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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

Compass cues used by a nocturnal bull ant, Myrmecia midas.

Ants use both terrestrial landmarks and celestial cues to navigate to and from their nest location. These cues persist even as light levels drop during the twilight/night. Here, we determined the compass cues used by a nocturnal bull ant, Myrmecia midas, in which the majority of individuals begin foraging during the evening twilight period. Myrmecia midas foragers with vectors of ≤5 m when displaced to unfamiliar locations did not follow the home vector, but instead showed random heading directions. Foragers with larger home vectors (≥10 m) oriented towards the fictive nest, indicating a possible increase in cue strength with vector length. When the ants were displaced locally to create a conflict between the home direction indicated by the path integrator and terrestrial landmarks, foragers oriented using landmark information exclusively and ignored any accumulated home vector regardless of vector length. When the visual landmarks at the local displacement site were blocked, foragers were unable to orient to the nest direction and their heading directions were randomly distributed. Myrmecia midas ants typically nest at the base of the tree and some individuals forage on the same tree. Foragers collected on the nest tree during evening twilight were unable to orient towards the nest after small lateral displacements away from the nest. This suggests the possibility of high tree fidelity and an inability to extrapolate landmark compass cues from information collected on the tree and at the nest site to close displacement sites.

Ocellar structure is driven by the mode of locomotion and activity time in Myrmecia ants.

Insects have exquisitely adapted their compound eyes to suit the ambient light intensity in the different temporal niches they occupy. In addition to the compound eye, most flying insects have simple eyes known as ocelli, which assist in flight stabilisation, horizon detection and orientation. Among ants, typically the flying alates have ocelli while the pedestrian workers lack this structure. The Australian ant genus Myrmecia is one of the few ant genera in which both workers and alates have three ocellar lenses. Here, we studied the variation in the ocellar structure in four sympatric species of Myrmecia that are active at different times of the day. In addition, we took advantage of the walking and flying modes of locomotion in workers and males, respectively, to ask whether the type of movement influences the ocellar structure. We found that ants active in dim light had larger ocellar lenses and wider rhabdoms compared with those in bright-light conditions. In the ocellar rhabdoms of workers active in dim-light habitats, typically each retinula cell contributed microvilli in more than one direction, probably destroying polarisation sensitivity. The organisation of the ocellar retina in the day-active workers and the males suggests that in these animals some cells are sensitive to the pattern of polarised skylight. We found that the night-flying males had a tapetum that reflects light back to the rhabdom, increasing their optical sensitivity. We discuss the possible functions of ocelli to suit the different modes of locomotion and the discrete temporal niches that animals occupy.

Head roll stabilisation in the nocturnal bull ant Myrmecia pyriformis: implications for visual navigation.

Ant foragers are known to memorise visual scenes that allow them to repeatedly travel along idiosyncratic routes and to return to specific places. Guidance is provided by a comparison between visual memories and current views, which critically depends on how well the attitude of the visual system is controlled. Here we show that nocturnal bull ants stabilise their head to varying degrees against locomotion-induced body roll movements, and this ability decreases as light levels fall. There are always un-compensated head roll oscillations that match the frequency of the stride cycle. Head roll stabilisation involves both visual and non-visual cues as ants compensate for body roll in complete darkness and also respond with head roll movements when confronted with visual pattern oscillations. We show that imperfect head roll control degrades navigation-relevant visual information and discuss ways in which navigating ants may deal with this problem.

Light and dark adaptation mechanisms in the compound eyes of Myrmecia ants that occupy discrete temporal niches.

Ants of the Australian genus Myrmecia partition their foraging niche temporally, allowing them to be sympatric with overlapping foraging requirements. We used histological techniques to study the light and dark adaptation mechanisms in the compound eyes of diurnal (Myrmecia croslandi), crepuscular (M. tarsata, M. nigriceps) and nocturnal ants (M. pyriformis). We found that, except in the day-active species, all ants have a variable primary pigment cell pupil that constricts the crystalline cone in bright light to control for light flux. We show for the nocturnal M. pyriformis that the constriction of the crystalline cone by the primary pigment cells is light dependent whereas the opening of the aperture is regulated by an endogenous rhythm. In addition, in the light-adapted eyes of all species, the retinular cell pigment granules radially migrate towards the rhabdom, a process that in both the day-active M. croslandi and the night-active M. pyriformis is driven by ambient light intensity. Visual system properties thus do not restrict crepuscular and night-active ants to their temporal foraging niche, while day-active ants require high light intensities to operate. We discuss the ecological significance of these adaptation mechanisms and their role in temporal niche partitioning.

Three spectrally distinct photoreceptors in diurnal and nocturnal Australian ants.

Ants are thought to be special among Hymenopterans in having only dichromatic colour vision based on two spectrally distinct photoreceptors. Many ants are highly visual animals, however, and use vision extensively for navigation. We show here that two congeneric day- and night-active Australian ants have three spectrally distinct photoreceptor types, potentially supporting trichromatic colour vision. Electroretinogram recordings show the presence of three spectral sensitivities with peaks (λmax) at 370, 450 and 550 nm in the night-active Myrmecia vindex and peaks at 370, 470 and 510 nm in the day-active Myrmecia croslandi. Intracellular electrophysiology on individual photoreceptors confirmed that the night-active M. vindex has three spectral sensitivities with peaks (λmax) at 370, 430 and 550 nm. A large number of the intracellular recordings in the night-active M. vindex show unusually broad-band spectral sensitivities, suggesting that photoreceptors may be coupled. Spectral measurements at different temporal frequencies revealed that the ultraviolet receptors are comparatively slow. We discuss the adaptive significance and the probability of trichromacy in Myrmecia ants in the context of dim light vision and visual navigation.

Three-dimensional models of natural environments and the mapping of navigational information.

Much evidence has accumulated in recent years, demonstrating that the degree to which navigating insects rely on path integration or landmark guidance when displaced depends on the navigational information content of their specific habitat. There is thus a need to quantify this information content. Here we present one way of achieving this by constructing 3D models of natural environments using a laser scanner and purely camera-based methods that allow us to render panoramic views at any location. We provide (1) ground-truthing of such reconstructed views against panoramic images recorded at the same locations; (2) evidence of their potential to map the navigational information content of natural habitats; (3) methods to register these models with GPS or with stereo camera recordings and (4) examples of their use in reconstructing the visual information available to walking and flying insects. We discuss the current limitations of 3D modelling, including the lack of spectral and polarisation information, but also the opportunities such models offer to map the navigational information content of natural habitats and to test visual navigation algorithms under 'real-life' conditions.

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.

Homing abilities of the Australian intertidal ant Polyrhachis sokolova.

The pressure of returning to and locating the nest after a successful foraging trip is immense in ants. To find their way back home, ants use a number of different strategies (e.g. path integration, trail following) and rely on a range of cues (e.g. pattern of polarised skylight, landmark panorama) available in their environment. How ants weigh different cues has been a question of great interest and has primarily been addressed in the desert ants from Africa and Australia. We here identify the navigational abilities of an intertidal ant, Polyrhachis sokolova, that lives on mudflats where nests and foraging areas are frequently inundated with tidal water. We find that these solitary foraging ants rely heavily on visual landmark information for navigation, but they are also capable of path integration. By displacing ants with and without vector information at different locations within the local familiar territory, we created conflicts between information from the landmarks and information from the path integrator. The homing success of full-vector ants, compared with the zero-vector ants, when displaced 5 m behind the feeder, indicate that vector information had to be coupled with landmark information for successful homing. To explain the differences in the homing abilities of ants from different locations we determined the navigational information content at each release station and compared it with that available at the feeder location. We report here the interaction of multiple navigation strategies in the context of the information content in the environment.