction. Directivity is not always toward the nest, but rather is distributed around it. The diversity of the first colony is less than that of the second colony. Based on the above results, a mechanical model is constructed. Using the translational and rotational motion equations of a rigid rod, the model mimics a food item being pulled by single or multiple ants. The directions of pulling forces exerted by individual ants are assumed to be distributed around the direction pointing toward the nest. The simulation results suggest that, as diversity in directivity increases, so does the success rate in more complicated obstacle navigation. In contrast, depending on group size, the speed of group transportation increases in the case of lower diversity while it is almost constant in the case of higher diversity. Transportation speed and obstacle navigation success rate are in a trade-off relationship.

animal behavior and cognition↗

bioRxiv2017

A cross-cultural study of sex-typicality and averageness: Correlation between frontal and lateral measures of human faces

ObjectivesFacial averageness and sexual dimorphism are extensively studied attractiveness markers, which are viewed as possible indicators of biological quality. Both are complex morphological traits and both can be easily assessed from frontal and lateral projection of a human face. Interestingly, examination of mutual relations between the frontal and lateral dimensions of these markers has so far received little attention in published research.\n\nMethodsIn our cross-cultural study, we used geometric morphometric data from male and female faces from Brazil, Cameroon, Colombia, and the Czech Republic, and analysed correlations between frontal and lateral measurements of averageness and degree of maleness/femaleness, i.e. individual variation in features that characterize sexual dimorphism. We also analysed whether the association between frontal and lateral measurements differs in men and women.\n\nResultsIn general, our results showed a moderate correlation in sexually dimorphic features between lateral and frontal facial configuration in both sexes, while frontal and lateral facial averageness was moderately correlated only in women. This pattern was less consistent when individual populations were analysed separately.\n\nConclusionsReferring to the multiple signalling theory, we propose that especially in women, lateral/frontal correlations support a hypothesis of redundancy of information provided by the frontal and lateral dimension of a given facial attractiveness marker. The absence of a significant correlation in male facial averageness suggests that frontal and lateral averageness may convey different information about an individual.

animal behavior and cognition↗

bioRxiv2017

Quantifying male and female pheromone-based mate choice in Caenorhabditis nematodes using a novel microfluidic technique

Pheromone cues are an important component of intersexual communication, particularly in regards to mate choice. Caenorhabditis nematodes predominant rely on pheromone production for mate finding and mate choice. Here we describe a new microfluidic paradigm for studying mate choice in nematodes. Specifically, the Pheromone Arena allows for a constant flow of small molecule signals to be passed in real time from signaling worms to those making a choice without any physical contact. We validated this microfluidic paradigm by corroborating previous studies in showing that virgin C. remanei and C. elegans males have a strong preference for virgin females over mated ones. Moreover, our results suggest that the strength of attraction is an additive effect of male receptivity and female signal production. We go on to explicitly examine female choice and find that females are more attracted to virgin males. However, a females mate choice is strongly dependent on her mating status.

animal behavior and cognition↗