Spider movement, UV reflectance and size, but not spider crypsis, affect the response of honeybees to Australian crab spiders

According to the crypsis hypothesis, the ability of female crab spiders to change body colour and match the colour of flowers has been selected because flower visitors are less likely to detect spiders that match the colour of the flowers used as hunting platform. However, recent findings suggest that spider crypsis plays a minor role in predator detection and some studies even showed that pollinators can become attracted to flowers harbouring Australian crab spider when the UV contrast between spider and flower increases. Here we studied the response of Apis mellifera honeybees to the presence of white or yellow Thomisus spectabilis Australian crab spiders sitting on Bidens alba inflorescences and also the response of honeybees to crab spiders that we made easily detectable painting blue their forelimbs or abdomen. To account for the visual systems of crab spider's prey, we measured the reflectance properties of the spiders and inflorescences used for the experiments. We found that honeybees did not respond to the degree of matching between spiders and inflorescences (either chromatic or achromatic contrast): they responded similarly to white and yellow spiders, to control and painted spiders. However spider UV reflection, spider size and spider movement determined honeybee behaviour: the probability that honeybees landed on spider-harbouring inflorescences was greatest when the spiders were large and had high UV reflectance or when spiders were small and reflected little UV, and honeybees were more likely to reject inflorescences if spiders moved as the bee approached the inflorescence. Our study suggests that only the large, but not the small Australian crab spiders deceive their preys by reflecting UV light, and highlights the importance of other cues that elicited an anti-predator response in honeybees.     

Crab spiders (Thomisidae) attract insect flower‐visitors without UV signalling

1. Crab spiders (Thomisidae) indirectly affect insect flower‐visitor and flowering plant interactions by consuming and altering the behaviour of insects. 2. Although one expects insect flower‐visitors to avoid crab spiders actively, some crab spider species are known to attract flower‐visitors. Crab spiders may use UV signalling to lure potential prey to the flowers they occupy. 3. In the present study, a field experiment was conducted to examine the effects of crab spiders occupying three prairie plant species for the insect flower‐visitor community. Pollinating insects were significantly attracted to inflorescences with crab spiders compared to inflorescences without crab spiders for two plant species, and herbivorous insects were attracted to inflorescences with crab spiders for one of these plant species. The two flowering plant species with increased pollinator visitation showed increased seed weights for plants with crab spiders, indicating crab spider presence indirectly increased pollination. 4. To test the UV signalling hypothesis, inflorescences with crab spiders of one plant species were observed under both a UV‐blocking plastic and a clear plastic control. Contrary to our prediction, flower‐visitors were not more likely to land on inflorescences under the clear plastic; the UV signalling hypothesis was not supported. Other unknown explanations underlie prey attraction to inflorescences with crab spiders.     

Ineffective crypsis in a crab spider: a prey community perspective

Cryptic coloration is assumed to be beneficial to predators because of an increased encounter rate with unwary prey. This hypothesis is, however, very rarely, if ever, studied in the field. The aim of this study was to quantify the encounter rate and capture success of an ambush predator, in the field, as a function of its level of colour-matching with the background. We used the crab spider Misumena vatia, which varies its body colour and can thereby match the colour of the flower it hunts upon. We carried out a manipulative field experiment using a complete factorial design resulting in six different colour combinations of crab spiders and flowers differing in their degree of colour-matching. A rich and diverse set of naturally occurring insects visited the flowers while we continuously video-recorded the spider''s foraging activity. This enabled us to test the crypsis, the spider avoidance and the flower visitor attraction hypotheses, all three supported by previous studies. Flower visitors of different groups either avoided crab spiders independent of colour-matching, such as solitary bees and syrphid flies, or ignored them, such as bumble-bees and honeybees. Moreover, colour-matched spiders did not have a higher encounter rate and capture success compared to the visually apparent ones. Thus, our results support the spider avoidance hypothesis, reject the two other hypotheses and uncovered a fourth behaviour: indifference to predators. Because flower visitors reacted differently, a community approach is mandatory in order to understand the function of background colour-matching in generalist predators. We discuss our results in relation to the size and sociality of the prey and in relation to the functional significance of colour change in this predator.     

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.     

Visual preference of flower-visiting crab spiders (Ebrechtella tricuspidata) for host flowers

1. Crab spiders (Thomisidae) are common flower-visiting spiders that ambush prey on inflorescences. As such, they require specific flowers or substrates for hunting, which are most often selected using sensory cues (e.g. vision). However, few studies have examined the visual preference of crab spiders for particular flowers. In this study, the visual preferences of the crab spider Ebrechtella tricuspidata for different inflorescence characteristics (e.g. colour and shape) were investigated. 2. The results showed that adult spiders explored all colours and shapes, whereas juvenile spiders displayed an overall preference for long (red) and short (purple) wavelength colours. Thus, differences in colour were not particularly important for E. tricuspidata with regard to visual attractiveness and selection. 3. However, inflorescence shape (e.g. tulip) was found to be a more desirable trait for selection, which was probably due to the provision of shelter. 4. These results also suggest that male preference for female spiders depended somewhat on the background colour (wavelength) of the flower on which the female was located.     

Costs and benefits of facultative aggregating behaviour in the orb-spinning spider Gasteracantha minax Thorell (Araneae: Araneidae)

Abstract The potential costs and benefits of foraging in aggregations are examined for the orb-spinning spider Gasteracantha minax. Web-site tenacity is low in this species; individuals frequently move among sites, thereby joining aggregations of different sizes. Female spiders in aggregations suffered lower predation rates and attracted more males than their solitary counterparts. However, aggregated eggsacs, probably produced by females in aggregations, experienced higher rates of parasitism than solitary eggsacs. We found no evidence of higher prey capture success rates among spiders in aggregations. However, we demonstrate a novel way in which spiders can increase their foraging efficiency by decreasing silk investment. A spider spinning a web within an existing aggregation can attach the support threads of its web to those of other webs, thereby exploiting the silk produced by other spiders.     

Foraging Benefits in a Colour Polymorphic Neotropical Orb Web Spider

Conspicuous body colouration in sedentary predators such as orb web spiders seems paradoxical as potential prey can see and avoid the webs. Several studies have demonstrated that rather than deterring prey, the colours act as sensory traps for flower‐seeking insects. In chromatically polymorphic species, the existence of more than one colour morph may lead to differing levels of prey attraction. To explore these issues, we studied a neotropical orb web spider, Verrucosa arenata, which shows colour polymorphism with predominantly white or yellow abdomen colours. We asked whether a particular morph is dominant in the population, and whether a particular morph is associated with enhanced foraging success and body condition. Here we showed that although yellow morphs attracted more prey, white morphs were in better body condition. We showed that model prey such as honeybees are able to discriminate between the morphs. We discuss these findings in relation to the functional significance of bright body colouration and colour polymorphism in spiders.     

Advantages of social foraging in crab spiders: Groups capture more and larger prey despite the absence of a web

Among group‐living spiders, subsocial representatives in the family of crab spiders (Thomisidae) are a special case, as they build protective communal leaf nests instead of extensive communal capture webs. It could thus be inferred that antipredator benefits (e.g., enhanced protection in larger nests) rather than foraging‐related advantages (e.g., capture of more and larger prey) promote sociality in this family. Nonetheless, subsocial crab spiders do share prey, and if this behaviour does not reflect mere food scramble but has a cooperative character, crab spiders may offer insights into the evolution of social foraging applicable to many other cooperative predators that hunt without traps. Here, we performed a comparative laboratory feeding experiment on three of the four subsocial crab spider species—Australomisidia ergandros, Australomisidia socialis and Xysticus bimaculatus—to determine if crab spiders derive advantages from foraging in groups. In particular, we tested artificially composed groups of five sibling spiderlings vs. single siblings in terms of prey capture success and prey size preference. Across species, groups had higher prey capture success (measured in terms of capture rates and capture latency) and were more likely to attack large, sharable prey—dynamics leading to reduced food competition among group members in favour of living and foraging in groups. Within groups, we further compared prey extraction efficiency among the three applied social foraging tactics: producing, scrounging and feeding alone. In A. ergandros, individuals were exceptionally efficient when using the non‐cooperative scrounger tactic, which entails feeding on the prey provided by others. Thus, our multispecies comparison confirms foraging advantages in maintaining a cooperative lifestyle for crab spiders, but also demonstrates the relevance of research into exploitation of cooperative foraging in this family.     

Conspicuous colouration attracts prey to a stationary predator

Abstract 1. Conspicuous body colouration is counter‐intuitive in stationary predators because sit‐and‐wait tactics frequently rely on concealed traps to capture prey. Consequently, bright colours and contrasting patterns should be rare in predators using traps as they may alert potential prey. Yet, some orb‐weaving spiders are brightly coloured and contrastingly patterned. How can conspicuousness of trap‐building sit‐and‐wait predators be favoured by natural selection? 2. Observations of spiny spiders Gasteracantha fornicata in north‐eastern Australia showed that the size of spiders relative to their orb webs correlated positively with relative prey numbers already captured in their webs. A possible explanation is that the relatively larger appearance of the yellow–black striped dorsal surface of this spider attracts more visually oriented prey items. Prey attracted to webs may get trapped, thereby increasing the spiders' foraging success. 3. To test this hypothesis for the function of conspicuous body colouration, a field experiment was conducted that documented the prey capture rates of spiny spiders after manipulating or sham‐manipulating their appearance. 4. As predicted, spiders that were dyed black on their striped dorsal surface caught relatively fewer prey items than did control spiders. Thus, conspicuous dorsal body colouration may be adaptive in spiny spiders because it increases foraging success and, presumably, survival rates and reproductive outputs. Overall, these data support the colour‐as‐prey‐attractant hypothesis in a stationary, trap‐building predator.     

Aging and foraging efficiency in an orb-web spider

Aging is often associated with reduced behavioral performance such as decreased locomotion or food consumption, related to a deterioration in physiological functions. In orb-web spiders, webs are used to capture prey and aging can affect web-building behavior and web structure. Here, we investigated the effect of aging on prey capture in the orb-web spider Zygiella x-notata. The ability of adult females to capture flies was examined at different ages. The rate of prey capture did not change with age, but older spiders took more time to subdue and capture the prey. Alterations which appeared in web structure with age (increase in the number of anomalies affecting radii and capture spiral) affected prey capture behavior. Furthermore, the analysis of individual performance (carried out on 17 spiders at two different ages) showed that older females spent more time handling the prey and finding it in the web. Our results suggest that, in the laboratory, age does not affect prey capture rates but it influences prey capture behavior by affecting web structure or/and spider motor functions.     

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.     

Evidence suggests that modified setae of the crab spiders Stephanopis spp. fasten debris from the background

Crab spiders (Thomisidae) are known by their ability to change their body colouration via change in epithelial pigments. However, the crab spider genus Stephanopis appears to match the colouration of the bark they are sitting on by having debris attached to its dorsal cuticle. The functional morphology, colouration, and evolution of this phenomenon were investigated in Stephanopis cf. scabra and S. cambridgei. Analysis under the microscope revealed that debris originated from the bark they were sitting on. Using scanning electron microscopy, three different types of setae likely related in the retention of debris were found in S. cf. scabra and one in S. cambridgei. These setae are branched and possess barbs, unlike the more filiform setae found in other crab spider species. In addition, the presence of debris improved the brightness background matching of spiders against the bark, but not hue and chroma matching. Ancestral character state reconstruction suggested that presence of debris evolved two to three times within Thomisidae. The evolution of both masking and colour change among crab spiders indicates that they are under a strong selection to avoid detection.     

Spinneret Microstructure of the Silk Spinning Apparatus in the Crab Spider, Misumenops tricuspidatus (Araneae: Thomisidae)

The silk spinning apparatus in the crab spider, Misumenops tricuspidatus was studied with the field emission scanning electron microscope (FESEM) and the main microstructural characteristics of the silk glands are presented. In spite of the fact that the crab spiders do not spin webs to trap a prey, they also have silk apparatus even though the functions are not fully defined. The crab spider, Misumenops tricuspidatus possesses only three types of silk glands which connected through the typical spinning tubes on the spinnerets. The spinning apparatus of Misumenops closely corresponds to that of wandering spiders such as jumping spiders or wolf spiders except some local variations. Anterior spinnerets comprise 2 pairs of the ampullates and 48 (±5) pairs of pyriform glands. Another 2 pairs of ampullate glands and nearly 20 (±3) pairs of aciniform glands were connected on the middle spinnerets. Additional 50 (±5) pairs of the aciniform glands were connected on the posterior spinnerets. The aggregate glands and the flagelliform glands which have the function of sticky capture thread production in orb‐web spiders as well as the tubuliform glands for cocoon production in females were not developed at both sexes of this spider, characteristically.     

The effect of colour variation in predators on the behaviour of pollinators: Australian crab spiders and native bees

1. Australian crab spiders exploit the plant–pollinator mutualism by reflecting UV light that attracts pollinators to the flowers where they sit. However, spider UV reflection seems to vary broadly within and between individuals and species, and we are still lacking any comparative studies of prey and/or predator behaviour towards spider colour variation. 2. Here we looked at the natural variation in the coloration of two species of Australian crab spiders, Thomisus spectabilis and Diaea evanida, collected from the field. Furthermore, we examined how two species of native bees responded to variation in colour contrast generated by spiders sitting in flowers compared with vacant flowers. We used data from a bee choice experiment with D. evanida spiders and Trigona carbonaria bees and also published data on T. spectabilis spiders and Austroplebeia australis bees. 3. In the field both spider species were always achromatically (from a distance) undetectable but chromatically (at closer range) detectable for bees. Experimentally, we showed species‐specific differences in bee behaviour towards particular spider colour variation: T. carbonaria bees did not show any preference for any colour contrasts generated by D. evanida spiders but A. australis bees were more likely to reject flowers with more contrasting T. spectabilis spiders. 4. Our study suggests that some of the spider colour variation that we encounter in the field may be partly explained by the spider's ability to adjust the reflectance properties of its colour relative to the behaviour of the species of prey available.     

Wasp Attacks and Spider Defence in the Orb Weaving Species <Emphasis Type="Italic">Zygiella x-notata</Emphasis>

Predator–prey relationships are generally based on arm-race. Wasps and spiders are both predators, which could be potential prey for each other. The orb weaver spider Zygiella x-notata is sometimes a prey for the wasp Vespula germanica. We observed the wasp hunting behaviour under natural conditions, and we tested the influence of the spider’s behaviour on the wasp attack success. Wasps were active predators during the reproductive period of the spider. Results showed that wasps located more easily male spiders than females particularly when they were engaged in mate guarding. Female location depended on the presence of a web, but also of prey or prey remains in the web. On the other hand, their location depend neither on the characteristics and the position of the retreat in the environment nor on the size of the web. After location, males were more often captured than females whatever their behaviour (mate guarding or not). Presence of prey remains or prey in the web did not increase the risk for the spider to be captured. There was also no influence of the retreat’s characteristics or of its position in the habitat on the risk for the spider to be captured; but wasp successful attacks were less numerous when silk was present around the entrance of the retreat or when the spider was completely inside. As prey and prey remains favoured location of spiders by the wasps, we tested spider web cleaning behaviour as a response to wasp predatory pressure. By throwing small polystyrene pellets in the webs, we observed that more 80% of the spiders rejected the pellets in less than one minute. Our data indicated that wasps were significant predators of Z. x-notata and wasp attack could have been a selective pressure that had favoured spider defensive behaviours such as web cleaning.     

蜘蛛位置对成功捕获猎物和球型网图案的影响

静坐在球型网的中心,蜘蛛可能遭受天敌的攻击并暴露在不利的天气条件下,如风和雨。然而,栖居于网的中心使蜘蛛比隐藏在隐蔽场所中的蜘蛛能更迅速地察觉并捕获猎物,这是因为猎物的位置仅能被位于网中心的蜘蛛所确定。对在隐蔽场所中的蜘蛛而言,提高对猎物捕获率的方式之一是尽量减少隐蔽所与网中心的距离。而且,网中心与隐蔽所之间较短的距离使蜘蛛能更迅速地逃离危险境况。我使用既在网中心、又在隐蔽场所的硬类肥蛛(Larinioides sclopetarius Clerck),来检验这两种行为如何影响对猎物的捕获成功率。隐藏在隐蔽场所中的蜘蛛更经常忽略猎物,使猎物也有比较多的逃离机会,这样,与在网中心的蜘蛛相比,猎物的损失率就更高。另外,研究了隐蔽场所的位置对球型网图案的影响。在大多数球型网中,网中心上方的区域比网下方小,丝也比较少,形成了结构不对称的网;隐蔽场所通常在网的上方。当隐蔽场所的位置在实验中被倒转时,就形成了非典型的球型网。最后,L．sclopetarius建造的网有很突出的边缘非对称性,与隐蔽场所相邻的区域面积较小,而远离隐蔽场所的区域面积较大,这也可解释为减少了隐蔽场所和网中心之间的距离[动物学报50(4)：559-565．2004]。     

Impact of flower-dwelling crab spiders on plant-pollinator mutualisms

Indirect effects in interactions occur when a species influences a third species by modifying the behaviour of a second one. It has been suggested that indirect effects of crab spiders (Thomisidae) on pollinator behaviour can cascade down the food web and negatively affect plant fitness. However, it is poorly understood how different pollinator groups react to crab spiders and, thus, when a reduction in plant fitness is likely to occur. Using continuous video surveillance, we recorded the behaviour of pollinators on two flower species and the pollinators’ responses to three crab spider treatments: inflorescences (1) with a pinned dried spider, (2) with a spider model made of paper, and (3) without spiders (control). We found that pollinators avoided inflorescences with dried spiders only on one plant species (Anthemis tinctoria). Pollinators showed no significant avoidance of paper spiders. Honeybees and bumblebees did not react to dried spiders, but solitary bees and syrphid flies showed a strong avoidance. Finally, we found no evidence that inflorescences with dried spiders suffered from a decrease in fitness in terms of a reduced seed set. We hypothesise that top-down effects of predators on plants via pollinators depend on the degree of specialisation of pollinators and their tendency to avoid spiders.     

Distribution of plant‐dwelling spiders: Inflorescences versus vegetative branches

Abstract The influence of the architecture of vegetative branches on the distribution of plant‐dwelling spiders has been intensively studied, and the effects on the aggregation of individuals in several spider species on plants include variation in prey abundance, availability of predator‐free refuges and smoother microclimate conditions. The emergence of inflorescences at the reproductive time of the plants changes branch architecture, and could provide higher prey abundance for the spiders. The distribution of spiders between inflorescences and vegetative branches was compared on four widespread plant species in a Brazilian savannah‐like system. Inflorescences attracted more spiders than vegetative branches for all plant species sampled. The influence of branch type (inflorescence and vegetative) on spider distribution was also evaluated by monitoring branches of Baccharis dracunculifolia DC. in vegetative and flowering periods for 1 year, and through a field experiment carried out during the same period where artificial inflorescences were available for spider colonization. Artificial inflorescences attached to B. dracunculifolia branches attracted more spiders than non‐manipulated vegetative branches for most of the year. However, this pattern differed among spider guilds. Foliage‐runners and stalkers occurred preferentially on artificial inflorescences relative to control branches. The frequencies of ambushers and web‐builders were not significantly different between treatment and control branches. However, most ambush spiders (65%) occurred only during the flowering period of B. dracunculifolia, suggesting that this guild was influenced only by natural inflorescences. The experimental treatment also influenced the size distribution of spiders: larger spiders were more abundant on artificial inflorescences than on vegetative branches. The hypothesis that habitat architecture can influence the spider assemblage was supported. In addition, our observational and experimental data strongly suggest that inflorescences can be a higher quality microhabitat than non‐reproductive branches for most plant‐dwelling spiders.     

Body‐colour variation in an orb‐web spider and its effect on predation success

Animal body coloration serves several functions such as thermoregulation, camouflage, aposematism, and intraspecific communication. In some orb‐web spiders, bright and conspicuous body colours are used to attract prey. On the other hand, there are other species whose body colour does not attract prey. Using a spider species showing individual body‐colour variation, the present study aimed to determine whether or not the variation in body colour shows a correlation with predation rates. We studied the orb‐web spider (Cyclosa argenteoalba) using both field observations and T‐maze experiments, in which the prey were exposed to differently coloured spiders. Cyclosa argenteoalba has silver‐ and black‐coloured areas on its dorsal abdomen, with the ratio of these two colours varying continuously among individuals. The bright and conspicuous silver area reflects ultraviolet light. Results of both field observations and colour choice experiments using Drosophila flies as prey showed that darker spiders have a greater chance of capturing prey than silver spiders. This indicates that body‐colour variation affects predation success among individuals and that the bright silver colour does not function to attract prey in C. argenteoalba.     

Web-building behaviour in the orb-weaving spider Zygiella x-notata: influence of experience

Zygiella x-notata is an orb-weaving spider that often renews its trap daily. Web building has associated costs and benefits, and building successive webs may have consequences for lifetime reproductive success. In the laboratory, we tested the ability of Z. x-notata to modify its building behaviour in response to various stages in predation (prey detection, capture and ingestion) experienced with a previous web. We determined which stages provided information for the spiders. Spiders that detected, captured and ingested prey and then rebuilt their web used less silk and made a smaller capture area than in the previous web. There was no effect of prey detection alone on the next web. Capture without feeding gave the same results as capture followed by feeding. The spiders that ate prey without detection and capture (feeding by hand) had the same energetic gains as spiders that caught prey but delayed building a new web. The spiders thus showed plasticity in web-building behaviour and in the amount of silk used (energetic investment) in the short term (from one web to the next). Changes in body condition may therefore influence web construction. Moreover, information gained during prey capture appeared to influence the size and structure of the next web. This ability should enable spiders to adapt their web building to maximize their fitness. Copyright 2000 The Association for the Study of Animal Behaviour.