Spiders manipulate and exploit bioluminescent signals of fireflies.

Predators often search for prey while moving through the environment, but there are important exceptions, including the way sedentary predators sometimes rely on signals for drawing prey to within striking distance1,2. Some spiders, for instance, leave the remnants of previously-captured prey in their webs where they function as static lures that effectively attract a diverse array of additional prey3456. However, important questions remain concerning how specific the targeted prey may be and how dynamic, instead of static, signalling might be. With these questions as our rationale, we initiated research on Araneus ventricosus (L. Koch, 1878), an orb-weaving spider, as the predator and the firefly Abscondita terminalis males as the prey (Figure 1A-C). Using two lanterns situated on their abdomen (Figure 1D,F), A. terminalis males make female-attracting multi-pulse flash trains (Figure 1J), whereas sedentary females attract males by making single-pulse signals (Figure 1C,K) with a single lantern (Figure 1E,G). Drawing from extensive field observations, we propose that A. ventricosus practices deceptive interspecific communication by first ensnaring firefly males in its web and then predisposing the entrapped male fireflies to broadcast bioluminescent signals that deviate from female-attracting signals typically made by A. terminalis males and instead mimic the male-attracting signals typically made by females. The outcome is that the entrapped male fireflies broadcast false signals that lure more male fireflies into the web.

Spatial acuity-sensitivity trade-off in the principal eyes of a jumping spider: possible adaptations to a 'blended' lifestyle.

Jumping spiders (Salticidae) are diurnal visual predators known for elaborate, vision-mediated behaviour achieved through the coordinated work of four pairs of camera-type eyes. One pair ('principal' eyes) is responsible for colour and high spatial acuity vision, while three pairs ('secondary' eyes) are mostly responsible for motion detection. Based on its unusual capacity to visually discriminate specific prey in very low, but also under bright light settings, we investigated the structure of the principal and one pair of secondary eyes (antero-lateral eyes) of Cyrba algerina to determine how these eyes achieve the sensitivity, while maintaining spatial acuity, needed to sustain behaviour in low light. Compared to salticids that live in bright light, the principal eyes of C. algerina have a short focal length, and wide contiguous twin rhabdomeres that support optical pooling, overall favouring sensitivity (0.39 µm2), but without fully compromising acuity (12.4 arc min). The antero-lateral eye retinae have large receptors surrounded by pigment granules, providing effective shielding from scattered light. These adaptations may be beneficial for a xeric salticid species with a 'blended' lifestyle: generally living and hunting under stones in the dark, but sometimes venturing above them, in dramatically different light conditions.

Odour priming of a mosquito-specialist predator's vision-based detouring decisions.

A capacity to execute long detours that are planned ahead of time has cognitive implications pertaining to reliance on internal representation. Here we investigate the detouring behaviour of Evarcha culicivora, an East African salticid spider that specializes at preying on blood-carrying mosquitoes. The findings from our experiments are the first evidence of a salticid making detouring plans based on whether the path chosen leads to more preferred instead of less preferred prey, as well as the first evidence of olfactory priming effects on motivation and selective attention in the context of detouring. Test spiders began on top of a starting platform from which, in some trials, they could view lures on top of two poles and, in some trials, the odour of blood-carrying mosquitoes was also present. When odour was present and prey were visible, significantly more test spiders took a detour and chose a pole than when only odour was present (prey not visible) or when prey were visible but odour was absent. When odour was present, test spiders also significantly more often chose the pole holding a blood-carrying mosquito instead of the pole holding another prey type.

Arthropod Intelligence? The Case for Portia.

Macphail's "null hypothesis," that there are no differences in intelligence, qualitative, or quantitative, between non-human vertebrates has been controversial. This controversy can be useful if it encourages interest in acquiring a detailed understanding of how non-human animals express flexible problem-solving capacity ("intelligence"), but limiting the discussion to vertebrates is too arbitrary. As an example, we focus here on Portia, a spider with an especially intricate predatory strategy and a preference for other spiders as prey. We review research on pre-planned detours, expectancy violation, and a capacity to solve confinement problems where, in each of these three contexts, there is experimental evidence of innate cognitive capacities and reliance on internal representation. These cognitive capacities are related to, but not identical to, intelligence. When discussing intelligence, as when discussing cognition, it is more useful to envisage a continuum instead of something that is simply present or not; in other words, a continuum pertaining to flexible problem-solving capacity for "intelligence" and a continuum pertaining to reliance on internal representation for "cognition." When envisaging a continuum pertaining to intelligence, Daniel Dennett's notion of four Creatures (Darwinian, Skinnerian, Popperian, and Gregorian) is of interest, with the distinction between Skinnerian and Popperian Creatures being especially relevant when considering Portia. When we consider these distinctions, a case can be made for Portia being a Popperian Creature. Like Skinnerian Creatures, Popperian Creatures express flexible problem solving capacity, but the manner in which this capacity is expressed by Popperian Creatures is more distinctively cognitive.

Influence of seeing a red face during the male-male encounters of mosquito-specialist spiders.

Males of Evarcha culicivora, an East African jumping spider (Salticidae), have bright red faces. Here, we investigated how seeing a red face might influence a male's behaviour during encounters with another male. We applied black eyeliner to conceal the red on a male's face and measured the spectral properties of male faces with and without the eyeliner. Only the faces without eyeliner reflected in the long-wavelength range corresponding to red. In experiments over 2 days, where eyeliner was absent on the first day and present on the second, we compared how two groups of males responded to their mirror images. Face Group: eyeliner concealed their faces. Head Group: eyeliner was applied to the tops of the males' heads instead of on their faces. The males from both groups displayed to their mirror image as if it were a living same-sex conspecific. However, when they could see a red face, males in the face group escalated to higher levels of aggression to their mirror image and initiated displaying from farther away than when the red had been concealed. We also found that the influence of eyeliner was stronger for the face group than for the head group. These findings suggest that, when seeing a red face, E. culicivora males become more confident that the individual in view is another male.

Portia's capacity to decide whether a detour is necessary.

Proficiency at planning is known to be part of the exceptionally complex predatory repertoire of Portia, a genus of jumping spiders (Salticidae) that specialize in preying on other spiders. This includes proficiency at choosing between two detour routes, with only one leading to otherwise inaccessible prey. Less is known about Portia's proficiency at making strategic decisions pertaining to whether a detour is required or not. Using Portia africana, we investigated this by having lures (prey or leaf pieces) visible at the beginning of a trial but not later, and by using water to restrict P. africana's freedom of movement. A detour path was always present, but sometimes a causeway was also present, allowing direct access to lures. After seeing prey, P. africana more often took the causeway when present and, when absent, more often took the detour path. After seeing leaf pieces, P. africana never took the detour path.

Dim-light vision in jumping spiders (Araneae, Salticidae): identification of prey and rivals.

Jumping spiders (family Salticidae) are known for their intricate vision-based behavior during encounters with prey and conspecific individuals. This is achieved using eyes specialized for discerning fine detail, but there has been minimal research on the capacity that salticids might have for visual performance under low ambient light levels. Here, we investigated the capacity of two salticid species, Cyrba algerina from Portugal and Cyrbaocellata from Kenya, to perform two specific visual tasks under low ambient light levels. We used lures made from spiders and midges in prey-identification experiments and mirror images (virtual conspecifics) in rival-identification experiments. These experiments were implemented under a range of ambient light levels (234, 1.35, 0.54, 0.24 cd m-2). In most instances, Calgerina and Cocellata were proficient at performing both of these visual tasks when ambient light was 234 and 1.35 cd m-2, and a minority performed these tasks at 0.54 cd m-2, but none succeeded when the light level was 0.24 cd m-2Cyrbaalgerina and C. ocellata showed vision-based discrimination under low ambient light levels previously associated with nocturnal species.

Lateral eyes direct principal eyes as jumping spiders track objects.

One way of circumventing the functional tradeoffs on eye design [1,2] is to have different eyes for different tasks. For example, jumping spiders (Salticidae), known for elaborate, visually guided courtship and predatory behavior [3], view the same object simultaneously with two of their four pairs of eyes: the antero-lateral eyes (ALEs) and the principal eyes (reviewed in [2]; Figure 1A). The ALEs, with immobile lenses and retinas, wide fields of view, and hyperacute sensitivity to moving stimuli [4], are structurally distinct from the principal eyes, which have the best spatial acuity known for terrestrial invertebrates and can discern fine details of stationary objects [5]. Behind the immobile corneal lenses of the principal eyes are miniature, boomerang-shaped retinas with correspondingly small fields of view (Figure 1B). The principal-eye visual fields are greatly expanded and overlap because of eye movements: these retinas are at the proximal ends of long, moveable tubes within the spider's cephalothorax [6]. By designing and using a specialized eyetracker, we tested whether principal-eye gaze direction is influenced by what the ALEs see. The principal eyes scanned stationary objects regardless of whether the ALEs were masked, but only when the ALEs were unmasked did the principal eyes smoothly track moving disks. The principal eyes, with high acuity but a narrow field of view, can thus precisely target moving stimuli, but only with the guidance of the secondary eyes.

When it looks and walks like an ant.

Some jumping spiders (family Salticidae) bear a striking resemblance to ants, a dangerous type of prey, both in terms of their appearance and in terms of how they move. Recent research has taken important steps toward determining whether predators categorize these spiders as ants on the basis of the way they move.

Representation of different exact numbers of prey by a spider-eating predator.

Our objective was to use expectancy-violation methods for determining whether Portia africana, a salticid spider that specializes in eating other spiders, is proficient at representing exact numbers of prey. In our experiments, we relied on this predator's known capacity to gain access to prey by following pre-planned detours. After Portia first viewed a scene consisting of a particular number of prey items, it could then take a detour during which the scene went out of view. Upon reaching a tower at the end of the detour, Portia could again view a scene, but now the number of prey items might be different. We found that, compared with control trials in which the number was the same as before, Portia's behaviour was significantly different in most instances when we made the following changes in number: 1 versus 2, 1 versus 3, 1 versus 4, 2 versus 3, 2 versus 4 or 2 versus 6. These effects were independent of whether the larger number was seen first or second. No significant effects were evident when the number of prey changed between 3 versus 4 or 3 versus 6. When we changed prey size and arrangement while keeping prey number constant, no significant effects were detected. Our findings suggest that Portia represents 1 and 2 as discrete number categories, but categorizes 3 or more as a single category that we call 'many'.

Ontogenetic shift in plant-related cognitive specialization by a mosquito-eating predator.

Evarcha culicivora, an East African salticid spider, is a mosquito specialist and it is also a plant specialist, with juveniles visiting plants primarily for acquiring nectar meals and adults visiting plants primarily as mating sites. The hypothesis we consider here is that there are ontogenetic shifts in cognition-related responses by E. culicivora to plant odour. Our experiments pertain to cross-modality priming effects in three specific contexts: executing behaviour that we call the 'visual inspection of plants' (Experiment 1), adopting selective visual attention to specific visual targets (Experiment 2) and becoming prepared to respond rapidly to specific visual targets (Experiment 3). Our findings appear not to be a consequence of salient odours in general elevating E. culicivora's motivation to respond to salient visual stimuli. Instead, effects were specific to particular odours paired with particular visual targets, with the salient volatile plant compounds being caryophyllene and humulene. We found evidence that prey odour primes juveniles and adults to respond to seeing specifically prey, mate odour primes adults to respond to seeing specifically mates and plant odour primes juveniles to respond to seeing specifically flowers. However, plant odour appears to prime adults to respond to seeing specifically a mate associated with a plant.

The execution of planned detours by spider-eating predators.

Many spiders from the salticid subfamily Spartaeinae specialize at preying on other spiders and they adopt complex strategies when targeting these dangerous prey. We tested 15 of these spider-eating spartaeine species for the capacity to plan detours ahead of time. Each trial began with the test subject on top of a tower from which it could view two boxes: one containing prey and the other not containing prey. The distance between the tower and the boxes was too far to reach by leaping and the tower sat on a platform surrounded by water. As the species studied are known to avoid water, the only way they could reach the prey without getting wet was by taking one of two circuitous walkways from the platform: one leading to the prey ('correct') and one not leading to the prey ('incorrect'). After leaving the tower, the test subject could not see the prey and sometimes it had to walk past the incorrect walkway before reaching the correct walkway. Yet all 15 species chose the correct walkway significantly more often than the incorrect walkway. We propose that these findings exemplify genuine cognition based on representation.

Convergence between a mosquito-eating predator's natural diet and its prey-choice behaviour.

On the basis of 1115 records of Evarcha culicivora feeding in the field, we can characterize this East African jumping spider (Salticidae) as being distinctively stenophagic. We can also, on the basis of laboratory prey-choice experiments, characterize E. culicivora as having a specialized prey-classification system and a hierarchy of innate preferences for various categories of mosquitoes and other arthropods. Prey from the field belonged to 10 arthropod orders, but 94.5% of the prey records were dipterans. Mosquitoes were the dominant prey (80.2% of the records), with the majority (82.9%) of the mosquitoes being females, and thereafter midges were the most common prey (9.2% of the records). Preference profiles that were determined from experiments showed strong convergence with natural diet in some, but not all, instances. In experiments, E. culicivora adults appeared to distinguish between six prey categories and juveniles between seven, with blood-carrying anopheline female mosquitoes being ranked highest in preference. For adults, this was followed by blood-carrying culicine female mosquitoes and then anopheline female mosquitoes not carrying blood, but these two preferences were reversed for juveniles. Moreover, for juveniles, but not for adults, anopheline male mosquitoes seem to be a distinct prey category ranked in preference after blood-carrying culicine females and, for both adults and juveniles, preference for midges is evident when the alternatives are not mosquitoes. These findings illustrate the importance of going beyond simply specifying preferred prey categories when characterizing predators as 'specialized' and a need to make clear conceptual distinctions between a predator's natural diet, the prey categories that are relevant to the predator, and the predator's prey-choicebehaviour.

Rapid nectar-meal effects on a predator's capacity to kill mosquitoes.

Using Evarcha culicivora, an East African jumping spider (Salticidae), we investigate how nectar meals function in concert with predation specifically at the juvenile stage between emerging from the egg sac and the first encounter with prey. Using plants and using artificial nectar consisting of sugar alone or sugar plus amino acids, we show that the plant species (Lantana camara, Ricinus communis, Parthenium hysterophorus), the particular sugars in the artificial nectar (sucrose, fructose, glucose, maltose), the concentration of sugar (20%, 5%, 1%) and the duration of pre-feeding fasts (3 days, 6 days) influence the spider's prey-capture proficiency on the next day after the nectar meal. However, there were no significant effects of amino acids. Our findings suggest that benefits from nectar feeding are derived primarily from access to particular sugars, with fructose and sucrose being the most beneficial, glucose being intermediate and maltose being no better than a water-only control.

Solving a novel confinement problem by spartaeine salticids that are predisposed to solve problems in the context of predation.

Intricate predatory strategies are widespread in the salticid subfamily Spartaeinae. The hypothesis we consider here is that the spartaeine species that are proficient at solving prey-capture problems are also proficient at solving novel problems. We used nine species from this subfamily in our experiments. Eight of these species (two Brettus, one Cocalus, three Cyrba, two Portia) are known for specialized invasion of other spiders' webs and for actively choosing other spiders as preferred prey ('araneophagy'). Except for Cocalus, these species also use trial and error to derive web-based signals with which they gain dynamic fine control of the resident spider's behaviour ('aggressive mimicry').The ninth species, Paracyrba wanlessi, is not araneophagic and instead specializes at preying on mosquitoes. We presented these nine species with a novel confinement problem that could be solved by trial and error. The test spider began each trial on an island in a tray of water, with an atoll surrounding the island. From the island, the spider could choose between two potential escape tactics (leap or swim), but we decided at random before the trial which tactic would fail and which tactic would achieve partial success. Our findings show that the seven aggressive-mimic species are proficient at solving the confinement problem by repeating 'correct' choices and by switching to the alternative tactic after making an 'incorrect' choice. However, as predicted, there was no evidence of C. gibbosus or P. wanlessi, the two non-aggressive-mimic species, solving the confinement problem. We discuss these findings in the context of an often-made distinction between domain-specific and domain-general cognition.

Cross-modality effects of prey odour during the intraspecific interactions of a mosquito-specialist predator.

One of the predictions from evolutionary game theory is that individuals will increase their willingness (i.e., become primed) to escalate aggression when they detect the presence of a limiting resource. Here we test this prediction in the context of prey odour priming escalation decisions during vision-based encounters by Evarcha culicivora. This East African jumping spider (Salticidae) feeds indirectly on vertebrate blood by actively choosing blood-carrying female mosquitoes as preferred prey. Unlike many salticid species, it also expresses pronounced mutual mate choice. As predicted, we show here that, in the presence of odour from their preferred prey, both sexes of E. culicivora escalate during vision-based same-sex encounters. This is further evidence that the odour of blood-carrying mosquitoes is salient to this salticid. For both sexes of E. culicivora, this particular prey may be a resource that matters in the context of intrasexual selection.

Specialised use of working memory by Portia africana, a spider-eating salticid.

Using expectancy-violation methods, we investigated the role of working memory in the predatory strategy of Portia africana, a salticid spider from Kenya that preys by preference on other spiders. One of this predator's tactics is to launch opportunistic leaping attacks on to other spiders in their webs. Focussing on this particular tactic, our experiments began with a test spider on a ramp facing a lure (dead prey spider mounted on a cork disc) that could be reached by leaping. After the test spider faced the lure for 30 s, we blocked the test spider's view of the lure by lowering an opaque shutter before the spider leapt. When the shutter was raised 90 s later, either the same lure came into view again (control) or a different lure came into view (experimental: different prey type in same orientation or same prey type in different orientation). We recorded attack frequency (number of test spiders that leapt at the lure) and attack latency (time elapsing between shutter being raised and spiders initiating a leap). Attack latencies in control trials were not significantly different from attack latencies in experimental trials, regardless of whether it was prey type or prey orientation that changed in the experimental trials. However, compared with test spiders in the no-change control trials, significantly fewer test spiders leapt when prey type changed. There was no significant effect on attack frequency when prey orientation changed. These findings suggest that this predator represents prey type independently of prey orientation.

Intricate predatory decisions by a mosquito-specialist spider from Malaysia.

Paracyrba wanlessi is a southeast Asian jumping spider (Salticidae) that lives in the hollow internodes of fallen bamboo and preys on the larvae, pupae and adults of mosquitoes. In contrast to Evarcha culicivora, an East African salticid that is also known for actively targeting mosquitoes as preferred prey, there was no evidence of P. wanlessi choosing mosquitoes on the basis of species, sex or diet. However, our findings show that P. wanlessi chooses mosquitoes significantly more often than a variety of other prey types, regardless of whether the prey are in or away from water, and regardless of whether the mosquitoes are adults or juveniles. Moreover, a preference for mosquito larvae, pupae and adults is expressed regardless of whether test spiders are maintained on a diet of terrestrial or aquatic prey and regardless of whether the diet includes or excludes mosquitoes. Congruence of an environmental factor (in water versus away from water) with prey type (aquatic versus terrestrial mosquitoes) appeared to be important and yet, even when the prey were in the incongruent environment, P. wanlessi continued to choose mosquitoes more often than other prey.

A COGNITIVE PERSPECTIVE ON AGGRESSIVE MIMICRY.

We use the term 'aggressive mimic' for predators that communicate with their prey by making signals to indirectly manipulate prey behaviour. For understanding why the aggressive mimic's signals work, it is important to appreciate that these signals interface with the prey's perceptual system, and that the aggressive mimic can be envisaged as playing mind games with its prey. Examples of aggressive mimicry vary from instances in which specifying a model is straight forward to instances where a concise characterisation of the model is difficult. However, the less straightforward examples of aggressive mimicry may be the more interesting examples in the context of animal cognition. In particular, there are spiders that prey on other spiders by entering their prey's web and making signals. Web invasion brings about especially intimate contact with their prey's perceptual system because the prey spider's web is an important component of the prey spider's sensory apparatus. For the web-invading spider, often there is also a large element of risk when practising aggressive mimicry because the intended prey is also a potential predator. This element of risk, combined with exceptionally intimate interfacing with prey perceptual systems, may have favoured the web-invading aggressive mimic's strategy becoming strikingly cognitive in character. Yet a high level of flexibility may be widespread among aggressive mimics in general and, on the whole, we propose that research on aggressive mimicry holds exceptional potential for advancing our understanding of animal cognition.

Mediation of a plant-spider association by specific volatile compounds.

Evarcha culicivora, an East African jumping spider (Salticidae), is the only spider for which there is evidence of innate olfactory affinity for particular plant species. Evarcha culicivora also actively chooses as preferred prey the females of Anopheles mosquitoes, and both sexes of Anopheles are known to visit plants for nectar meals. Here, we identified compounds present in the headspace of one of these species in Kenya, Lantana camara, and then used 11 of these compounds in olfactometer experiments. Our findings show that three terpenes [(E)-ß-caryophyllene, α-humulene and 1,8 cineole] can be discriminated by, and are salient to, E. culicivora. The spiders experienced no prior training with plants or the compounds we used. This is the first experimental demonstration of specific phytochemicals being innately attractive to a spider, a group normally characterized as predators.