Individual personalities shape task differentiation in a social spider

Deciphering the mechanisms involved in shaping social structure is key to a deeper understanding of the evolutionary processes leading to sociality. Individual specialization within groups can increase colony efficiency and consequently productivity. Here, we test the hypothesis that within-group variation in individual personalities (i.e. boldness and aggression) can shape task differentiation. The social spider Stegodyphus sarasinorum (Eresidae) showed task differentiation (significant unequal participation) in simulated prey capture events across 10-day behavioural assays in the field, independent of developmental stage (level of maturation), eliminating age polyethism. Participation in prey capture was positively associated with level of boldness but not with aggression. Body size positively correlated with being the first spider to emerge from the colony as a response to prey capture but not with being the first to attack, and dispersal distance from experimental colonies correlated with attacking but not with emerging. This suggests that different behavioural responses to prey capture result from a complex set of individual characteristics. Boldness and aggression correlated positively, but neither was associated with body size, developmental stage or dispersal distance. Hence, we show that personalities shape task differentiation in a social spider independent of age and maturation. Our results suggest that personality measures obtained in solitary, standardized laboratory settings can be reliable predictors of behaviour in a social context in the field. Given the wealth of organisms that show consistent individual behavioural differences, animal personality could play a role in social organization in a diversity of animals.     

Effects of within‐colony competition on body size asymmetries and reproductive skew in a social spider

Reproductive partitioning is a key component of social organization in groups of cooperative organisms. In colonies of permanently social spiders of the genus Stegodyphus less than half of the females reproduce, while all females, including nonreproducers, perform suicidal allo‐maternal care. Some theoretical models suggest that reproductive skew is a result of contest competition within colonies, leading to size hierarchies where only the largest females become reproducers. We investigated the effect of competition on within‐group body size variation over six months in S. dumicola, by manipulating food level and colony size. We found no evidence that competition leads to increased size asymmetry within colonies, suggesting that contest competition may not be the proximate explanation for reproductive skew. Within‐colony body size variation was high already in the juvenile stage, and did not increase over the course of the experiment, suggesting that body size variation is shaped at an early stage. This might facilitate task specialization within colonies and ensure colony‐level reproductive output by early allocation of reproductive roles. We suggest that reproductive skew in social spiders may be an adaptation to sociality selected through inclusive fitness benefits of allo‐maternal care as well as colony‐level benefits maximizing colony survival and production.     

Prey Capture Behaviour in the Social Spider Anelosimus eximius (Araneae: Theridiidae): Responses to Prey Size and Type

Some species of web building spiders use different capture tactics for different prey types. The main factors influencing the attack behaviour are the ability of the insect to escape, the risks of injury to the spiders and prey size. This study evaluated the effects of size and prey type on prey capture behaviour of the social spider Anelosimus eximius as influenced by the number of spiders attracted by prey movements that did not bite until the immobilization (bystanders) and the number of spiders that contributed to prey immobilization (catchers). We carried out a two‐factor (prey size and type) experiment offering prey belonging to four orders: Diptera, Lepidoptera, Hymenoptera and Orthoptera, in a size gradient within each prey type. Both factors influenced the number of spiders recruited as bystanders, but only prey body size influenced the number of catchers in the subduing process. The possible advantages of the presence of bystanders around the interception site are discussed.     

How within-group behavioural variation and task efficiency enhance fitness in a social group

How task specialization, individual task performance and within-group behavioural variation affects fitness is a longstanding and unresolved problem in our understanding of animal societies. In the temperate social spider, Anelosimus studiosus, colony members exhibit a behavioural polymorphism; females either exhibit an aggressive 'asocial' or docile 'social' phenotype. We assessed individual prey-capture success for both phenotypes, and the role of phenotypic composition on group-level prey-capture success for three prey size classes. We then estimated the effect of group phenotypic composition on fitness in a common garden, as inferred from individual egg-case masses. On average, asocial females were more successful than social females at capturing large prey, and colony-level prey-capture success was positively associated with the frequency of the asocial phenotype. Asocial colony members were also more likely to engage in prey-capture behaviour in group-foraging situations. Interestingly, our fitness estimates indicate females of both phenotypes experience increased fitness when occupying colonies containing unlike individuals. These results imply a reciprocal fitness benefit of within-colony behavioural variation, and perhaps division of labour in a spider society.     

Trophic structure of the spider community of a Mediterranean citrus grove: A stable isotope analysis

Spiders are dominant terrestrial predators that consume a large variety of prey and engage in intraguild predation. Although the feeding habits of certain species are well known, the trophic structure of spider assemblages still needs to be investigated. Stable isotope analysis enables characterisation of trophic relationships between organisms because it tracks the energy flow in food webs and indicates the average number of trophic transfers between a given species and the base of the web, thus being a useful tool to estimate the magnitude of intraguild predation in food webs. Using this technique, we studied the trophic groups of spiders and their links within the arthropod food web of a Mediterranean organic citrus grove. We assessed the trophic positions of the 25 most common spider species relative to other arthropod predators and potential prey in the four seasons of the year, both in the canopy and on the ground. The analyses showed great seasonal variation in the isotopic signatures of some arthropod species, as well as the existence of various trophic groups and a wide range of trophic levels among spiders, even in species belonging to the same family. Differences in δ¹⁵N between spiders and the most abundant prey in the grove usually spanned two trophic levels or more. Our findings provide field evidence of widespread intraguild predation in the food web and caution against using spider families or guilds instead of individual species when studying spider trophic interactions.     

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.     

Non-webbuilding spiders: prey specialists or generalists?

Summary Feeding experiments were performed with seven species of non-webbuilding spiders and a variety of prey taxa. Some species were generally polyphagous whereas other spiders restricted their prey to a few groups. At one end of the spectrum of prey specialization the thomisid Misumena vatia is limited to a few taxa of possible prey (Table 1). The literature of prey records of non-webbuilding spiders is reviewed (Table 2) with special emphasis on oligophagous or monophagous spiders. Monophagous spiders are generally rare and have specialized on only a few prey taxa: social insects (ants, bees, termites) and spiders.     

Is There Division of Labor in Cooperative Pseudoscorpions? An Analysis of the Behavioral Repertoire of a Tropical Species

Division of labor is a strategy that maximizes the foraging and reproductive success of eusocial insects. Although some arachnids exhibit colony structure and social organization similar to that of hymenopterans, temporal polyethism has only been demonstrated in few species. The social organization of cooperative pseudoscorpions Paratemnoides nidificator is similar to that of social spiders, but it involves a clear division of labor. Work allocation was experimentally investigated in colonies composed of only one developmental stage (young or adults) or by one sex (males or females), through laboratory manipulation. During 44 h of observation, more than 14 000 behavioral repetitions were quantified, distributed in 95 different types of behavioral acts, and grouped in 10 behavioral categories. The results showed that reproductive colonies of P. nidificator are maintained by gender‐ and age‐based activities. Males and non‐reproductive females performed the external cleaning of the colony and prey capture. Reproductive females take care of the juveniles and build reproductive silk chambers. Nymphs build most of the molt chambers and perform internal cleaning. In the absence of nymphs, male colonies survived 1–2 mo, while female colonies survived 3–4 mo. In nymph colonies, work is readjusted so that all maintenance tasks are executed. This is the first study clearly demonstrating division of tasks in arachnids. It suggests that specialization is an adaptative and evolutionarily old trait in this species. Unlike cooperative spiders, P. nidificator possesses physiological (e.g. reproduction, ecdysis, lifespan) and behavioral (e.g. behavioral synchrony or self‐organization) characteristics that allow task specialization.     

Coordination of Behavioral Sequences Between Individuals During Prey Capture in a Social Spider, Anelosimus eximius

The analysis of collaborative predation sequences performed by groups of 10 individuals (females) in a nonterritorial permanent-social spider, A. eximius, shows that prey-captures are organized in successive steps. Spiders begin by throwing sticky silk, which hinders the prey in the web; they then throw dry silk, which completes the immobilization of the prey. The third step is characterized by bites that paralyze the prey that will be then carried. A concordance test reveals a coordination of the individual's acts that explains the collaborative prey-capture efficiency. No individual specialization in one type of act has been shown. On the contrary, by using living preys or artificially dead vibrated preys, we show that all individuals have equipotential behaviors. Furthermore, each spider is able to adjust its behavior to the state of the prey. Individuals already involved in prey transportation can again display bites or sticky silk throwing if the prey is artificially vibrated. This mechanism, which corresponds to stimergic processes responsible for self-organized phenomena, already described in social insects, permits a coordination of individual acts without the recourse of direct communication. These results permit us to understand better how individuals coordinate their acts and lead us to support the hypothesis that the transition between solitary species and social species in spiders could have been sudden.     

Age-related sequential web building in the colonial spider Metepeira incrassata (Araneidae): an adaptive spacing strategy

Colonial orb-weaving spiders provide insight into the proximate mechanisms by which social animals space themselves within a group. We examined mechanisms for the temporal patterns of web building that determine individual positions in Metepeira incrassata (Araneidae) colonies. The spiders display a characteristic age-related sequence of daily web building, with larger spiders completing their webs significantly earlier than smaller ones. We used data on behavioural interactions, web building, prey capture and predator attacks to evaluate four hypotheses. (1) Larger spiders are better competitors and pre-empt optimal spatial positions. (2) Smaller spiders reduce competition with larger individuals by building webs later. (3) Prey captured by different size classes is available at different times. (4) Differential predation risk determines web-building times. Large individuals dominated behavioural interactions. Disturbances by larger spiders during web construction significantly delayed the completion of smaller individuals' webs and precipitated movements to new web sites. One prediction of the first hypothesis, that spatial needs translate into earlier building, was confirmed by significantly earlier web building by mature females with egg sacs (which are unable to move their egg sacs) compared with same-sized females without eggs (which can change locations freely). Experiments to determine whether the presence of large spiders inhibited the web building of smaller individuals were equivocal. Prey availability and risk of predation are not factors affecting web-building patterns. Sequential web building appears to be a result of both larger spiders competing to pre-empt space from one another and smaller individuals attempting to reduce conflict during web construction. Sequential web building is a proximate mechanism that influences spacing among colonial orb-weaving spiders and helps shape the typical hierarchical size distribution of spiders within the colony. Similar spacing mechanisms may be seen in colonial birds and marine invertebrates. Copyright 2000 The Association for the Study of Animal Behaviour.     

Caught in the web: Spider web architecture affects prey specialization and spider–prey stoichiometric relationships

Quantitative approaches to predator–prey interactions are central to understanding the structure of food webs and their dynamics. Different predatory strategies may influence the occurrence and strength of trophic interactions likely affecting the rates and magnitudes of energy and nutrient transfer between trophic levels and stoichiometry of predator–prey interactions. Here, we used spider–prey interactions as a model system to investigate whether different spider web architectures—orb, tangle, and sheet‐tangle—affect the composition and diet breadth of spiders and whether these, in turn, influence stoichiometric relationships between spiders and their prey. Our results showed that web architecture partially affects the richness and composition of the prey captured by spiders. Tangle‐web spiders were specialists, capturing a restricted subset of the prey community (primarily Diptera), whereas orb and sheet‐tangle web spiders were generalists, capturing a broader range of prey types. We also observed elemental imbalances between spiders and their prey. In general, spiders had higher requirements for both nitrogen (N) and phosphorus (P) than those provided by their prey even after accounting for prey biomass. Larger P imbalances for tangle‐web spiders than for orb and sheet‐tangle web spiders suggest that trophic specialization may impose strong elemental constraints for these predators unless they display behavioral or physiological mechanisms to cope with nutrient limitation. Our findings suggest that integrating quantitative analysis of species interactions with elemental stoichiometry can help to better understand the occurrence of stoichiometric imbalances in predator–prey interactions.     

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.     

Synchronized and rhythmical activity during the prey capture in the social spiderAnelosimus eximius (Araneae,Theridiidae)

Summary Anelosimus eximius is a social spider species of South America. Many individuals share the same web and participate in prey capture, taking some ten seconds to locate the prey in the silky structures. In the laboratory, we analyzed the movements of each spider which took part in the pursuit, and showed that they were both synchronized and rhythmical. Spiders alternate simultaneous periods of immobility (involving 100% of the attacking individuals) and activity (involving at least 70% of the spiders).The results are discussed with reference to the model developed by Goss and Deneubourg (1988) suggesting that autocatalysis may be the motor of certain synchronized and rhythmical activities in social arthropods.     

Intraspecific variation in responses to aposematic prey in a jumping spider (Phidippus regius)

Aposematic signals often allow chemically defended prey to avoid attack from generalist predators, including jumping spiders. However, not all individual predators in a population behave in the same way. Here, in laboratory trials, we document that most individual Phidippus regius jumping spiders attack and reject chemically defended milkweed bugs (Oncopeltus fasciatus), immediately releasing them unharmed. However, a small number of individuals within the population kill and completely consume these presumably toxic prey items. This phenomenon was infrequent with only 14% of our sample (17/122) consuming the milkweed bugs over the course of the study. Individuals that killed and consumed bugs often did so repeatedly; specifically, individuals that consumed a bug in their first test were more likely to kill a bug in their second test and also tended to consume them again. We explored what might drive some (but not all) individuals to consume these bugs and found that neither sex, sexual maturity, body size, laboratory housing type, nor being wild-caught or being laboratory-reared, predicted milkweed bug consumption. Consuming bugs had no negative effects on spider mass or body condition; contrary to expectations, individuals that consumed milkweed bugs actually gained more body mass and increased in body condition. We discuss potential behavioural and physiological variation between individuals that may drive these rare behaviours and the implications for the evolution of prey defences.     

Repeatability but no short-term plasticity in the web architecture of Latrodectus hesperus western black widow spiders (Araneae: Theridiidae)

A spider's web is an extended phenotype and a direct product of behavior. Variation in web architecture may be the result of individual differences in genotype, environment, or experience. We analyzed variation in the web architecture of western black widow spiders, Latrodectus hesperus, by testing two hypotheses: (a) intrinsic individual differences and (b) plasticity according to experience of the site of prey capture. We used treatments manipulating the site of prey capture experienced by the spiders: sheet only, gum-footed lines only, and alternating patterns between sheet and gum-footed lines equally. We found considerable consistent individual variation (repeatability of r = .56) in one web component (gum-footed lines) and negligible plasticity in either component. We discuss our results in terms of the potential for the design of these web components to respond to selection, and of potential additional causes of variation in extended phenotypes.     

Local feeding specialization by badgers (Meles meles) in a mediterranean environment

A case of local feeding specialization in the European badger (Meles meles), a carnivore species with morphological, physiological and behavioural traits proper to a trophic generalist, is described. For the first time, we report a mammalian species, the European rabbit (Oryctolagus cuniculus), as the preferred prey of badgers. Secondary prey are consumed according to their availability, compensating for temporal fluctuations in the abundance of rabbit kittens. We discuss how both predator (little ability to hunt) and prey (profitability and predictability) features, may favour the observed specialization, as predicted by foraging theory. Badgers show a trend to specialize on different prey in different areas throughout the species range. It is suggested that changes in prey features can reverse the badger feeding strategy at the population level. Such dynamic behavioural responses make difficult to label badgers as generalists or specialists at the species level.     

<Emphasis Type="Italic">Argiope bruennichi</Emphasis> shows a drinking-like behaviour in web hub decorations (Araneae,Araneidae)

As stationary predators, araneid spiders that lack protective retreats are especially vulnerable to abiotic influences. Species of the genus Argiope permanently remain at the hub of their orb webs and are thereby exposed to desiccating circumstances. Like other land arthropods, spiders must balance their hygric status. Beside desiccation avoidance behaviours, they can manage this balance by water gain through either liquefied prey items or direct ingestions of free water. Drinking-like behaviours are sparely documented for Araneids. We observed Argiope bruennichi ingesting accumulated water droplets from the silk-overstitched web hub, a part of the web decoration, and subsequently tested whether this behaviour is a regular feature of this species. In 50% of our observations, spiders that had been sprayed with water actively searched the hub decoration for water droplets and ingested them. The behavioural elements were very stereotypic among the tested individuals. Significantly, A. bruennichi females only searched the covered web hubs for water, even though the entire web was moistened. These data suggest that hub decorations of A. bruennichi might have an adaptive significance by helping to maintain a balance of water metabolism, adding yet another element to the spirited debate about the functional significance of web decorations.     

Tracing the evolutionary origin of a visual signal: the coincidence of wrap attack and web decorating behaviours in orb web spiders (Araneidae)

The silk decorations that adorn the webs of many orb-web spiders are thought to have a signal function, but the evolution of the decorating behaviour remains unresolved. The decoration signal is maintained apparently because it improves foraging efficiency, through either increased encounter rates with prey or reduced damage to the web. Recent investigations suggest that the decorations may originate in a regulation of the activity of the aciniform silk glands, which produce silk for both decorating the web and wrapping prey. This view predicts a link between decorating behaviour and a preference for restraining prey by wrapping with silk, which is evident among species of Argiope spiders. Here I compare the frequency of the wrap attack behaviour in four species of orb-web spiders that occupy the same habitat, but differ in their silk decorating behaviour: two species, Plebs bradleyi and Gea theridioides, build silk decorations, while the other two, Araneus hamiltoni and Backobourkia brounii do not. Spiders were presented with prey items that varied in the ease with which they could be captured, with houseflies being more easily subdued than house crickets. As predicted, the silk decorating species used wrap attacks significantly more often than non-decorating spiders, irrespective of the prey species. These data support the view that both behaviours are evolutionary linked. I propose that silk decorating originated from the evolution of wrap attacking, and that silken web decorations have later evolved into a signal and are now maintained for that function.     

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.     

Oldest true orb-weaving spider (Araneae: Araneidae)

The aerial orb web woven by spiders of the family Araneidae typifies these organisms to laypersons and scientists alike. Here we describe the oldest fossil species of this family, which is preserved in amber from Alava, Spain and represents the first record of Araneidae from the Lower Cretaceous. The fossils provide direct evidence that all three major orb web weaving families: Araneidae, Tetragnathidae and Uloboridae had evolved by this time, confirming the antiquity of the use of this remarkable structure as a prey capture strategy by spiders. Given the complex and stereotyped movements that all orb weavers use to construct their webs, there is little question regarding their common origin, which must have occurred in the Jurassic or earlier. Thus, various forms of this formidable prey capture mechanism were already in place by the time of the explosive Cretaceous co-radiation of angiosperms and their flying insect pollinators. This permitted a similar co-radiation of spider predators with their flying insect prey, presumably without the need for a 'catch-up lag phase' for the spiders.