Mapping the navigational knowledge of individually foraging ants,Myrmecia croslandi

Ants are efficient navigators, guided by path integration and visual landmarks. Path integration is the primary strategy in landmark-poor habitats, but landmarks are readily used when available. The landmark panorama provides reliable information about heading direction, routes and specific location. Visual memories for guidance are often acquired along routes or near to significant places. Over what area can such locally acquired memories provide information for reaching a place? This question is unusually approachable in the solitary foraging Australian jack jumper ant, since individual foragers typically travel to one or two nest-specific foraging trees. We find that within 10 m from the nest, ants both with and without home vector information available from path integration return directly to the nest from all compass directions, after briefly scanning the panorama. By reconstructing panoramic views within the successful homing range, we show that in the open woodland habitat of these ants, snapshot memories acquired close to the nest provide sufficient navigational information to determine nest-directed heading direction over a surprisingly large area, including areas that animals may have not visited previously.     

Cultural Modulation of Face and Gaze Scanning in Young Children

Previous research has demonstrated that the way human adults look at others’ faces is modulated by their cultural background, but very little is known about how such a culture-specific pattern of face gaze develops. The current study investigated the role of cultural background on the development of face scanning in young children between the ages of 1 and 7 years, and its modulation by the eye gaze direction of the face. British and Japanese participants’ eye movements were recorded while they observed faces moving their eyes towards or away from the participants. British children fixated more on the mouth whereas Japanese children fixated more on the eyes, replicating the results with adult participants. No cultural differences were observed in the differential responses to direct and averted gaze. The results suggest that different patterns of face scanning exist between different cultures from the first years of life, but differential scanning of direct and averted gaze associated with different cultural norms develop later in life.     

Better tired than lost: Turtle ant trail networks favor coherence over short edges

Creating a routing backbone is a fundamental problem in both biology and engineering. The routing backbone of the trail networks of arboreal turtle ants (Cephalotes goniodontus) connects many nests and food sources using trail pheromone deposited by ants as they walk. Unlike species that forage on the ground, the trail networks of arboreal ants are constrained by the vegetation. We examined what objectives the trail networks meet by comparing the observed ant trail networks with networks of random, hypothetical trail networks in the same surrounding vegetation and with trails optimized for four objectives: minimizing path length, minimizing average edge length, minimizing number of nodes, and minimizing opportunities to get lost. The ants’ trails minimized path length by minimizing the number of nodes traversed rather than choosing short edges. In addition, the ants’ trails reduced the opportunity for ants to get lost at each node, favoring nodes with 3D configurations most likely to be reinforced by pheromone. Thus, rather than finding the shortest edges, turtle ant trail networks take advantage of natural variation in the environment to favor coherence, keeping the ants together on the trails.     

Bumblebee Homing: The Fine Structure of Head Turning Movements

Changes in flight direction in flying insects are largely due to roll, yaw and pitch rotations of their body. Head orientation is stabilized for most of the time by counter rotation. Here, we use high-speed video to analyse head- and body-movements of the bumblebee Bombus terrestris while approaching and departing from a food source located between three landmarks in an indoor flight-arena. The flight paths consist of almost straight flight segments that are interspersed with rapid turns. These short and fast yaw turns (“saccades”) are usually accompanied by even faster head yaw turns that change gaze direction. Since a large part of image rotation is thereby reduced to brief instants of time, this behavioural pattern facilitates depth perception from visual motion parallax during the intersaccadic intervals. The detailed analysis of the fine structure of the bees’ head turning movements shows that the time course of single head saccades is very stereotypical. We find a consistent relationship between the duration, peak velocity and amplitude of saccadic head movements, which in its main characteristics resembles the so-called "saccadic main sequence" in humans. The fact that bumblebee head saccades are highly stereotyped as in humans, may hint at a common principle, where fast and precise motor control is used to reliably reduce the time during which the retinal images moves.     

Assessing Self-Awareness through Gaze Agency

We define gaze agency as the awareness of the causal effect of one’s own eye movements in gaze-contingent environments, which might soon become a widespread reality with the diffusion of gaze-operated devices. Here we propose a method for measuring gaze agency based on self-monitoring propensity and sensitivity. In one task, naïf observers watched bouncing balls on a computer monitor with the goal of discovering the cause of concurrently presented beeps, which were generated in real-time by their saccades or by other events (Discovery Task). We manipulated observers’ self-awareness by pre-exposing them to a condition in which beeps depended on gaze direction or by focusing their attention to their own eyes. These manipulations increased propensity to agency discovery. In a second task, which served to monitor agency sensitivity at the sensori-motor level, observers were explicitly asked to detect gaze agency (Detection Task). Both tasks turned out to be well suited to measure both increases and decreases of gaze agency. We did not find evident oculomotor correlates of agency discovery or detection. A strength of our approach is that it probes self-monitoring propensity–difficult to evaluate with traditional tasks based on bodily agency. In addition to putting a lens on this novel cognitive function, measuring gaze agency could reveal subtle self-awareness deficits in pathological conditions and during development.     

Population Responses to Environmental Change in a Tropical Ant: The Interaction of Spatial and Temporal Dynamics

Spatial structure can have a profound, but often underappreciated, effect on the temporal dynamics of ecosystems. Here we report on a counterintuitive increase in the population of a tree-nesting ant, Azteca sericeasur, in response to a drastic reduction in the number of potential nesting sites. This surprising result is comprehensible when viewed in the context of the self-organized spatial dynamics of the ants and their effect on the ants’ dispersal-limited natural enemies. Approximately 30% of the trees in the study site, a coffee agroecosystem in southern Mexico, were pruned or felled over a two-year period, and yet the abundance of the ant nests more than doubled over the seven-year study. Throughout the transition, the spatial distribution of the ants maintained a power-law distribution – a signal of spatial self organization – but the local clustering of the nests was reduced post-pruning. A cellular automata model incorporating the changed spatial structure of the ants and the resulting partial escape from antagonists reproduced the observed increase in abundance, highlighting how self-organized spatial dynamics can profoundly influence the responses of ecosystems to perturbations.     

Visual gaze control during peering flight manoeuvres in honeybees

As animals travel through the environment, powerful reflexes help stabilize their gaze by actively maintaining head and eyes in a level orientation. Gaze stabilization reduces motion blur and prevents image rotations. It also assists in depth perception based on translational optic flow. Here we describe side-to-side flight manoeuvres in honeybees and investigate how the bees’ gaze is stabilized against rotations during these movements. We used high-speed video equipment to record flight paths and head movements in honeybees visiting a feeder. We show that during their approach, bees generate lateral movements with a median amplitude of about 20 mm. These movements occur with a frequency of up to 7 Hz and are generated by periodic roll movements of the thorax with amplitudes of up to ±60°. During such thorax roll oscillations, the head is held close to horizontal, thereby minimizing rotational optic flow. By having bees fly through an oscillating, patterned drum, we show that head stabilization is based mainly on visual motion cues. Bees exposed to a continuously rotating drum, however, hold their head fixed at an oblique angle. This result shows that although gaze stabilization is driven by visual motion cues, it is limited by other mechanisms, such as the dorsal light response or gravity reception.     

Keep the nest clean: survival advantages of corpse removal in ants

Sociality increases exposure to pathogens. Therefore, social insects have developed a wide range of behavioural defences, known as ‘social immunity’. However, the benefits of these behaviours in terms of colony survival have been scarcely investigated. We tested the survival advantage of prophylaxis, i.e. corpse removal, in ants. Over 50 days, we compared the survival of ants in colonies that were free to remove corpses with those that were restricted in their corpse removal. From Day 8 onwards, the survival of adult workers was significantly higher in colonies that were allowed to remove corpses normally. Overall, larvae survived better than adults, but were slightly affected by the presence of corpses in the nest. When removal was restricted, ants removed as many corpses as they could and moved the remaining corpses away from brood, typically to the nest corners. These results show the importance of nest maintenance and prophylactic behaviour in social insects.     

Eye-Head Coordination for Visual Cognitive Processing

We investigated coordinated movements between the eyes and head (“eye-head coordination”) in relation to vision for action. Several studies have measured eye and head movements during a single gaze shift, focusing on the mechanisms of motor control during eye-head coordination. However, in everyday life, gaze shifts occur sequentially and are accompanied by movements of the head and body. Under such conditions, visual cognitive processing influences eye movements and might also influence eye-head coordination because sequential gaze shifts include cycles of visual processing (fixation) and data acquisition (gaze shifts). In the present study, we examined how the eyes and head move in coordination during visual search in a large visual field. Subjects moved their eyes, head, and body without restriction inside a 360° visual display system. We found patterns of eye-head coordination that differed those observed in single gaze-shift studies. First, we frequently observed multiple saccades during one continuous head movement, and the contribution of head movement to gaze shifts increased as the number of saccades increased. This relationship between head movements and sequential gaze shifts suggests eye-head coordination over several saccade-fixation sequences; this could be related to cognitive processing because saccade-fixation cycles are the result of visual cognitive processing. Second, distribution bias of eye position during gaze fixation was highly correlated with head orientation. The distribution peak of eye position was biased in the same direction as head orientation. This influence of head orientation suggests that eye-head coordination is involved in gaze fixation, when the visual system processes retinal information. This further supports the role of eye-head coordination in visual cognitive processing.     

Facilitation of Visual Perception in Head Direction: Visual Attention Modulation Based on Head Direction

People usually see things using frontal viewing, and avoid lateral viewing (or eccentric gaze) where the directions of the head and eyes are largely different. Lateral viewing interferes with attentive visual search performance, probably because the head is directed away from the target and/or because the head and eyes are misaligned. In this study, we examined which of these factors is the primary one for interference by conducting a visual identification experiment where a target was presented in the peripheral visual field. The critical manipulation was the participants’ head direction and fixation position: the head was directed to the fixation location, the target position, or the opposite side of the fixation. The performance was highest when the head was directed to the target position even when there was misalignment of the head and eye, suggesting that visual perception can be influenced by both head direction and fixation position.     

How Do Ants Make Sense of Gravity? A Boltzmann Walker Analysis of Lasius niger Trajectories on Various Inclines

The goal of this study is to describe accurately how the directional information given by support inclinations affects the ant Lasius niger motion in terms of a behavioral decision. To this end, we have tracked the spontaneous motion of 345 ants walking on a 0.5×0.5 m plane canvas, which was tilted with 5 various inclinations by rad ( data points). At the population scale, support inclination favors dispersal along uphill and downhill directions. An ant''s decision making process is modeled using a version of the Boltzmann Walker model, which describes an ant''s random walk as a series of straight segments separated by reorientation events, and was extended to take directional influence into account. From the data segmented accordingly ( segments), this extension allows us to test separately how average speed, segments lengths and reorientation decisions are affected by support inclination and current walking direction of the ant. We found that support inclination had a major effect on average speed, which appeared approximately three times slower on the incline. However, we found no effect of the walking direction on speed. Contrastingly, we found that ants tend to walk longer in the same direction when they move uphill or downhill, and also that they preferentially adopt new uphill or downhill headings at turning points. We conclude that ants continuously adapt their decision making about where to go, and how long to persist in the same direction, depending on how they are aligned with the line of maximum declivity gradient. Hence, their behavioral decision process appears to combine klinokinesis with geomenotaxis. The extended Boltzmann Walker model parameterized by these effects gives a fair account of the directional dispersal of ants on inclines.     

Melissotarsus ants are likely able to digest plant polysaccharides

Melissotarsus ants have an extremely specialized set of behaviours. Both workers and gynes tunnel galleries in their host tree bark. Workers walk with their mesothoracic legs pointing upwards and tend Diaspididae hemiptera for their flesh. The ants use their forelegs to plug the galleries with silk that they secrete themselves. We hypothesised that the ants’ energetic needs for nearly constant gallery digging could be satisfied through the absorption of host tree tissues; so, using basic techniques, we examined the digestive capacities of workers from two species. We show that workers are able to degrade oligosaccharides and heterosides as well as, to a lesser degree, polysaccharides. This is one of the rare reports on ants able to digest plant polysaccharides other than starch.     

Subtle cues of predation risk: starlings respond to a predator's direction of eye-gaze

For prey animals to negotiate successfully the fundamental trade-off between predation and starvation, a realistic assessment of predation risk is vital. Prey responses to conspicuous indicators of risk (such as looming predators or fleeing conspecifics) are well documented, but there should also be strong selection for the detection of more subtle cues. A predator's head orientation and eye-gaze direction are good candidates for subtle but useful indicators of risk, since many predators orient their head and eyes towards their prey as they attack. We describe the first explicit demonstration of a bird responding to a live predator's eye-gaze direction. We present wild-caught European starlings (Sturnus vulgaris) with human 'predators' whose frontal appearance and gaze direction are manipulated independently, and show that starlings are sensitive to the predator's orientation, the presence of eyes and the direction of eye-gaze. Starlings respond in a functionally significant manner: when the predator's gaze was averted, starlings resumed feeding earlier, at a higher rate and consumed more food overall. By correctly assessing lower risk and returning to feeding activity earlier (as in this study), the animal gains a competitive advantage over conspecifics that do not respond to the subtle predator cue in this way.     

The Effect of Trail Pheromone and Path Confinement on Learning of Complex Routes in the Ant Lasius niger

Route learning is key to the survival of many central place foragers, such as bees and many ants. For ants which lay pheromone trails, the presence of a trail may act as an important source of information about whether an error has been made. The presence of trail pheromone has been demonstrated to support route learning, and the effect of pheromones on route choice have been reported to persist even after the pheromones have been removed. This could be explained in two ways: the pheromone may constrain the ants onto the correct route, thus preventing errors and aiding learning. Alternatively, the pheromones may act as a ‘reassurance’, signalling that the learner is on the right path and that learning the path is worthwhile. Here, we disentangle pheromone presence from route confinement in order to test these hypotheses, using the ant Lasius niger as a model. Unexpectedly, we did not find any evidence that pheromones support route learning. Indeed, there was no evidence that ants confined to the correct route learned at all. Thus, while we cannot support the ‘reassurance’ hypothesis, we can rule out the ‘confinement’ hypothesis. Other findings, such as a reduction in pheromone deposition in the presence of trail pheromones, are remarkably consistent with previous experiments. As previously reported, ants which make errors on their outward journey upregulate pheromone deposition on their return. Surprisingly, ants which would go on to make an error down-regulate pheromone deposition on their outward journey, hinting at a capacity for ants to gauge the quality of their own memories.     

Social orienting in gaze leading: a mechanism for shared attention

Here, we report a novel social orienting response that occurs after viewing averted gaze. We show, in three experiments, that when a person looks from one location to an object, attention then shifts towards the face of an individual who has subsequently followed the person''s gaze to that same object. That is, contrary to ‘gaze following’, attention instead orients in the opposite direction to observed gaze and towards the gazing face. The magnitude of attentional orienting towards a face that ‘follows’ the participant''s gaze is also associated with self-reported autism-like traits. We propose that this gaze leading phenomenon implies the existence of a mechanism in the human social cognitive system for detecting when one''s gaze has been followed, in order to establish ‘shared attention’ and maintain the ongoing interaction.     

Opposing effects of allogrooming on disease transmission in ant societies

To prevent epidemics, insect societies have evolved collective disease defences that are highly effective at curing exposed individuals and limiting disease transmission to healthy group members. Grooming is an important sanitary behaviour—either performed towards oneself (self-grooming) or towards others (allogrooming)—to remove infectious agents from the body surface of exposed individuals, but at the risk of disease contraction by the groomer. We use garden ants (Lasius neglectus) and the fungal pathogen Metarhizium as a model system to study how pathogen presence affects self-grooming and allogrooming between exposed and healthy individuals. We develop an epidemiological SIS model to explore how experimentally observed grooming patterns affect disease spread within the colony, thereby providing a direct link between the expression and direction of sanitary behaviours, and their effects on colony-level epidemiology. We find that fungus-exposed ants increase self-grooming, while simultaneously decreasing allogrooming. This behavioural modulation seems universally adaptive and is predicted to contain disease spread in a great variety of host–pathogen systems. In contrast, allogrooming directed towards pathogen-exposed individuals might both increase and decrease disease risk. Our model reveals that the effect of allogrooming depends on the balance between pathogen infectiousness and efficiency of social host defences, which are likely to vary across host–pathogen systems.     

Neural Signals Evoked by Stimuli of Increasing Social Scene Complexity Are Detectable at the Single-Trial Level and Right Lateralized

Classification of neural signals at the single-trial level and the study of their relevance in affective and cognitive neuroscience are still in their infancy. Here we investigated the neurophysiological correlates of conditions of increasing social scene complexity using 3D human models as targets of attention, which may also be important in autism research. Challenging single-trial statistical classification of EEG neural signals was attempted for detection of oddball stimuli with increasing social scene complexity. Stimuli had an oddball structure and were as follows: 1) flashed schematic eyes, 2) simple 3D faces flashed between averted and non-averted gaze (only eye position changing), 3) simple 3D faces flashed between averted and non-averted gaze (head and eye position changing), 4) animated avatar alternated its gaze direction to the left and to the right (head and eye position), 5) environment with 4 animated avatars all of which change gaze and one of which is the target of attention. We found a late (> 300 ms) neurophysiological oddball correlate for all conditions irrespective of their complexity as assessed by repeated measures ANOVA. We attempted single-trial detection of this signal with automatic classifiers and obtained a significant balanced accuracy classification of around 79%, which is noteworthy given the amount of scene complexity. Lateralization analysis showed a specific right lateralization only for more complex realistic social scenes. In sum, complex ecological animations with social content elicit neurophysiological events which can be characterized even at the single-trial level. These signals are right lateralized. These finding paves the way for neuroscientific studies in affective neuroscience based on complex social scenes, and given the detectability at the single trial level this suggests the feasibility of brain computer interfaces that can be applied to social cognition disorders such as autism.     

Fermat’s Principle of Least Time Predicts Refraction of Ant Trails at Substrate Borders

Fermat’s principle of least time states that light rays passing through different media follow the fastest (and not the most direct) path between two points, leading to refraction at medium borders. Humans intuitively employ this rule, e.g., when a lifeguard has to infer the fastest way to traverse both beach and water to reach a swimmer in need. Here, we tested whether foraging ants also follow Fermat’s principle when forced to travel on two surfaces that differentially affected the ants’ walking speed. Workers of the little fire ant, Wasmannia auropunctata, established “refracted” pheromone trails to a food source. These trails deviated from the most direct path, but were not different to paths predicted by Fermat’s principle. Our results demonstrate a new aspect of decentralized optimization and underline the versatility of the simple yet robust rules governing the self-organization of group-living animals.     

Ants show a leftward turning bias when exploring unknown nest sites

Behavioural lateralization in invertebrates is an important field of study because it may provide insights into the early origins of lateralization seen in a diversity of organisms. Here, we present evidence for a leftward turning bias in Temnothorax albipennis ants exploring nest cavities and in branching mazes, where the bias is initially obscured by thigmotaxis (wall-following) behaviour. Forward travel with a consistent turning bias in either direction is an effective nest exploration method, and a simple decision-making heuristic to employ when faced with multiple directional choices. Replication of the same bias at the colony level would also reduce individual predation risk through aggregation effects, and may lead to a faster attainment of a quorum threshold for nest migration. We suggest the turning bias may be the result of an evolutionary interplay between vision, exploration and migration factors, promoted by the ants'' eusociality.     

Viewing Complex,Dynamic Scenes “Through the Eyes” of Another Person: The Gaze-Replay Paradigm

We present a novel “Gaze-Replay” paradigm that allows the experimenter to directly test how particular patterns of visual input—generated from people’s actual gaze patterns—influence the interpretation of the visual scene. Although this paradigm can potentially be applied across domains, here we applied it specifically to social comprehension. Participants viewed complex, dynamic scenes through a small window displaying only the foveal gaze pattern of a gaze “donor.” This was intended to simulate the donor’s visual selection, such that a participant could effectively view scenes “through the eyes” of another person. Throughout the presentation of scenes presented in this manner, participants completed a social comprehension task, assessing their abilities to recognize complex emotions. The primary aim of the study was to assess the viability of this novel approach by examining whether these Gaze-Replay windowed stimuli contain sufficient and meaningful social information for the viewer to complete this social perceptual and cognitive task. The results of the study suggested this to be the case; participants performed better in the Gaze-Replay condition compared to a temporally disrupted control condition, and compared to when they were provided with no visual input. This approach has great future potential for the exploration of experimental questions aiming to unpack the relationship between visual selection, perception, and cognition.