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.

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.

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.

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.

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.

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.

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.

The discerning predator: decision rules underlying prey classification by a mosquito-eating jumping spider.

Evarcha culicivora is an East African jumping spider that feeds indirectly on vertebrate blood by choosing blood-fed female Anopheles mosquitoes as prey. Previous studies have shown that this predator can identify its preferred prey even when restricted to using only visual cues. Here, we used lures and virtual mosquitoes to investigate the optical cues underlying this predator's prey-choice behaviour. We made lures by dissecting and then reconstructing dead mosquitoes, combining the head plus thorax with different abdomens. Depending on the experiment, lures were either moving or motionless. Findings from the lure experiments suggested that, for E. culicivora, seeing a blood-fed female mosquito's abdomen on a lure was a necessary, but not sufficient, cue by which preferred prey was identified, as cues from the abdomen needed to be paired with cues from the head and thorax of a mosquito. Conversely, when abdomens were not visible or were identical, spiders based their decisions on the appearance of the head plus thorax of mosquitoes, choosing prey with female characteristics. Findings from a subsequent experiment using animated 3D virtual mosquitoes suggest that it is specifically the mosquito's antennae that influence E. culicivora's prey-choice decisions. Our results show that E. culicivora uses a complex process for prey classification.

The role of numerical competence in a specialized predatory strategy of an araneophagic spider.

Although a wide range of vertebrates have been considered in research on numerical competence, little is known about the role of number-related decisions in the predatory strategies of invertebrates. Here, we investigate how numerical competence is expressed in a highly specialized predatory strategy adopted by the small juveniles of Portia africana when practicing communal predation, with the prey being another spider, Oecobius amboseli. Two or more P. africana juveniles sometimes settle by the same oecobiid nest and then share the meal after one individual captures the oecobiid. Experiments were designed to clarify how these predators use number-related cues in conjunction with non-numerical cues when deciding whether to settle at a nest. We used lures (dead spiders positioned in lifelike posture) arranged in a series of 24 different scenes defined by the type, configuration and especially number of lures. On the whole, our findings suggest that P. africana juveniles base settling decisions on the specific number of already settled conspecific juveniles at the nest and express a preference for settling when the number is one instead of zero, two or three. By varying the size of the already settled juveniles and their positions around the nest, we show that factors related to continuous variables and stimulus configuration are unlikely explanations for our findings.

Attending to detail by communal spider-eating spiders.

Communal predators may often need to make especially intricate foraging decisions, as a predator's success may depend on the actions of its neighbours. Here,we consider the decisions made by Portia africana, a jumping spider (Salticidae) that preys on other spiders, including Oecobius amboseli (Oecobiidae), a small prey spider that lives under small sheets of silk (nests) on the walls of buildings. P. africana juveniles settle near oecobiid nests and then ambush oecobiids as they leave or enter the nest. Two or more P. africana juveniles sometimes settle at the same nest and, when an oecobiid is captured, the P. africana juveniles may share the meal. We investigated the joining decisions made by naïve P. africana juveniles. Experiments were based on using lures (dead spiders positioned in lifelike posture) arranged in a series of 17 different scenes defined by the presence/absence of a nest, the lure types present and the configuration of the lures and the nest. Our findings imply that P. africana juveniles make remarkably precise predatory decisions, with the variables that matter including whether a nest is present, the identity of spiders inside and outside a nest and how spiders are positioned relative to each other and the nest.

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.

How blood-derived odor influences mate-choice decisions by a mosquito-eating predator.

Evarcha culicivora (Araneae, Salticidae) feeds indirectly on vertebrate blood by choosing, as preferred prey, bloodcarrying female mosquitoes. Mutual mate-choice behavior is also pronounced in this species. Here we show that, when E. culicivora feeds indirectly on blood, it acquires a diet-related odor that makes it more attractive to the opposite sex. The mate-choice decisions of the adults of both sexes were investigated in a series of experiments based on comparing how long the test spider remained close to the odor of one source spider on one day and to the odor of a different source spider on the following day. Four different maintenance diets for source spiders were used in these experiments: bloodfed female mosquitoes (Culicidae, Anopheles gambiae ss), sugar-fed female mosquitoes, male mosquitoes, and lake flies (Chironomidae, Nilodorum brevibucca). Both sexes of E. culicivora spent more time close to the odor of opposite-sex conspecifics that had been on a diet of bloodfed mosquitoes (blood diet) instead of any of the three nonblood diets. Opposite-sex conspecifics that had been on a nonblood diet became more attractive once they were switched to a blood diet. That the attractive odor from blood dissipates was shown when spiders became less attractive once they were switched to a nonblood diet or subjected to a fast. However, there was no evident preference for the odor of a same-sex conspecific on a blood diet instead of a lake fly diet. These findings are discussed in the context of sexual selection and sensory exploitation.

Olfaction-based anthropophily in a mosquito-specialist predator.

Evarcha culicivora is an unusual salticid spider because it feeds indirectly on vertebrate blood by choosing blood-carrying mosquitoes as preferred prey. Its preferred mosquitoes are Anopheles, the genus to which all human malaria vectors belong. Here, we show that human odour, which is known to be salient to malaria vectors, is also salient to the adults and juveniles of E. culicivora. Test spiders spent more time in the vicinity of a source of human odour (previously worn socks) when the alternative was unworn socks.

Olfactory search-image use by a mosquito-eating predator.

By choosing blood-carrying mosquitoes as prey, Evarcha culicivora, an East African salticid spider, specializes at feeding indirectly on vertebrate blood. It also has an exceptionally complex mate-choice system. An earlier study revealed that search-image use assists E. culicivora in finding prey and mates when restricted to using vision alone. Here we show that search-image use assists E. culicivora in finding prey and mates when restricted to using olfaction alone. After being primed with prey odour or mate odour (control: not primed with odour), spiders were transferred to an olfactometer designed to test ability to find a prey-odour or mate-odour source that was either 'cryptic' (i.e. accompanied by a masking odour source, Lantana camara) or 'conspicuous' (no L. camara odour). When tested with conspicuous odour, the identity of the priming odour had no significant effect on how many spiders found the odour source. However, when tested with cryptic odour, significantly more spiders found the odour source when primed with congruent odour and significantly fewer spiders found the odour source when primed with incongruent odour.

Specialized prey selection behavior of two East African assassin bugs, Scipinnia repax and Nagusta sp. that prey on social jumping spiders.

The prey choice behavior and predatory strategies of two East African assassin bugs, Scipinnia repax (Stäl 1961) and Nagusta sp. (Hemiptera: Reduviidae), were investigated in the field and the laboratory. Both of these species are from the subfamily Harpactorinae and specialize in eating spiders. They prey especially often on social jumping spiders (Salticidae) that build nest complexes (nests connected by silk) in vegetation near the shoreline of Lake Victoria. Both reduviid species associate with these nest complexes and prey on the resident salticids. Nagusta sp., but not S. repax, form groups on nest complexes with 2-3 individuals of Nagusta sometimes feeding together on a single salticid. In addition to social salticids, Nagusta sp. preys on Portia africana, an araneophagic salticid that often invades the same nest complexes. S. repax preys on salticid eggs and also on Nagusta. Although they avoid ants, Nagusta and especially S. repax prey on ant-mimicking salticids, suggesting that sensory modalities other than vision play a dominant role in prey detection.

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.

Aggressive use of Batesian mimicry by an ant-like jumping spider.

Batesian and aggressive mimicry are united by deceit: Batesian mimics deceive predators and aggressive mimics deceive prey. This distinction is blurred by Myrmarachne melanotarsa, an ant-like jumping spider (Salticidae). Besides often preying on salticids, ants are well defended against most salticids that might target them as potential prey. Earlier studies have shown that salticids identify ants by their distinctive appearance and avoid them. They also avoid ant-like salticids from the genus Myrmarachne. Myrmarachne melanotarsa is an unusual species from this genus because it typically preys on the eggs and juveniles of ant-averse salticid species. The hypothesis considered here is that, for M. melanotarsa, the distinction between Batesian and aggressive mimicry is blurred. We tested this by placing female Menemerus sp. and their associated hatchling within visual range of M. melanotarsa, its model, and various non-ant-like arthropods. Menemerus is an ant-averse salticid species. When seeing ants or ant mimics, Menemerus females abandoned their broods more frequently than when seeing non-ant-like arthropods or in control tests (no arthropods visible), as predicted by our hypothesis that resembling ants functions as a predatory ploy.

The meaning of predatory specialization as illustrated by Aelurillus m-nigrum, an ant-eating jumping spider (Araneae: Salticidae) from Azerbaijan.

The distinctions between a predator's diet, its prey-choice behaviour and its preference are illustrated in a study of Aelurillus m-nigrum Kulczyn'ski, a salticid spider from Azerbaijan. The natural diet of A. m-nigrum was determined from records of individuals feeding in the field (N=58). Ten arthropod orders were represented. Nine were from the class Insecta (Coleoptera, Collembola, Diptera, Heteroptera, Homoptera, Hymenoptera, Lepidoptera, Orthoptera, Psocoptera) and one from the class Arachnida (Araneae). Of 50 insects among the prey, 21 (42%) were Hymenoptera, with ants (family Formicidae) alone accounting for 31% of all prey records. Although the majority (69%) of the natural prey were not ants, results from prey-choice testing in the laboratory implied that A. m-nigrum preferred ants as prey. However, this preference was evident only when the testing environment included sand and a small stone. Our findings illustrate the importance of not conflating the concept of a predator's preference with the concept of a predator's natural diet and illustrate that physical features of a predator's habitat may be an important factor in influencing how strongly preference is expressed.