Visual antipredator effects of web flexing in an orb web spider, with special reference to web decorations.

Some visual antipredator strategies involve the rapid movement of highly contrasting body patterns to frighten or confuse the predator. Bright body colouration, however, can also be detected by potential predators and used as a cue. Among spiders, Argiope spp. are usually brightly coloured but they are not a common item in the diet of araneophagic wasps. When disturbed, Argiope executes a web-flexing behaviour in which they move rapidly and may be perceived as if they move backwards and towards an observer in front of the web. We studied the mechanisms underlying web-flexing behaviour as a defensive strategy. Using multispectral images and high-speed videos with deep-learning-based tracking techniques, we evaluated body colouration, body pattern, and spider kinematics from the perspective of a potential wasp predator. We show that the spider's abdomen is conspicuous, with a disruptive colouration pattern. We found that the body outline of spiders with web decorations was harder to detect when compared to spiders without decorations. The abdomen was also the body part that moved fastest, and its motion was composed mainly of translational (vertical) vectors in the potential predator's optical flow. In addition, with high contrast colouration, the spider's movement might be perceived as a sudden change in body size (looming effect) as perceived by the predator. These effects alongside the other visual cues may confuse potential wasp predators by breaking the spider body outline and affecting the wasp's flight manoeuvre, thereby deterring the wasp from executing the final attack.

Physiological properties of the visual system in the Green Weaver ant, Oecophylla smaragdina.

The Green Weaver ants, Oecophylla smaragdina are iconic animals known for their extreme cooperative behaviour where they bridge gaps by linking to each other to build living chains. They are visually oriented animals, build chains towards closer targets, use celestial compass cues for navigation and are visual predators. Here, we describe their visual sensory capacity. The major workers of O. smaragdina have more ommatidia (804) in each eye compared to minor workers (508), but the facet diameters are comparable between both castes. We measured the impulse responses of the compound eye and found their response duration (42 ms) was similar to that seen in other slow-moving ants. We determined the flicker fusion frequency of the compound eye at the brightest light intensity to be 132 Hz, which is relatively fast for a walking insect suggesting the visual system is well suited for a diurnal lifestyle. Using pattern-electroretinography we identified the compound eye has a spatial resolving power of 0.5 cycles deg-1 and reached peak contrast sensitivity of 2.9 (35% Michelson contrast threshold) at 0.05 cycles deg-1. We discuss the relationship of spatial resolution and contrast sensitivity, with number of ommatidia and size of the lens.

Ecological strategies of (pl)ants: Towards a world-wide worker economic spectrum for ants.

Current global challenges call for a rigorously predictive ecology. Our understanding of ecological strategies, imputed through suites of measurable functional traits, comes from decades of work that largely focussed on plants. However, a key question is whether plant ecological strategies resemble those of other organisms.Among animals, ants have long been recognised to possess similarities with plants: as (largely) central place foragers. For example, individual ant workers play similar foraging roles to plant leaves and roots and are similarly expendable. Frameworks that aim to understand plant ecological strategies through key functional traits, such as the 'leaf economics spectrum', offer the potential for significant parallels with ant ecological strategies.Here, we explore these parallels across several proposed ecological strategy dimensions, including an 'economic spectrum', propagule size-number trade-offs, apparency-defence trade-offs, resource acquisition trade-offs and stress-tolerance trade-offs. We also highlight where ecological strategies may differ between plants and ants. Furthermore, we consider how these strategies play out among the different modules of eusocial organisms, where selective forces act on the worker and reproductive castes, as well as the colony.Finally, we suggest future directions for ecological strategy research, including highlighting the availability of data and traits that may be more difficult to measure, but should receive more attention in future to better understand the ecological strategies of ants. The unique biology of eusocial organisms provides an unrivalled opportunity to bridge the gap in our understanding of ecological strategies in plants and animals and we hope that this perspective will ignite further interest. Read the free Plain Language Summary for this article on the Journal blog.

Visual signals in the wing display of a tephritid fly deter jumping spider attacks.

Visual animal communication, whether to the same or to other species, is largely conducted through dynamic and colourful signals. For a signal to be effective, the signaller must capture and retain the attention of the receiver. Signal efficacy is also dependent on the sensory limitations of the receiver. However, most signalling studies consider movement and colour separately, resulting in a partial understanding of the signal in question. We explored the structure and function of predator-prey signalling in the jumping spider-tephritid fly system, where the prey performs a wing waving display that deters an attack from the predator. Using a custom-built spider retinal tracker combined with visual modelling, as well as behavioural assays, we studied the effect of fly wing movement and colour on the jumping spider's visual system. We show that jumping spiders track their prey less effectively during wing display and this can be attributed to a series of fluctuations in chromatic and achromatic contrasts arising from the wing movements. These results suggest that displaying flies deter spider attacks by manipulating the movement biases of the spider's visual system. Our results emphasise the importance of receiver attention on the evolution of interspecific communication.

Fast acrobatic maneuvers enable arboreal spiders to hunt dangerous prey.

Spiders, the most specious taxon of predators, have evolved an astounding range of predatory strategies, including group hunting, specialized silk traps, pheromone-loaded bolas, and aggressive mimicry. Spiders that hunt prey defended with behavioral, mechanical, or chemical means are under additional selection pressure to avoid injury and death. Ants are considered dangerous because they can harm or kill their predators, but some groups of spiders, such as the Theridiidae, have a very high diversification of ant-hunting species and strategies [J. Liu et al., Mol. Phylogenet. Evol. 94, 658-675 (2016)]. Here, we provide detailed behavioral analyses of the highly acrobatic Australian ant-slayer spider, Euryopis umbilicata (Theridiidae), that captures much larger and defended Camponotus ants on vertical tree trunks. The hunting sequence consists of ritualized steps performed within split seconds, resulting in an exceptionally high prey capture success rate.

AnimalTraits - a curated animal trait database for body mass, metabolic rate and brain size.

Trait databases have become important resources for large-scale comparative studies in ecology and evolution. Here we introduce the AnimalTraits database, a curated database of body mass, metabolic rate and brain size, in standardised units, for terrestrial animals. The database has broad taxonomic breadth, including tetrapods, arthropods, molluscs and annelids from almost 2000 species and 1000 genera. All data recorded in the database are sourced from their original empirical publication, and the original metrics and measurements are included with each record. This allows for subsequent data transformations as required. We have included rich metadata to allow users to filter the dataset. The additional R scripts we provide will assist researchers with aggregating standardised observations into species-level trait values. Our goals are to provide this resource without restrictions, to keep the AnimalTraits database current, and to grow the number of relevant traits in the future.

Nocturnal Myrmecia ants have faster temporal resolution at low light levels but lower adaptability compared to diurnal relatives.

Nocturnal insects likely have evolved distinct physiological adaptations to enhance sensitivity for tasks, such as catching moving prey, where the signal-noise ratio of visual information is typically low. Using electroretinogram recordings, we measured the impulse response and the flicker fusion frequency (FFF) in six congeneric species of Myrmecia ants with different diurnal rhythms. The FFF, which measures the ability of an eye to respond to a flickering light, is significantly lower in nocturnal ants (∼125 Hz) compared to diurnal ants (∼189 Hz). However, the nocturnal ants have faster eyes at very low light intensities than the diurnal species. During the day, nocturnal ants had slower impulse responses than their diurnal counterparts. However, at night, both latency and duration significantly shortened in nocturnal species. The characteristics of the impulse responses varied substantially across all six species and did not correlate well with the measured flicker fusion frequency.

Anesthesia disrupts distance, but not direction, of path integration memory.

Solitary foraging insects, such as ants, maintain an estimate of the direction and distance to their starting location as they move away from it, in a process known as path integration. This estimate, commonly known as the "home vector," is updated continuously as the ant moves1-4 and is reset as soon as it enters its nest,5 yet ants prevented from returning to their nest can still use their home vector when released several hours later.6,7 This conjunction of fast update and long persistence of the home vector memory does not directly map to existing accounts of short-, mid-, and long-term memory;2,8-12 hence, the substrate of this memory remains unknown. Chill-coma anesthesia13-15 has previously been shown to affect associative memory retention in fruit flies14,16 and honeybees.9,17,18 We investigate the nature of path integration memory by anesthetizing ants after they have accumulated home vector information and testing if the memory persists on recovery. We show that after anesthesia the memory of the distance ants have traveled is degraded, but the memory of the direction is retained. We also show that this is consistent with models of path integration that maintain the memory in a redundant Cartesian coordinate system and with the hypothesis that chill-coma produces a proportional reduction of the memory, rather than a subtractive reduction or increase of noise. The observed effect is not compatible with a memory based on recurrent circuit activity and points toward an activity-dependent molecular process as the basis of path integration memory.

Ocellar spatial vision in Myrmecia ants.

In addition to compound eyes, insects possess simple eyes known as ocelli. Input from the ocelli modulates optomotor responses, flight-time initiation, and phototactic responses - behaviours that are mediated predominantly by the compound eyes. In this study, using pattern electroretinography (pERG), we investigated the contribution of the compound eyes to ocellar spatial vision in the diurnal Australian bull ant Myrmecia tarsata by measuring the contrast sensitivity and spatial resolving power of the ocellar second-order neurons under various occlusion conditions. Furthermore, in four species of Myrmecia ants active at different times of the day, and in European honeybee Apis mellifera, we characterized the ocellar visual properties when both visual systems were available. Among the ants, we found that the time of activity had no significant effect on ocellar spatial vision. Comparing day-active ants and the honeybee, we did not find any significant effect of locomotion on ocellar spatial vision. In M. tarsata, when the compound eyes were occluded, the amplitude of the pERG signal from the ocelli was reduced 3 times compared with conditions when the compound eyes were available. The signal from the compound eyes maintained the maximum contrast sensitivity of the ocelli as 13 (7.7%), and the spatial resolving power as 0.29 cycles deg-1. We conclude that ocellar spatial vison improves significantly with input from the compound eyes, with a noticeably larger improvement in contrast sensitivity than in spatial resolving power.

Many paths, one destination: mapping the movements of a kleptoparasitic spider on the host's web.

Kleptoparasitic spiders live and forage in the webs of other spiders. Using vibratory cues generated by the host spider during prey capture, they leave their resting positions in the upper peripheries of the host web and move towards the centre of the web where they feed along with the host spider or steal small pieces of prey. While the triggers for initiating the foraging raids are known, there is little information about the fine-scale trajectory dynamics in this model system. We mapped the movement of the kleptoparasite Argyrodes elevatus in the web of the host Trichonephila clavipes. We filmed the movement of the kleptoparasite spiders and quantified the trajectory shape, speed, heading directions and path revisitation. Our results show that kleptoparasitic spider movement is spatially structured, with higher levels of speed at the peripheries and slower in the centre of the web. We found a high level of variation in trajectory shapes between individuals. We found that the majority of heading orientations were away from the hub suggesting that detouring or repeated approaches are an essential component of kleptoparasite movement strategies. Our results of the revisitation rate also confirm this pattern, where locations close to the hub were revisited more often than in the periphery. The kleptoparasite-host spider system is a promising model to study fine-scale movement patterns in small bounded spaces.

The Antarium: A Reconstructed Visual Reality Device for Ant Navigation Research.

We constructed a large projection device (the Antarium) with 20,000 UV-Blue-Green LEDs that allows us to present tethered ants with views of their natural foraging environment. The ants walk on an air-cushioned trackball, their movements are registered and can be fed back to the visual panorama. Views are generated in a 3D model of the ants' environment so that they experience the changing visual world in the same way as they do when foraging naturally. The Antarium is a biscribed pentakis dodecahedron with 55 facets of identical isosceles triangles. The length of the base of the triangles is 368 mm resulting in a device that is roughly 1 m in diameter. Each triangle contains 361 blue/green LEDs and nine UV LEDs. The 55 triangles of the Antarium have 19,855 Green and Blue pixels and 495 UV pixels, covering 360° azimuth and elevation from -50° below the horizon to +90° above the horizon. The angular resolution is 1.5° for Green and Blue LEDs and 6.7° for UV LEDs, offering 65,536 intensity levels at a flicker frequency of more than 9,000 Hz and a framerate of 190 fps. Also, the direction and degree of polarisation of the UV LEDs can be adjusted through polarisers mounted on the axles of rotary actuators. We build 3D models of the natural foraging environment of ants using purely camera-based methods. We reconstruct panoramic scenes at any point within these models, by projecting panoramic images onto six virtual cameras which capture a cube-map of images to be projected by the LEDs of the Antarium. The Antarium is a unique instrument to investigate visual navigation in ants. In an open loop, it allows us to provide ants with familiar and unfamiliar views, with completely featureless visual scenes, or with scenes that are altered in spatial or spectral composition. In closed-loop, we can study the behavior of ants that are virtually displaced within their natural foraging environment. In the future, the Antarium can also be used to investigate the dynamics of navigational guidance and the neurophysiological basis of ant navigation in natural visual environments.

Vertical Lobes of the Mushroom Bodies Are Essential for View-Based Navigation in Australian Myrmecia Ants.

Prior to leaving home, insects acquire visual landmark information through a series of well-choreographed walks or flights of learning [1-4]. This information allows them to pinpoint goals both when in their vicinity [5-7] and from locations they have not previously visited [8-10]. It is presumed that animals returning home match memorized views to their current view for successful view-based navigation [11]. While view-based navigation strategies have been incorporated into several navigation models [8, 12, 13], we still know little about how this behavior is performed by the insect brain. Mushroom bodies are essential for visual learning and memory [14-16], and therefore we investigated their role in view-based navigation in a visually oriented ant, Myrmecia midas. We injected the local anesthetic procaine [15, 17, 18] into the mushroom body vertical lobes (VLs) to selectively inhibit neural activity in this region. We compared the behavior of VL-procaine-treated ants with three groups: untreated control, VL-saline, and off-target (antennal lobe) procaine. Experienced foragers were collected, treated, and released in their familiar environment where we documented their behavior. Animals with procaine-inactivated VLs had tortuous paths and were unable to find their nest, whereas ants from the untreated and off-target procaine groups were well directed and were the most successful at returning home. Untreated animals walked faster when their gaze was directed toward home, and this behavior was eliminated by anesthetizing the VL region. Our data provide neurobiological evidence that the mushroom body vertical lobes are necessary for retrieving visual memories for successful view-based navigation.

The role of attractive and repellent scene memories in ant homing (Myrmecia croslandi).

Solitary foraging ants rely on vision when travelling along routes and when pinpointing their nest. We tethered foragers of Myrmecia croslandi on a trackball and recorded their intended movements when the trackball was located on their normal foraging corridor (on-route), above their nest and at a location several metres away where they have never been before (off-route). We found that at on- and off-route locations, most ants walk in the nest or foraging direction and continue to do so for tens of metres in a straight line. In contrast, above the nest, ants walk in random directions and change walking direction frequently. In addition, the walking direction of ants above the nest oscillates on a fine scale, reflecting search movements that are absent from the paths of ants at the other locations. An agent-based simulation shows that the behaviour of ants at all three locations can be explained by the integration of attractive and repellent views directed towards or away from the nest, respectively. Ants are likely to acquire such views via systematic scanning movements during their learning walks. The model predicts that ants placed in a completely unfamiliar environment should behave as if at the nest, which our subsequent experiments confirmed. We conclude first, that the ants' behaviour at release sites is exclusively driven by what they currently see and not by information on expected outcomes of their behaviour; and second, that navigating ants might continuously integrate attractive and repellent visual memories. We discuss the benefits of such a procedure.

Reeling in the prey: fishing behaviour in an orb web spider.

When an insect is intercepted by a spider web, spiders quickly locate the prey and run towards it. Once they make contact with the prey, they immobilise it and retrieve it to the centre of the web or the retreat for consumption. However, in rare circumstances, the spider can also pull the prey towards itself either while running to the prey or from a stationary position, a behaviour termed as 'reeling'. Reeling is paradoxical as it can lead to web deformation or damage, thereby jeopardising future foraging success. Reeling may increase the retention time for heavier prey or information acquisition with respect to the prey's identity, especially when these prey can cause damage to either the web or the spider itself. We explored the function of reeling behaviour in a neotropical orb web spider Verrucosa arenata We show that spiders performed reeling behaviour irrespective whether they were approaching heavy or light prey, but they changed their trajectories of approach. Spiders approached heavier prey more slowly than light prey and they showed a significantly higher frequency of change in velocity. We discuss these findings in the context of prey capture strategies and prey recognition.

Ocellar structure of African and Australian desert ants.

Few walking insects possess simple eyes known as the ocelli. The role of the ocelli in walking insects such as ants has been less explored. Physiological and behavioural evidence in the desert ant, Cataglyphis bicolor, indicates that ocellar receptors are polarisation sensitive and are used to derive compass information from the pattern of polarised skylight. The ability to detect polarised skylight can also be inferred from the structure and the organisation of the ocellar retina. However, the functional anatomy of the desert ant ocelli has not been investigated. Here we characterised the anatomical organisation of the ocelli in three species of desert ants. The two congeneric species of Cataglyphis we studied had a fused rhabdom, but differed in their organisation of the retina. In Cataglyphis bicolor, each retinula cell contributed microvilli in one orientation enabling them to compare e-vector intensities. In Cataglyphis fortis, some retinula cells contributed microvilli in more than one orientation, indicating that not all cells are polarisation sensitive. The desert ant Melophorus bagoti had an unusual ocellar retina with a hexagonal or pentagonal rhabdomere arrangement forming an open rhabdom. Each retinula cell contributed microvilli in more than one orientation, making them unlikely to be polarisation detectors.

Miniaturisation reduces contrast sensitivity and spatial resolving power in ants.

Vision is crucial for animals to find prey, locate conspecifics and navigate within cluttered landscapes. Animals need to discriminate objects against a visually noisy background. However, the ability to detect spatial information is limited by eye size. In insects, as individuals become smaller, the space available for the eyes reduces, which affects the number of ommatidia, the size of the lens and the downstream information-processing capabilities. The evolution of small body size in a lineage, known as miniaturisation, is common in insects. Here, using pattern electroretinography with vertical sinusoidal gratings as stimuli, we studied how miniaturisation affects spatial resolving power and contrast sensitivity in four diurnal ants that live in a similar environment but vary in their body and eye size. We found that ants with fewer and smaller ommatidial facets had lower spatial resolving power and contrast sensitivity. The spatial resolving power was maximum in the largest ant Myrmecia tarsata at 0.60 cycles deg-1 compared with that of the ant with smallest eyes Rhytidoponera inornata at 0.48 cycles deg-1 Maximum contrast sensitivity (minimum contrast threshold) in M. tarsata (2627 facets) was 15.51 (6.4% contrast detection threshold) at 0.1 cycles deg-1, while the smallest ant R. inornata (227 facets) had a maximum contrast sensitivity of 1.34 (74.1% contrast detection threshold) at 0.05 cycles deg-1 Miniaturisation thus dramatically decreases maximum contrast sensitivity and also reduces spatial resolution, which could have implications for visually guided behaviours. This is the first study to physiologically investigate contrast sensitivity in the context of insect allometry.

Differential investment in brain regions for a diurnal and nocturnal lifestyle in Australian Myrmecia ants.

Animals are active at different times of the day. Each temporal niche offers a unique light environment, which affects the quality of the available visual information. To access reliable visual signals in dim-light environments, insects have evolved several visual adaptations to enhance their optical sensitivity. The extent to which these adaptations reflect on the sensory processing and integration capabilities within the brain of a nocturnal insect is unknown. To address this, we analyzed brain organization in congeneric species of the Australian bull ant, Myrmecia, that rely predominantly on visual information and range from being strictly diurnal to strictly nocturnal. Weighing brains and optic lobes of seven Myrmecia species, showed that after controlling for body mass, the brain mass was not significantly different between diurnal and nocturnal ants. However, the optic lobe mass, after controlling for central brain mass, differed between day- and night-active ants. Detailed volumetric analyses showed that the nocturnal ants invested relatively less in the primary visual processing regions but relatively more in both the primary olfactory processing regions and in the integration centers of visual and olfactory sensory information. We discuss how the temporal niche occupied by each species may affect cognitive demands, thus shaping brain organization among insects active in dim-light conditions.

Principles of Insect Path Integration.

Continuously monitoring its position in space relative to a goal is one of the most essential tasks for an animal that moves through its environment. Species as diverse as rats, bees, and crabs achieve this by integrating all changes of direction with the distance covered during their foraging trips, a process called path integration. They generate an estimate of their current position relative to a starting point, enabling a straight-line return, following what is known as a home vector. While in theory path integration always leads the animal precisely back home, in the real world noise limits the usefulness of this strategy when operating in isolation. Noise results from stochastic processes in the nervous system and from unreliable sensory information, particularly when obtaining heading estimates. Path integration, during which angular self-motion provides the sole input for encoding heading (idiothetic path integration), results in accumulating errors that render this strategy useless over long distances. In contrast, when using an external compass this limitation is avoided (allothetic path integration). Many navigating insects indeed rely on external compass cues for estimating body orientation, whereas they obtain distance information by integration of steps or optic-flow-based speed signals. In the insect brain, a region called the central complex plays a key role for path integration. Not only does the central complex house a ring-attractor network that encodes head directions, neurons responding to optic flow also converge with this circuit. A neural substrate for integrating direction and distance into a memorized home vector has therefore been proposed in the central complex. We discuss how behavioral data and the theoretical framework of path integration can be aligned with these neural data.

The choreography of learning walks in the Australian jack jumper ant Myrmecia croslandi.

We provide a detailed analysis of the learning walks performed by Myrmecia croslandi ants at the nest during which they acquire visual information on its location. Most learning walks of 12 individually marked naïve ants took place in the morning with a narrow time window separating the first two learning walks, which most often occurred on the same day. Naïve ants performed between two and seven walks over up to four consecutive days before heading out to forage. On subsequent walks, naïve ants tend to explore the area around the nest in new compass directions. During learning walks, ants move along arcs around the nest while performing oscillating scanning movements. In a regular temporal sequence, the ants' gaze oscillates between the nest direction and the direction pointing away from the nest. Ants thus experience a sequence of views roughly across the nest and away from the nest from systematically spaced vantage points around the nest. Further, we show that ants leaving the nest for a foraging trip often walk in an arc around the nest on the opposite side to the intended foraging direction, performing a scanning routine indistinguishable from that of a learning walk. These partial learning walks are triggered by disturbance around the nest and may help returning ants with reorienting when overshooting the nest, which they frequently do. We discuss what is known about learning walks in different ant species and their adaptive significance for acquiring robust navigational memories.

Miniaturisation decreases visual navigational competence in ants.

Evolution of a smaller body size in a given lineage, called miniaturisation, is commonly observed in many animals including ants. It affects various morphological features and is hypothesised to result in inferior behavioural capabilities, possibly owing to smaller sensory organs. To test this hypothesis, we studied whether reduced spatial resolution of compound eyes influences obstacle detection or obstacle avoidance in five different species of ants. We trained all ant species to travel to a sugar feeder. During their return journeys, we placed an obstacle close to the nest entrance. We found that ants with higher spatial resolution exited the corridor - the area between the two ends of the obstacle - on average 10 cm earlier, suggesting they detected the obstacle earlier in their path. Ants with the lowest spatial resolution changed their viewing directions only when they were close to the obstacle. We discuss the effects of miniaturisation on visual navigational competence in ants.