Similar yet different: differential response of a praying mantis to ant‐mimicking spiders

Batesian mimics typically dupe visual predators by resembling noxious or deadly model species. Ants are unpalatable and dangerous to many arthropod taxa, and are popular invertebrate models in mimicry studies. Ant mimicry by spiders, especially jumping spiders, has been studied and researchers have examined whether visual predators can distinguish between the ant model, spider mimic and spider non‐mimics. Tropical habitats harbour a diverse community of ants, their mimics and predators. In one such tripartite mimicry system, we investigated the response of an invertebrate visual predator, the ant‐mimicking praying mantis (Euantissa pulchra), to two related ant‐mimicking spider prey of the genus Myrmarachne, each closely mimicking its model ant species. We found that weaver ants (Oecophylla smaragdina) were much more aggressive than carpenter ants (Camponotus sericeus) towards the mantis. Additionally, mantids exhibited the same aversive response towards ants and their mimics. More importantly, mantids approached carpenter ant‐mimicking spiders significantly more than often that they approached weaver ant‐mimicking spiders. Thus, in this study, we show that an invertebrate predator, the praying mantis, can indeed discriminate between two closely related mimetic prey. The exact mechanism of the discrimination remains to be tested, but it is likely to depend on the level of mimetic accuracy by the spiders and on the aggressiveness of the ant model organism.     

The adaptive bases of ant-mimicry in a neotropical aphantochilid spider (Araneae: Aphantochilidae)

The aphantochilid spider Aphanlochilus rogersi accurately mimics black ants of tribe Cephalotini, and is commonly found in the neighbourhood of its models' nests. The mimic seems to be a specialized predator of this type of ant, rejecting any insect offered as prey other than cephalotines. In the field, A. rogersi was observed preying on the model species Zacryptocerus pusillus. In captivity, the spider preyed on the models Z. pusillus and Z. depressus, as well as on the yellow non-model Z. clypeatus. Recognition of correct prey by A. rogersi appears to be based primarily on visual and tactile stimuli. Capturing ant prey from behind was the most common attack tactic observed in A. rogersi, and is probably safer than frontal attacks, as in this case the spider can be bitten on the legs before the ant is immobilized. Aphanlochilus rogersi, when feeding on the hard-bodied ant models, uses the ant corpses as a ‘protective shield’ against patrolling ants of the victim's colony and resembles an ant carrying a dead companion. Certain types of mimetic traits in A. rogersi (close similarity to ant models in integument texture and pilosity of body and legs), together with ‘shielding behaviour’, are thought to function as ant-deceivers, facilitating the obligatory intimate contact the mimic must make with cephalotines in order to capture a prey among other ants. The close similarity in the arrangement of dorsal spines, body shape, integument brightness and locomotion, together with antennal illusion, is regarded as a strategy of A. rogersi for deceiving visually-hunting predators that avoid its sharp spined ant models. It is proposed that ant-mimicry in A. rogersi has both an aggressive and a Batesian adaptive component, and evolved as a result of combined selective pressures exerted both by Cephalotini ant models (through defensive behaviour towards the mimics which attack them) and predators that avoid cephalotines (through predatory behaviour toward imperfect mimics). This suggestion is schematized and discussed in terms of two tripartite mimicry systems.     

Can ant‐eating Zodarion spiders (Araneae: Zodariidae) develop on a diet optimal for euryphagous arthropod predators?

Abstract Little attention is paid to the behavioural and physiological adaptations of ant‐eating predators. It is expected that there should be a strong selection for traits related to prey handling, leading to the evolution of morphological, behavioural and nutritional adaptations. Such adaptations may then entail trade‐offs in handling and utilization of alternative prey. To investigate behavioural as well as nutritional adaptations and the occurrence of the corresponding trade‐offs in two ant‐eating spiders of the genus Zodarion [Zodarion atlanticum Pekár & Cardoso and Zodarion germanicum (C. L. Koch)], spiders are reared on two diets: ants (i.e. their preferred prey) and fruit flies (i.e. an alternative prey that is nutritionally optimal for euryphagous spiders). Food consumption is observed and several fitness‐related life‐history parameters are measured. Although spiders readily accept ants, more than one‐third of 35 spiders refuse to consume fruit flies and starve. Furthermore, severe hunger does not induce these individuals to accept fruit flies. Starving spiders die before moulting to the second stadium. Spiders that eat fruit flies increase only little and slowly in weight, and all of these die during the first two stadia. By contrast, spiders on an ant diet increase dramatically in weight, and develop up to the fourth stadium. These data indicate that fruit flies are not suitable for Zodarion, supporting the hypothesis that there are behavioural and nutritional trade‐offs. Taking into account the results of previous studies, it is suggested that nutritional trade‐offs are generally important for stenophagous spiders.     

Pre-adaptive shift of a native predator (Araneae, Zodariidae) to an abundant invasive ant species (Hymenoptera, Formicidae)

Invasive species often displace native species and can affect ecological processes in invaded habitats. If invasive species become abundant, changes in prey availability may be particularly harmful to specialist predators. The Argentine ant, Linepithema humile Mayr, is an important invasive species on nearly all continents. Spiders of the genus Zodarion are specialised ant-eating predators native to the Mediterranean yet it is unknown if they can exploit invasive ant species. Here we studied spatial and temporal abundance of this invasive ant and the native spider, Zodarion cesari Pekár, during 4?years in four citrus groves. Circadian activity of both spiders and ants, and capture efficiency and prey specificity of the predator were also evaluated. The abundance of Z. cesari was strongly correlated to L. humile abundance. The predatory activity of spiders varied seasonally with differences on the relative frequency of spiders capturing ants depending on the time of the year. In laboratory, Z. cesari displayed most efficient capture upon the native ant Tapinoma nigerrimum (Nylander) and the invasive ant L. humile in comparison with five other native ant species. These results demonstrate that the native spider Z. cesari is successfully exploiting the invasive ant species L. humile and is likely a locally monophagous predator. We suggest that Z. cesari shifted away from native T. nigerrimum post invasion as both ant species are phylogenetically related and of similar size.     

Innate aversion to ants (Hymenoptera: Formicidae) and ant mimics: experimental findings from mantises (Mantodea)

Field data suggest that ants may be important predators of mantises which, in turn, may be important predators of jumping spiders (Salticidae). Using a tropical fauna from the Philippines as a case study, the reactions of mantises to ants, myrmecomorphic salticids (i.e. jumping spiders that resemble ants) and ordinary salticids (i.e. jumping spiders that do not resemble ants) were investigated in the laboratory. Three mantis species ( Loxomantis sp., Orthodera sp., and Statilia sp.) were tested with ten ant species, five species of Myrmarachne (i.e. myrmecomorphic salticids), and 23 ordinary salticid species. Two categories of the myrmecomorphic salticids were recognized: (1) 'typical Myrmarachne ' (four species with a strong resemblance to ants) and (2) Myrmarachne bakeri (a species with less strong resemblance to ants). Ants readily killed mantises in the laboratory, confirming that, for the mantises studied, ants are dangerous. In alternate-day testing, the mantises routinely preyed on the ordinary salticids, but avoided ants. The mantises reacted to myrmecomorphic salticids similarly to how they reacted to ants (i.e. myrmecomorphic salticids appear to be, for mantises, Batesian mimics of ants). Although myrmecomorphic salticids were rarely eaten, M . bakeri was eaten more often than typical Myrmarachne . Because the mantises had no prior experience with ants, ant mimics or ordinary salticids, our findings suggest that mantises have an innate aversion to attacking ants and that this aversion is generalized to myrmecomorphic salticids even in the absence of prior experience with ants. © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 23–32.     

Do Malaysian Myrmarachne associate with particular species of ant?

Ant-mimicry has evolved in numerous families of spiders. Although some mimics resemble ants very precisely in their morphology and behaviour, others have only a superficial resemblance to ants. In the present study, each of at least seven (and probably ten) out of 11 species of Myrmarachne from peninsular Malaysia associates with one particular species or genus of ant that it specifically resembles; these are therefore 'good' or 'specific' mimics. Myrmarachne malayana lives in the foraging ranges of a variety of ants and shows no specific resemblance to any one genus of ant, and it is best considered as a 'poor' or 'general' mimic. A species of Castianeira (Corinnidae) with a much less precise similarity to ants (a 'poor' mimic) was associated with Polyrhachis ants. It had previously been suggested that Orsima ichneumon (Salticidae) is an ant or insect mimic in reverse; in the present study, it was associated with Polyrhachis ants but is not considered to be an ant-mimic. Two recent theoretical models show how a poor ant-mimic may be better protected than a good mimic under certain circumstances. These data provide some support for the multimodel hypothesis, although not for Sherratt's hypothesis. However, a realistic test of these hypotheses requires more information than that provided here on both mimics and models.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 645–653.     

Biology and behaviour of the neotropical ant-mimicking spider Aphantochilus rogersi (Araneae: Aphantochilidae): nesting, maternal care and ontogeny of ant-hunting techniques

Aphantochilus rogersi is an ant-mimicking spider that preys exclusively on cephalotine ants. The spiders oviposit in close proximity to nests of the model ant Zacryptocerus pusillus , and emergent spiderlings tend to remain in the vicinity of natal egg sacs. Females of A. rogersi actively defend their egg sacs against approaching workers of Z. pusillus , but the latter may sometimes destroy the eggs. Feeding specialization on these ants is confirmed by more than 300 observation of young and adult A. rogersi carrying ant corpses in the field. Although A. rogersi possesses several behavioural traits which may reduce the risk of being injured by ants during subjugation, field and laboratory observations showed that social defence by Z. pusillus may cause mutilation to the spiders. Tests in captivity revealed an ontogenetic change in the prey-capture techniques employed by A. rogersi. Early-instar spiderlings can apparently only seize the ant's petiole tightly if they are able to approach the ant from the front. As the ant is paralysed, the spiderling positions itself vertically in relation to the substratum. Larger spiders, on the other hand, attack ants most frequently from behind, and seem better equipped to seize the ant's petiole firmly with their larger chelicerae. Owing to their greater strength, late-instar spiders are able to lift the struggling ant aloft. The selection of a suitable oviposition site, the mother's ability to defend herself and the eggs from nearby ants, and the capacity to capture and subdue ants safely from emergence to maturity, are regarded as crucial traits inherent in the mimetic and feeding specialization by A. rogersi.     

The multiple disguises of spiders: web colour and decorations, body colour and movement

Diverse functions have been assigned to the visual appearance of webs, spiders and web decorations, including prey attraction, predator deterrence and camouflage. Here, we review the pertinent literature, focusing on potential camouflage and mimicry. Webs are often difficult to detect in a heterogeneous visual environment. Static and dynamic web distortions are used to escape visual detection by prey, although particular silk may also attract prey. Recent work using physiological models of vision taking into account visual environments rarely supports the hypothesis of spider camouflage by decorations, but most often the prey attraction and predator confusion hypotheses. Similarly, visual modelling shows that spider coloration is effective in attracting prey but not in conveying camouflage. Camouflage through colour change might be used by particular crab spiders to hide from predator or prey on flowers of different coloration. However, results obtained on a non-cryptic crab spider suggest that an alternative function of pigmentation may be to avoid UV photodamage through the transparent cuticle. Numerous species are clearly efficient locomotory mimics of ants, particularly in the eyes of their predators. We close our paper by highlighting gaps in our knowledge.     

Comparative study of the femoral organ in Zodarion spiders (Araneae: Zodariidae)

The femoral organ of Zodarion spiders has not been investigated in detail yet. In this study we describe the external and internal structure of this organ. The organ is situated at the distal tip of the femora of all the legs during all developmental stages. The size of the organ (expressed as the number of hairs) increased with the ontogenetic development of Zodarion species. The organ was confirmed to occur in both sexes of all 47 Zodarion species examined. It is possibly present in all species of this genus. The size of the organ increased with the size of the species. A comparative anatomical study was performed in juveniles and adults of both sexes of Zodarion rubidum, and females of both Z. cyrenaicum and Z. jozefienae. The femoral organ represents an exocrine gland composed of a group of secretory cells located below the epidermis. Each gland cell is connected with the leg surface by a single duct. The ducts run in intercellular spaces and specialised canal cells are lacking. The structure of the secretory cells, namely the abundance of smooth endoplasmic reticulum, suggests that the gland produces a volatile compound(s). The composition and the role of the secretion, however, remains unknown.     

Salticid predation as one potential driving force of ant mimicry in jumping spiders

Many spiders possess myrmecomorphy, and species of the jumping spider genus Myrmarachne exhibit nearly perfect ant mimicry. Most salticids are diurnal predators with unusually high visual acuity that prey on various arthropods, including conspecifics. In this study, we tested whether predation pressure from large jumping spiders is one possible driving force of perfect ant mimicry in jumping spiders. The results showed that small non-ant-mimicking jumping spiders were readily treated as prey by large ones (no matter whether heterospecific or conspecific) and suffered high attack and mortality rates. The size difference between small and large jumping spiders significantly affected the outcomes of predatory interactions between them: the smaller the juvenile jumping spiders, the higher the predation risk from large ones. The attack and mortality rates of ant-mimicking jumping spiders were significantly lower than those of non-ant-mimicking jumping spiders, indicating that a resemblance to ants could provide protection against salticid predation. However, results of multivariate behavioural analyses showed that the responses of large jumping spiders to ants and ant-mimicking salticids differed significantly. Results of this study indicate that predation pressure from large jumping spiders might be one selection force driving the evolution of nearly perfect myrmecomorphy in spiders and other arthropods.     

Poor Display Repertoire, Tolerance and Kleptobiosis: Results of Specialization in an Ant-Eating Spider (Araneae, Zodariidae)

The agonistic display repertoire of myrmecophagous Zodarion rubidum has five displays. This is fewer than in other spiders, which is a result of the short time spent in contests (4 s). Such a short duration seems to be an adaptation to living among foraging ants, which are dangerous to spiders. The interaction procedure was markedly affected by the presence of preyimmobilized ant. Contests between individuals without prey, or each holding prey, were usually resolved by leg waving. But contests between an individual without and an individual with prey escalated to more aggressive levels. Nevertheless, spiders were never observed to harm or cannibalize one another. Absence of cannibalism is explained as a result of diet specialization: only ants elicit a predatory behavior and provide Zodarion spiders with optimal nutrients. Some spiders used kleptobiosis to gain ants. They first tried to gain immobilized prey aggressively and if failed they adopted a stealthy tactic and shared the prey with the owner. Kleptobiosis is an alternative foraging strategy for Zodarion spiders as it reduces risks associated with hunting dangerous ants.     

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.     

Out of the Frying Pan and into the Fire: a Novel Trade-Off for Batesian Mimics

A mimicry system was investigated in which the models were ants (Formicidae) and both the mimics and the predators were jumping spiders (Salticidae). By using motionless lures in simultaneous‐presentation prey‐choice tests, how the predators respond specifically to the static appearance of ants and ant mimics was determined. These findings suggest a rarely considered adaptive trade‐off for Batesian mimics of ants. Mimicry may be advantageous when it deceives ant‐averse potential predators, but disadvantageous in encounters with ant‐eating specialists. Nine myrmecophagic (ant‐eating) species (from Africa, Asia, Australia and North America) and one araneophagic (spider‐eating) species (Portia fimbriata from Queensland) were tested with ants (five species), with myrmecomorphic (ant‐like) salticids (six species of Myrmarachne) and with non‐ant‐like prey (dipterans and ordinary salticids). The araneophagic salticid chose an ordinary salticid and chose flies significantly more often than ants. Portia fimbriata also chose the ordinary salticid and chose flies significantly more often than myrmecomorphic salticids. However, there was no significant difference in how P. fimbriata responded to ants and to myrmecomorphic salticids. The myrmecophagic salticids chose ants and chose myrmecomorphic salticids significantly more often than ordinary salticids and significantly more often than flies, but myrmecophagic salticids did not respond significantly differently to myrmecomorphic salticids and ants.     

The effect of a single colony of the red wood ant,Formica polyctena,on the spider fauna (Araneae) of a beech forest floor

Summary The predation on spiders in a forest ecosystem by a colony of red wood ants, Formica polyctena, was estimated using a barrier to isolate the colony. Of the ants' total prey, 4.6% were spiders. In order to estimate the effect of F. polyctena within their hunting area on the spider population, the spiders' population density was studied inside and outside the hunting area. Samples of the forest floor were taken, spider webs were counted and pitfall traps were used. No significant difference was found in density or composition of the spider fauna inside and outside the hunting area.     

Is inaccurate mimicry ancestral to accurate in myrmecomorphic spiders (Araneae)?

Batesian mimicry, in which a palatable organism resembles an unpalatable model, is widespread among taxa. Batesian mimics can be classified based on their level of accuracy (inaccurate or accurate). Using data on defensive strategies in more than 1000 species of spiders I investigated whether inaccurate myrmecomorphy is ancestral to accurate myrmecomorphy. I classified 233 myrmecomorphic species into four accuracy levels based on morphology, from poor inaccurate mimics to very accurate ones. I found that myrmecomorphy has evolved independently in 16 families and 85 genera. On the family‐level phylogeny, the occurrence of myrmecomorphy is confined mainly to families branching later on the tree, from the RTA clade. On the generic‐level phylogenies in Corinnidae and Salticidae, myrmecomorphy is not only of derived origin. Estimated ancestral state was non‐mimetic in Salticidae and poor inaccurate myrmecomorphy in Corinnidae. Thus, inaccurate myrmecomorphic spider mimics seem rather ancestral to accurate but additional analysis on species‐level phylogenies is needed to support this conclusion. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 97–111.     

A novel property of spider silk: chemical defence against ants

Spider webs are made of silk, the properties of which ensure remarkable efficiency at capturing prey. However, remaining on, or near, the web exposes the resident spiders to many potential predators, such as ants. Surprisingly, ants are rarely reported foraging on the webs of orb-weaving spiders, despite the formidable capacity of ants to subdue prey and repel enemies, the diversity and abundance of orb-web spiders, and the nutritional value of the web and resident spider. We explain this paradox by reporting a novel property of the silk produced by the orb-web spider Nephila antipodiana (Walckenaer). These spiders deposit on the silk a pyrrolidine alkaloid (2-pyrrolidinone) that provides protection from ant invasion. Furthermore, the ontogenetic change in the production of 2-pyrrolidinone suggests that this compound represents an adaptive response to the threat of natural enemies, rather than a simple by-product of silk synthesis: while 2-pyrrolidinone occurs on the silk threads produced by adult and large juvenile spiders, it is absent on threads produced by small juvenile spiders, whose threads are sufficiently thin to be inaccessible to ants.     

Ant mimicry lessens predation on a North American jumping spider by larger salticid spiders

Ant-like appearance (myrmecomorphy) has evolved >70 times in insects and spiders, accounting for >2,000 species of myrmecomorphic arthropods. Most myrmecomorphic spiders are considered to be Batesian mimics; that is, a palatable spider avoids predation through resemblance to an unpalatable ant-although this presumption has been tested in relatively few cases. Here we explicitly examined the extent to which Peckhamia picata (Salticidae), a North American ant-mimicking jumping spider, is protected from four species of jumping spider predators, relative to nonmimetic salticids and model ants. In addition, we conducted focused behavioral observations on one salticid predator, Thiodina puerpera, to determine the point at which the predators' behaviors toward model, mimic, and nonmimic diverge. We also examined the behaviors of Peckhamia in the presence of Thiodina. We found that mimetic jumping spiders were consumed less than a third as often as nonmimetic jumping spiders, suggesting that Peckhamia does indeed gain protection as a result of its resemblance to ants, and so can be considered a Batesian mimic. Furthermore, our focal predator did not consume any ant-mimicking spiders, and seemed to categorize Peckhamia with its model ant early in the hunting sequence. Such early determination of prey versus nonprey may be the result of speed-accuracy trade-offs in predator decision-making.     

Negative effects of ant foraging on spiders in Douglas-fir canopies

 Spiders and ants are potential competitors and mutual predators. Indirect evidence from previous research has suggested that ant foraging may significantly lower the abundance of arboreal spiders in young Douglas-fir plantations in western Oregon. This study tested the effect of foraging by ants, dominated by Camponotus spp., on spider assemblages in Douglas-fir canopies in a 5-month ant-exclusion experiment. The biomass of potential prey organisms on foliage, dominated by Psocoptera, increased significantly by 1.9- to 2.4-fold following ant exclusion. The removal of ants did not affect the abundance of flying arthropods in the vicinity of tree canopies as indicated by sticky trap catches. The abundance of hunting spiders, the majority being Salticidae, increased significantly by 1.5- to 1.8-fold in trees without ants in the late summer; neither the abundance of web-building spiders nor the average body size of hunting and web-building spiders were significantly affected by ant removal. Spider diversity and community structure did not differ significantly between control and ant-removal trees. The majority of prey captured by ants were Aphidoidea (48.1%) and Psocoptera (12.5%); spiders represented only 1.4% of the ants’ diet. About 40% of observed ants were tending Cinara spp. aphids. Our observations suggest that the lower abundance of hunting spiders in control canopies with ants may be due to interference competition with ants resulting from ant foraging and aphid-tending activities. Direct predation of spiders by ants appeared to be of minor importance in this study system. This study did not provide sufficient evidence for exploitative competition for prey between ants and spiders. Received: 21 February 1996 / Accepted: 14 August 1996     

Prey capture behavior in an arboreal African ponerine ant

I studied the predatory behavior of Platythyrea conradti, an arboreal ponerine ant, whereas most species in this subfamily are ground-dwelling. The workers, which hunt solitarily only around dusk, are able to capture a wide range of prey, including termites and agile, nocturnal insects as well as diurnal insects that are inactive at that moment of the Nyctemeron, resting on tree branches or under leaves. Prey are captured very rapidly, and the antennal palpation used by ground-dwelling ponerine species is reduced to a simple contact; stinging occurs immediately thereafter. The venom has an instant, violent effect as even large prey (up to 30 times the weight of a worker) never struggled after being stung. Only small prey are not stung. Workers retrieve their prey, even large items, singly. To capture termite workers and soldiers defending their nest entrances, ant workers crouch and fold their antennae backward. In their role as guards, the termites face the crouching ants and end up by rolling onto their backs, their legs batting the air. This is likely due to volatile secretions produced by the ants' mandibular gland. The same behavior is used against competing ants, including territorially-dominant arboreal species that retreat further and further away, so that the P. conradti finally drive them from large, sugary food sources.     

Function of bright coloration in the wasp spider Argiope bruennichi (Araneae: Araneidae)

There are two major competing explanations for the counter-intuitive presence of bright coloration in certain orb-web spiders. Bright coloration could lure insect prey to the web vicinity, increasing the spider's foraging success. Alternatively, the markings could function as disruptive camouflage, making it difficult for the insect prey to distinguish spiders from background colour variation. We measured the prey capture rates of wasp spiders, Argiope bruennichi, that were blacked out, shielded from view using a leaf fragment, or left naturally coloured. Naturally coloured spiders caught over twice the number of prey as did either blacked-out or leaf-shielded spiders, and almost three times as many orthopteran prey. Spectrophotometer measurements suggest that the bright yellow bands on the spider's abdomen are visible to insect prey, but not the banding on the legs, which could disguise the spider's outline. Thus, our results provide strong support for the hypothesis that bright coloration in the wasp spider acts as a visual lure for insect prey and weak support for the hypothesis that the arrangement of the banding pattern across the spider's body disguises the presence of the spider on the web.