Altitudinal patterns of spider sociality and the biology of a new midelevation social Anelosimus species in Ecuador

To the extent that geography correlates with particular environmental parameters, the geographical distribution of phylogenetically related social and nonsocial organisms should shed light on the conditions that lead to sociality versus nonsociality. Social spiders are notorious for being concentrated in tropical regions of the world, occupying a set of habitats more restricted than those available to the phylogenetic lineages in which they occur. Here we document a parallel pattern involving elevation in the spider genus Anelosimus in America and describe the biology of a newly discovered social species found at what appears to be the altitudinal edge of sociality in the genus. We show that this is a cooperative permanent-social species with highly female-biased sex ratios but colonies that are one to two orders of magnitude smaller than those of a low-elevation congener of similar body size. We suggest that the absence of subsocial Anelosimus species in the lowland rain forest may be due to an increased probability of maternal death in this habitat due to greater predation and/or precipitation, while absence of a sufficient supply of large insects at high elevations or latitudes may restrict social species to low- to midelevation tropical moist forests. We refer to these as the "maternal survival" and "prey size" hypotheses, respectively, and suggest that both in combination may explain the geographical distribution of sociality in the genus.     

The role of prey size and abundance in the geographical distribution of spider sociality

1. Social species in the spider genus Anelosimus predominate in lowland tropical rainforests, while congeneric subsocial species occur at higher elevations or higher latitudes. 2. We conducted a comparative study to determine whether differences in total biomass, insect size or both have been responsible for this pattern. 3. We found that larger average insect size, rather than greater overall biomass per se, is a key characteristic of lowland tropical habitats correlating with greater sociality. 4. Social species occupied environments with insects several times larger than the spiders, while subsocial species nearing dispersal occupied environments with smaller insects in either high or low overall biomass. 5. Similarly, in subsocial spider colonies, individuals lived communally at a time when they were younger and therefore smaller than the average insect landing on their webs. 6. We thus suggest that the availability of large insects may be a critical factor restricting social species to their lowland tropical habitats.     

Social behaviour in a web-building lynx spider, Tapinillus sp. (Araneae: Oxyopidae)

Social behaviour involving cooperative prey capture and communal feeding is reported for the first time in the spider family Oxyopidae (lynx spiders), in a web-building species of the genus Tapinillus. This social spider inhabits communal webs that may contain several dozen individuals, including adults of both sexes and juveniles of different cohorts. Its colonies occur in clusters and appear to be long-lived, much like those of non-territorial permanently social species such as Anelosimus eximius (Theridiidae) or Agelena consociata (Agelenidae). However, unlike colonies of these other cooperative spiders, the colonies of the social Tapinillus do not have highly female-biased sex ratios. The possible explanations for this difference are discussed.     

Female body size, fecundity parameters and foundation of new colonies in Anelosimus jabaquara (Araneae, Theridiidae)

Summary. As in other social spider species, subadult Anelosimus jabaquara females found new colonies after solitary dispersal. Some individuals, however, usually remain and reproduce in their natal nests. To test the hypothesis that large females disperse more often than smaller ones, we compared the body size of A. jabaquara females that remained in their natal colonies with those that left to build solitary webs. We also compared clutch size, egg diameter, total egg volume and spiderling size in both conditions. Emigrating females were significantly larger and laid larger clutches. The smaller females that had not dispersed laid significantly larger eggs, although their total egg volume was lower. Spiderlings of solitary females were smaller and had a smaller range of size variation than those from colonies. We discuss the implications of these results in terms of costs and benefits of dispersion for spiders in different nutritional conditions.     

Colony size and individual fitness in the social spider Anelosimus eximius

ABSTRACT The effects of colony size on individual fitness and its components were investigated in artificially established and natural colonies of the social spider Anelosimus eximius (Araneae: Theridiidae). In the tropical rain forest understory at a site in eastern Ecuador, females in colonies containing between 23-107 females had india significantly higher lifetime reproductive success than females in smaller colonies. Among larger colonies, this trend apparently reversed. This overall fitness function was a result of the conflicting effects of colony size on different components of fitness. In particular, the probability of offspring survival to maturity increased with colony size while the probability of a female reproducing within the colonies decreased with colony size. Average clutch size increased with colony size when few or no wasp parasitoids were present in the egg sacs. With a high incidence of egg sac parasitoids, this effect disappeared because larger colonies were more likely to be infected. The product of the three fitness components measured-probability of female reproduction, average clutch size, and offspring survival-produced a function that is consistent with direct estimates of the average female lifetime reproductive success obtained by dividing the total number of offspring maturing in a colony by the number of females in the parental generation. Selection, therefore, should favor group living and itermediate colony sizes in this social spider.     

Gradients of precipitation and ant abundance may contribute to the altitudinal range limit of subsocial spiders: insights from a transplant experiment

Species range boundaries often form along environmental gradients that dictate the success of the phenotypes present in each habitat. Sociality may allow colonization of environments where related species with a solitary lifestyle cannot persist. Social spiders in the genus Anelosimus appear restricted to low- and mid-elevation moist environments in the tropics, while subsocial spiders, common at higher elevations and latitudes, appear to be absent from the lowland tropical rainforest. Here, we seek factors that may simultaneously prevent subsocial Anelosimus species from colonizing the lowland rainforest while favouring species with large social groups in this habitat. To this end, we transplanted small groups of a subsocial species, which contain the offspring of a single female, from cloud forest habitat in the centre of its natural range to lower montane rainforest on the range margin and to lowland rainforest outside of the species range. Groups transplanted at the range margin and below their range limit were less likely to disperse and experienced increased mortality. This was correlated with greater rainfall intensity and ant abundance. We show that protection from rainfall enhances the performance of small groups of spiders in the lowland rainforest, and suggest that predation or disturbance by ants may influence the geographical range limits of this species.     

Colony Foundation in a Social Spider

Two modes of colony foundation are described for the social spider Anelosimus eximius. Foundress survivorship and colony mortality are discussed and correlated to the abundance of this species. The theoretical implications of these factors on the degree of relatedness of the members of a colony are discussed.     

Subsocial spiders in space and time: A fine scale approach to the dynamics of dispersal

Less than 0.2% of all spider species live in close associations with conspecifics. Among these, subsocial spiders show characteristics of both solitary spiders (e.g., individuals disperse for breeding) and social spiders (e.g., prolonged cooperative behaviours at least prior to independent reproduction). Dispersing individuals build small webs, usually with one inhabitant, whereas colonies are large webs with plant debris and harbouring multiple females. We studied the spatiotemporal dynamics of dispersal in the subsocial spider Anelosimus baeza. We followed the occupancy of all colonies and dispersal webs over the breeding season by mapping the number and sex of spiders with respect to their location in three dimensions. We studied the settlement patterns of new webs and fluctuation in web occupancy through movement between occupied and abandoned webs of colonies and dispersal webs. The occupancy of webs was highly dynamic with changes occurring at small time scales. The similarity in the patterns of web occupancy by females among dispersal webs was partially explained by their spatial and their temporal proximity. Our results suggest that dispersal webs may be used by spiders as a temporary refuge by both sexes during the breeding season. Patterns described here suggest new approaches to dispersal studies in group living spiders.     

Iterative evolution of increased behavioral variation characterizes the transition to sociality in spiders and proves advantageous

Abstract The evolution of group living is regarded as a major evolutionary transition and is commonly met with correlated shifts in ancillary characters. We tested for associations between social tendency and a myriad of abiotic variables (e.g., temperature and precipitation) and behavioral traits (e.g., boldness, activity level, and aggression) in a clade of spiders that exhibit highly variable social structures (genus Anelosimus). We found that, relative to their subsocial relatives, social species tended to exhibit reduced aggressiveness toward prey, increased fearfulness toward predators, and reduced activity levels, and they tended to occur in warm, wet habitats with low average wind velocities. Within-species variation in aggressiveness and boldness was also positively associated with sociality. We then assessed the functional consequences of within-species trait variation on reconstituted colonies of four test species (Anelosimus eximius, Anelosimus rupununi, Anelosimus guacamayos, and Anelosimus oritoyacu). We used colonies consisting of known ratios of docile versus aggressive individuals and group foraging success as a measure of colony performance. In all four test species, we found that groups composed of a mixture of docile and aggressive individuals outperformed monotypic groups. Mixed groups were more effective at subduing medium and large prey, and mixed groups collectively gained more mass during shared feeding events. Our results suggest that the iterative evolution of depressed aggressiveness and increased within-species behavioral variation in social spiders is advantageous and could be an adaptation to group living that is analogous to the formation of morphological castes within the social insects.     

Collective aggressiveness limits colony persistence in high‐ but not low‐elevation sites at Amazonian social spiders

Identifying the traits that foster group survival in contrasting environments is important for understanding local adaptation in social systems. Here, we evaluate the relationship between the aggressiveness of social spider colonies and their persistence along an elevation gradient using the Amazonian spider, Anelosimus eximius. We found that colonies of A. eximius exhibit repeatable differences in their collective aggressiveness (latency to attack prey stimuli) and that colony aggressiveness is linked with persistence in a site‐specific manner. Less aggressive colonies are better able to persist at high‐elevation sites, which lack colony‐sustaining large‐bodied prey, whereas colony aggression was not related to chance of persistence at low‐elevation sites. This suggests that low aggressiveness promotes colony survival in high‐elevation, prey‐poor habitats, perhaps via increased tolerance to resource limitation. These data reveal that the collective phenotypes that relate to colony persistence vary by site, and thus, the path of social evolution in these environments is likely to be affected.     

Spatio-temporal differentiation and sociality in spiders

Species that differ in their social system, and thus in traits such as group size and dispersal timing, may differ in their use of resources along spatial, temporal, or dietary dimensions. The role of sociality in creating differences in habitat use is best explored by studying closely related species or socially polymorphic species that differ in their social system, but share a common environment. Here we investigate whether five sympatric Anelosimus spider species that range from nearly solitary to highly social differ in their use of space and in their phenology as a function of their social system. By studying these species in Serra do Japi, Brazil, we find that the more social species, which form larger, longer-lived colonies, tend to live inside the forest, where sturdier, longer lasting vegetation is likely to offer better support for their nests. The less social species, which form single-family groups, in contrast, tend to occur on the forest edge where the vegetation is less robust. Within these two microhabitats, species with longer-lived colonies tend to occupy the potentially more stable positions closer to the core of the plants, while those with smaller and shorter-lived colonies build their nests towards the branch tips. The species further separate in their use of common habitat due to differences in the timing of their reproductive season. These patterns of habitat use suggest that the degree of sociality can enable otherwise similar species to differ from one another in ways that may facilitate their co-occurrence in a shared environment, a possibility that deserves further consideration.     

Cooperation and Prey Capture Efficiency in a Social Spider,Anelosimus eximius (Araneae,Theridiidae)

We studied the efficiency of the hunt and the characteristics of cooperation during the prey capture in a social spider Anelosimus eximius. Two natural types of prey of roughly the same length (20 mm) were used: grasshoppers (Orthoptera) and moths (Lepidoptera); 128 tests were made on 14 colonies, the smallest with 20 and the largest with 1,700 individuals. Test times were 12.00 h, defined as an inactive period for the spiders and 18.00 h, defined as an active period. Overall capture rate of intercepted prey was 66%: it was higher in large colonies or at 18.00 h, when more spider alerts were triggered by the struggling prey. Characteristics of cooperation during capture did not vary with colony size. Capture rate was higher for grasshoppers than moths (73%-58%) in spite of similar number of alerts (76%-87%); so moths must have been more difficult to capture. For both prey types, large colonies capture more rapidly and so had advantages in terms of time gain. We showed that cooperation depended on prey type: more spiders mobilised to attack moths and attack was faster than on grasshoppers. This may be interpreted as an adaptive response of the group to the prey type.     

Relatedness and genetic structure in a socially polymorphic population of the spider Anelosimus studiosus

The evolution of sociality remains a challenge in evolutionary biology and a central question is whether association between kin is a critical factor favouring the evolution of cooperation. This study examines genetic structure of Anelosimus studiosus, a spider exhibiting polymorphic social behaviour. Two phenotypes have been identified: an ‘asocial’ phenotype with solitary female nests and a ‘social’ phenotype with multi‐female/communal nests. To address the questions of whether these phenotypes are differentiated populations and whether cooperative individuals are closely related, we used microsatellites to analyse individuals from both communal and solitary nests. We found no evidence of differentiation between social and solitary samples, implying high rates of interbreeding. This is consistent with the hypothesis that these phenotypes coexist as a behavioural polymorphism within populations. Pairwise relatedness coefficients were used to test whether cooperating individuals are more closely related than expected by chance. Pairwise relatedness of females sharing communal webs averaged 0.25, the level expected for half‐siblings and significantly more closely related than random pairs from the population. Solitary females collected at similar distances to the communal spider pairs were also more closely related than expected by chance (mean relatedness = 0.18), but less related than social pairs. These results imply that low dispersal contributes to increase likelihood of interaction between kin, but relatedness between social pairs is not explained by spatial structure alone. We propose that these phenotypes represent stages in the evolution of sociality, where viscous population structure creates opportunities for kin selection and cooperation is favoured under certain environmental conditions.     

Prey size,prey perishability and group foraging in a social spider

Summary Selection might favor group foraging and social feeding when prey are distributed in patches that do not last long enough for a solitary individual to consume more than a small fraction of them (Pulliam and Millikan 1982; Pulliam and Caraco 1984). Here we considered the foraging behavior of a social spider, Anelosimus eximius, in light of this ephemeral resource hypothesis. This species builds large webs in which members cooperate to capture a wide variety of different sizes and types of prey, many of which are very large. The capture success of this species was very high across all prey sizes, presumably due to the fact that they foraged in groups. Group consumption times in natural colonies for all prey larger than five mm were less than the time that dead insects remained on the plastic sheets that we used as artificial webs. Solitary consumption estimates, calculated from the rate at which laboratory individuals extracted insect biomass while feeding, were the same as the residence times of insects on artificial webs in the field for insects between 6 and 15 mm in length and were significantly longer than the persistence of insects on plastic sheets for all larger insects. Large prey, that contribute substantially to colony energy supplies, appeared to be ephemeral resources for these spiders that could not be consumed by a single spider in the time they were available. These factors made the food intake of one spider in a group less sensitive to scavenging by others and could act to reinforce the social system of this species.     

Elevational Patterns of Diversity and Abundance of Eusocial Paper Wasps (Vespidae) in Costa Rica

We used a standard sampling protocol to measure elevational patterns of species richness and abundance of eusocial paper wasps (Hymenoptera: Vespidae) in Costa Rica. The sample transect of six sites spanned approximately 2000 m in elevation from lowland to montane forest. Species accumulation curves and species richness estimates both document a low elevation peak in paper wasp species richness at 50 and 300 m asl, with a decline in species richness at higher elevations. Comparison of species composition among elevations revealed strong species turnover from a rich lowland fauna to a depauperate, but distinct, montane fauna. We also observed a general trend toward a greater abundance of paper wasps at higher elevations, a pattern not usually observed in eusocial insects. Army ant species that prey on paper wasps declined in abundance with elevation across the sample transect, a pattern that has been observed at other sites. We discuss the possibility that elevational changes in predation pressure affect variation in paper wasp abundance and species richness. Eusocial paper wasp species employ one of two modes of colony founding, independent and swarm founding. We found that the total abundance of individual swarm-founding wasps was higher at all elevations than the abundance of independent-founding wasps, supporting previous suggestions that Neotropical swarm founders are more successful ecologically.     

Experimental study of foundation and development ofAnelosimus eximius colonies in the tropical forest of French Guiana

Summary Possibilities for new colony foundation inAnelosimus eximius (Theridiidae) were tested with isolated females (both with and without egg sacs) and with groups of individuals (groups from 150 to 250 spiders). Experimental groups were deposited in three different habitats: within the forest, on the forest edge (where natural colonies develop most frequently) and outside the forest (low savannah or areas cleared of vegetation, but in which plant life had started to grow back between the path and the forest edge).Isolated adult females had very low founding success: less than 13 % settled and spun a web; the presence of an egg sac provided by investigators was not an influencing factor. Webs of isolated females had the same architectures as those of colonies with several hundreds of individuals. This web was a horizontal sheet linked to a thick vertical network of threads.All groups of 150 to 250 spiders established colonies in appropriate habitats. The colonies outside the forest, and more than 90 % of the colonies along the forest edges successfully developed during the one month observation period. Conversely, 35 % of the colonies in the forest disappeared either a few days after being placed there, or one or two weeks after. In the latter case, spiders apparently left their webs, and all silk structures were left intact. No dead spiders were found in the webs.Average web surface areas increased in all colony types with age, except for those placed in the forest. In these colonies, the number of individuals decreased, and there were fewer egg sacs than in the colonies placed outside the forest.Results are discussed with regard to natural colony distribution along open paths and to the dispersive characteristics of this spider species.     

The attraction of silk: base of group cohesion and collective behavior in social spiders

Social spiders differ from social insects by the production and the use of silk to build irregular webs. This silk prevents dispersion of the individuals and ensures the group cohesion during swarming and collective displacements, playing a part similar to tracks of pheromones in ants. A social spider Anelosimus eximius is attracted by conspecific silk and does not show any discrimination relative to its origin, excluding any group closure. The quantity of silk and the state of satiety of the individual modulate this attraction, and might explain how the spider society adapts the size of the web to its nutritional needs.     

Reproductive success in a socially polymorphic spider: social individuals experience depressed reproductive success in isolation

1. Correlated individual differences in behaviour across ecological contexts, or behavioural syndromes, can theoretically constrain individuals' ability to optimally adjust their behaviour for specific contexts. 2. Female Anelosimus studiosus exhibit a unique behavioural polymorphism: ‘social’ females are tolerant of conspecifics and aggregate in multi‐female colonies, while ‘solitary’ females aggressively defend their singleton webs from intrusion by adult female conspecifics. Previous work found that social females are also less aggressive toward prey and are more fearful of predators. 3. In this study we quantify potential fitness consequences of these correlated behaviours by examining the potential and realised fecundities of the two phenotypes in naturally occurring colonies, and by quantifying their ability to rear offspring as singleton individuals. 4. There were no differences in the fecundities of laboratory‐reared females between the phenotypes, nor were there differences in field‐collected brooding females from naturally occurring solitary and social nests. 5. Brooding females from solitary and social colonies that were isolated in new nests for the growing season were both capable of rearing their broods; however, females from solitary nests had significantly greater success. 6. These results suggest a fitness consequence to the reduced‐aggression syndrome of social females that may represent a general impediment to the evolution of sociality in spiders.     

The body size of the New Zealand orb-weaving spider Waitkera waitakerensis (Uloboridae) is directly related to temperature and affects fecundity

Abstract. Waitkera waitakerensis occupies lowland forests of New Zealand's North Island, where temperatures decrease in a southwestward direction. The mean annual temperatures of 18 collecting sites, as extracted from GIS data, are directly related to the first femur length of adult females. Neither site elevation nor phylogeny affected spider size or other variables examined. The direct relationship between spider body size and environmental temperature followed a pattern observed in other terrestrial arthropods with a univoltine life cycle and can probably be explained by the longer growing season of warmer regions. Egg diameter was uniform across the species. Site temperature and female first femur length were each directly related to the number of eggs deposited in egg sacs. The date of egg sac collection was inversely related to egg number, suggesting that clutch size declines during the reproductive season. Females deposit eggs beneath a triangular platform and then cover them with a lower silk sheet. The area of this upper platform and the volume of the egg sac were each directly related to egg number, but not to female first femur length. The depth of the lower covering was not related to egg number or to spider first femur length. This suggests that spiders use information about the volume of eggs in their abdomens to construct an egg sac whose volume will accommodate the volume of eggs to be laid and that females do so principally by adjusting the size of the sac's upper triangular platform.     

Group living and inbreeding depression in a subsocial spider

Social spiders are unusual among social organisms in being highly inbred-males and females mature within their natal nest and mate with each other to produce successive generations. Several lines of evidence suggest that in spiders inbred social species originated from outbred subsocial ancestors, a transition expected to have been hindered by inbreeding depression. As a window into this transition, we examined the fitness consequences of artificially imposed inbreeding in the naturally outbred subsocial spider Anelosimus cf. jucundus. Subsocial spiders alternate periods of solitary and social living and are thought to resemble the ancestral system from which the inbred social species originated. We found that inbreeding depression in this subsocial spider only becomes evident in spiders raised individually following the end of their social phase and that ecological and demographic factors such as eclosion date, number of siblings in the group and mother's persistence are more powerful determinants of fitness during the social phase. A potential explanation for this pattern is that maternal care and group living provide a buffer against inbreeding depression, a possibility that may help explain the repeated origin of inbred social systems in spiders and shed light on the origin of other systems involving regular inbreeding.