Assessing the repeatability,robustness to disturbance,and parent–offspring colony resemblance of collective behavior

Groups of animals possess phenotypes such as collective behaviour, which may determine the fitness of group members. However, the stability and robustness to perturbations of collective phenotypes in natural conditions is not established. Furthermore, whether group phenotypes are transmitted from parent to offspring groups with fidelity is required for understanding how selection on group phenotypes contributes to evolution, but parent–offspring resemblance at the group level is rarely estimated. We evaluated the repeatability, robustness to perturbation and parent–offspring resemblance of collective foraging aggressiveness in colonies of the social spider Anelosimus eximius. Among‐colony differences in foraging aggressiveness were consistent over time but changed if the colony was perturbed through the removal of individuals or via individuals’ removal and subsequent return. Offspring and parent colony behaviour were correlated at the phenotypic level, but only once the offspring colony had settled after being translocated, and the correlation overlapped with zero at the among‐colony level. The parent–offspring resemblance was not driven by a shared elevation but could be due to other environmental factors. The behaviour of offspring colonies in a common garden laboratory setting was not correlated with the behaviour of the parent colony nor with the same colony's behaviour once it was returned to the field. The phenotypes of groups represent a potentially important tier of biological organization, and assessing the stability and heritability of such phenotypes helps us better understand their role in evolution.     

Population genetic evidence for sex‐specific dispersal in an inbred social spider

Dispersal in most group‐living species ensures gene flow among groups, but in cooperative social spiders, juvenile dispersal is suppressed and colonies are highly inbred. It has been suggested that such inbred sociality is advantageous in the short term, but likely to lead to extinction or reduced speciation rates in the long run. In this situation, very low levels of dispersal and gene flow among colonies may have unusually important impacts on fitness and persistence of social spiders. We investigated sex‐specific differences in dispersal and gene flow among colonies, as reflected in the genetic structure within colonies and populations of the African social spider Stegodyphus dumicola Pocock, 1898 (Eresidae). We used DNA fingerprinting and mtDNA sequence data along with spatial mapping of colonies to compare male and female patterns of relatedness within and among colonies at three study sites. Samples were collected during and shortly after the mating season to detect sex‐specific dispersal. Distribution of mtDNA haplotypes was consistent with proliferation of social nests by budding and medium‐ to long‐distance dispersal by ballooning females. Analysis of molecular variance and spatial autocorrelation analyses of AFLPs showed high levels of genetic similarity within colonies, and STRUCTURE analyses revealed that the number of source populations contributing to colonies ranged from one to three. We also showed significant evidence of male dispersal among colonies at one site. These results support the hypothesis that in social spiders, genetic cohesion among populations is maintained by long‐distance dispersal of female colony founders. Genetic diversity within colonies is maintained by colony initiation by multiple dispersing females, and adult male dispersal over short distances. Male dispersal may be particularly important in maintaining gene flow among colonies in local populations.     

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.     

Prey Capture and Feeding in the Social Spider Anelosimus eximius

Wild colonies of the social spider Anelosimus eximius (Araneae, Theridiidae) appear often to be food-limited and not all females come to reproduction. Using a limited number of marked females in an artificial colony, set up in the laboratory, this study attempts a first analysis of the participation in prey capture and ingestion. Marked females of the same age and experience were observed during the attack of prey insects, the ensuing transportation of the prey to the retreat, and the feeding session. No correlation was found between the time females spent hunting and the time they spent feeding. Females that laid eggs had fed longer and imbibed more nutrients, but had not hunted more than those females that did not reproduce. These, it is speculated, were denied access to the prey by the reproducing females.     

Personality composition is more important than group size in determining collective foraging behaviour in the wild

Describing the factors that shape collective behaviour is central to our understanding of animal societies. Countless studies have demonstrated an effect of group size in the emergence of collective behaviours, but comparatively few have accounted for the composition/diversity of behavioural phenotypes, which is often conflated with group size. Here, we simultaneously examine the effect of personality composition and group size on nest architecture and collective foraging aggressiveness in the social spider Stegodyphus dumicola. We created colonies of two different sizes (10 or 30 individuals) and four compositions of boldness (all bold, all shy, mixed bold and shy, or average individuals) in the field and then measured their collective behaviour. Larger colonies produced bigger capture webs, while colonies containing a higher proportion of bold individuals responded to and attacked prey more rapidly. The number of attackers during collective foraging was determined jointly by composition and size, although composition had an effect size more than twice that of colony size: our results suggest that colonies of just 10 bold spiders would attack prey with as many attackers as colonies of 110 ‘average’ spiders. Thus, personality composition is a more potent (albeit more cryptic) determinant of collective foraging in these societies.     

Relationship between prey consumption and colony size in an orb spider

Summary I studied the relationship between prey consumption and colony size in the orb spiderPhiloponella semiplumosa. Observations of unmanipulated colonies showed that prey biomass per juvenile spider was positively correlated with colony size, indicating that prey consumption was highest in the largest colonies observed. In contrast, the relationship between prey biomass per adult female and colony size was curvilinear; prey consumption tended to be highest in intermediatesized colonies. Adult female cephalothorax width was positively correlated with colony size. Number of egg sacs per adult female tended to be highest in intermediate-sized colonies. Prey biomass per juvenile was lower in experimentally reduced colonies than in large control colonies. Aerial-arthropod abundance was not correlated with colony size, and experimental prey supplementation did not affect colony size. Thus, the relationship between prey consumption and colony size was influenced by coloniality directly, rather than by a correlation between prey abundance at a site and colony size.     

The legacy effects of keystone individuals on collective behaviour scale to how long they remain within a group

The collective behaviour of social groups is often strongly influenced by one or few individuals, termed here ‘keystone individuals’. We examined whether the influence of keystone individuals on collective behaviour lingers after their departure and whether these lingering effects scale with their tenure in the group. In the social spider, Stegodyphus dumicola, colonies'' boldest individuals wield a disproportionately large influence over colony behaviour. We experimentally manipulated keystones'' tenure in laboratory-housed colonies and tracked their legacy effects on collective prey capture following their removal. We found that bolder keystones caused more aggressive collective foraging behaviour and catalysed greater inter-individual variation in boldness within their colonies. The longer keystones remained in a colony, the longer both of these effects lingered after their departure. Our data demonstrate that, long after their disappearance, keystones have large and lasting effects on social dynamics at both the individual and colony levels.     

Choice of nest site protects army ant colonies from environmental extremes in tropical montane forest

Unlike most social insects, Eciton burchellii army ants cannot thermoregulate through nest construction. Instead, army ants thermoregulate behaviorally by creating a living nest (bivouac), shifting its position and structure, and potentially through nest site selection. We hypothesized that bivouac site selection is critical to E. burchellii colony survival. We predicted elevation above sea level, with associated variation in local abiotic environments, would affect bivouac site selection by E. burchellii colonies. We also expected nest sites to buffer against ambient variation in abiotic conditions. We recorded bivouac site choice by E. burchellii colonies at sites ranging from lowland wet forests to montane forests and reviewed previously published data. We measured microclimatic variables associated with nest sites in high-elevation montane forests: temperature, relative humidity, and light levels. Bivouac site selection varied with elevation: as elevation increased, fewer bivouac sites were exposed, more were underground, and fewer were elevated (in trees). High-elevation bivouac sites moderated diurnal temperature variation and had higher relative humidity levels and lower light levels than ambient conditions. The buffering of ambient temperature and humidity decreased with elevation in montane forests, suggesting that abiotic extremes in bivouac sites at the highest elevations may contribute to the upper elevational range limits of E. burchellii.     

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.     

Individual and Group Personalities Characterise Consensus Decision‐Making in an Ant

Non‐human animals can exhibit idiosyncratic behaviour across individuals in much in the same way as humans. Animals with specific personalities may have advantages in some environments, and this idiosyncrasy may thus be of considerable ecological and evolutionary importance. In group‐living organisms, personality can occur at the level of the group as well as that of the individual. However, at present, we have very little understanding of the possible benefits of group‐level personality, and how this is linked with individual personality. In this study, I examine the influence of individual and group personality during the process of colony migration in the Japanese ant, Myrmecina nipponica. These ants use a consensus decision process to decide among alternatives when searching for a new home. Individuals contribute to this process by scouting for new nest sites, recruiting nestmates by laying pheromone trails, and carrying brood to the new site, although whether these roles are consistent among individuals and how roles are distributed within and between colonies remain unclear. Individual contributions to the nest‐site selection process were quantified over five repeated relocations in five colonies. Results demonstrate that contributions to the relocation effort were highly skewed within the colonies and that individuals were consistent in their contributions over repeated relocation events. Furthermore, the distribution of effort differed between colonies, indicating that intercolony differences in composition of behavioural types resulted in colony‐level personality. While these differences did not lead to any detectable difference in relocation performance between colonies in the simple experimental arrangement used, colony personality could influence decision outcomes in more complex environments.     

Intraspecific variation in size and density of Avocet colonies: effects of nest-distances on hatching and breeding success

In many colonial bird species there is considerable intraspecific variation in colony size and inter‐nest distance (colony density). Possible causes of this variation and its effects on hatching success (survival of eggs) and breeding success (probability of a pair raising chicks) were studied in 48 Avocet Recurvirostra avosetta colonies in Schleswig‐Holstein (Germany) between 1991 and 1996. Colony density was influenced by time of year and habitat (categories: island or mainland, close to or far from feeding grounds). Colonies on islands had the highest densities. When all available space at a colony site was used, colonies became very dense (mean nearest‐neighbour nest distance less than 1 m). Colony size (number of clutches) was influenced by time of year, but not by habitat. Hatching success was low in high density colonies and in very low density ‘colonies’ (single nests) and high over a broad range of intermediate nest densities. The low success rate of single nests was caused by a very high predation rate, whereas the low success rate in very dense colonies was caused by a high rate of nest abandonment. Nest abandonment in very dense colonies was associated with a high level of aggressiveness among Avocets during the egg‐laying period. Due to territorial behaviour, Avocets seemed to be expelled from the densest breeding sites. In very dense colonies, high frequencies of clutches of unusual size occurred due to conspecific nest parasitism. The number of Avocets taking part in attacks on potential egg predators was small and (in colonies of more than one clutch) depended neither on colony size nor on colony density. Despite a low hatching success in very dense colonies, individuals breeding in the densest colonies had significantly better chances of raising chicks than Avocets breeding in less dense colonies. Coloniality seemed to be obligatory for Avocets in order to ensure hatching success. The size and density of colonies seemed to be associated with the availability of suitable nesting habitats (islands).     

Local population success in heterogeneous habitats: reciprocal transplant experiments completed on a desert spider

Reciprocal transplant experiments were completed to test for selection against the mixing of behavioural phenotypes in a desert spider. Most Agelenopsis aperta populations experience low prey abundances and competition for web‐sites that provide shelter from thermal extremes. These conditions favour aggressiveness towards both prey and conspecifics (an ‘arid‐land behavioural phenotype’). The spider also occupies narrow stretches of riparian habitat bordering spring‐fed streams and rivers. Here it is released from competition for prey and foraging sites, but is subject to predation by birds. A less aggressive/more fearful behaviour is selected for in these riparian habitats (a ‘riparian behavioural phenotype’). Previous work with this spider indicates that there is genetic differentiation between arid‐land and riparian populations. However, the degree to which genetic differentiation is achieved may be limited by gene flow. Reciprocal sets of enclosures were established in: (1) a dry evergreen woodland site (arid‐land phenotype) and (2) a neighbouring riparian site (riparian phenotype) in south‐eastern Arizona. Equal numbers of field collected, early instar A. aperta were introduced into native and transplant enclosures in each habitat. After 6 months of site‐imposed selection, survivorship was determined and growth estimates and behavioural trials completed on spiders remaining in the different enclosures. The same behavioural test was subsequently applied to lab‐reared offspring of the spiders surviving the respective selection regimes. Riparian transplants showed both poor survival and retarded growth in the dry woodland habitat when compared with both arid‐land and riparian natives. Arid‐land transplants that survived, however, grew equally well in riparian habitat as did dry woodland and riparian natives. Behavioural assays conducted on test subjects after selection and on their offspring reared in a controlled laboratory environment indicate that phenotypes that were inappropriate to the respective habitats were selected against in the transplant experiments. The frequency distribution of transplant spider behaviour on a continuum from fearful to aggressive was intermediate between that exhibited by respective native riparian and dry woodland spiders. It is concluded that while arid‐land and riparian behavioural ecotypes do exist, directional gene flow of arid‐land phenotypes into riparian habitat limits population subdivision.     

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.     

Bottom‐up processes in a declining yellow‐footed rock‐wallaby (Petrogale xanthopus celeris) population

Populations of large herbivores are generally considered to be food limited, escaping the regulatory effects of predation through their large body size, migratory behaviour and/or the occurrence of alternate prey species. In the Australian arid and semi‐arid zones, the availability of forage biomass is considered to be the primary driver of fluctuations in kangaroo abundance. However, little is known about the population dynamics of the smaller sympatric macropods. We examined the demographic traits of a large colony of yellow‐footed rock‐wallabies (Petrogale xanthopus celeris), following a 2‐year period of above average rainfall. The population was located within a conservation reserve that was subject to a predator control program around its perimeter and on neighbouring properties. The low predator abundance provided an opportunity to gauge the strength of bottom‐up population processes. During the two years of the study, the population declined in size by 53%, resulting from both the virtual absence of juvenile recruitment and the loss of adult wallabies. Although reproductive output was high, low pouch young and juvenile survival rates resulted in few individuals progressing into the adult population. With minimal recruitment, the rate of population decline (r = 0.77) matched the observed adult survival rate (Φ = 0.76). Despite average rainfall conditions during the study, survival rates across all age‐classes were equivalent to those reported for other rock‐wallaby populations during periods of scarcity. The reduced survival rates were attributed to low levels of forage resources, particularly around the wallabies' refuge sites, suggesting the bottom‐up regulation of the colony at high densities. The data suggest that the colony was at temporarily high abundance, following a rainfall driven pulse of recruitment. Conservation management actions for this species should focus on increasing juvenile survival rates within declining populations, through the control of feral goats (Capra hircus), rabbits (Oryctolagus cuniculus) and red foxes (Vulpes vulpes).     

Variation in age composition among colony sizes in Cliff Swallows

Variation in group size is characteristic of most social species. The extent to which individuals sort among group sizes based on age may yield insight into why groups vary in size and the age‐specific costs and benefits of different social environments. We investigated the age composition of Cliff Swallow (Petrochelidon pyrrhonota) colonies of different sizes over 18 yr at a long‐term study site in western Nebraska, USA. Using years elapsed since banding as a relative measure of age for over 194,000 birds, we found that the proportion of age‐class‐1 swallows (birds banded as nestlings or juveniles or adults in the year of banding) of both sexes increased in larger colonies and at colony sites becoming active later in the summer. Age composition was unrelated to how often a particular colony site was used. The effect of colony size most likely reflected the fact that older birds return to the same colony site in successive years even when the colony size there decreases, and that yearlings and immigrants benefit more from larger colonies than do older, more experienced individuals. The date effect probably resulted in part from later spring arrival by younger and/or immigrant swallows. At fumigated sites where ectoparasitic swallow bugs (Oeciacus vicarius) had been removed, age composition did not vary with either colony size or colony initiation date. The patterns reported here appear to be driven partially by the presence of ectoparasites and suggest that the hematophagous bugs influence variation in Cliff Swallow group composition. Our results are consistent with the hypothesis that variation in colony size reflects, in part, age‐based sorting of individuals among groups.     

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.     

Evaluating environmental,demographic and genetic effects on population‐level survival in an island endemic

The population dynamics of island species are considered particularly sensitive to variation in environmental, demographic and/or genetic processes. However, few studies have attempted to evaluate the relative importance of these processes for key vital rates in island endemics. We integrated the results of long‐term capture–mark–recapture analysis, prey surveys, habitat quality assessments and molecular analysis to determine the causes of variation in the survival rates of Komodo dragons Varanus komodoensis at 10 sites on four islands in Komodo National Park, Indonesia. Using open population capture–mark–recapture methods, we ranked competing models that considered environmental, ecological, genetic and demographic effects on site‐specific Komodo dragon survival rates. Site‐specific survival rates ranged from 0.49 (95% CI: 0.33–0.68) to 0.92 (0.79–0.97) in the 10 study sites. The three highest‐ranked models (i.e. ΔQAIC_c < 2) explained ～70% of variation in Komodo dragon survival rates and identified interactions between inbreeding coefficients, prey biomass density and habitat quality as important explanatory variables. There was evidence of additive effects from ecological and genetic (e.g. inbreeding) processes affecting Komodo dragon survival rates. Our results indicate that maintaining high ungulate prey biomass and habitat quality would enhance the persistence of Komodo dragon populations. Assisted gene flow may also increase the genetic and demographic viability of the smaller Komodo dragon populations.     

A specialized araneophagic predator's short‐term nutrient utilization depends on the macronutrient content of prey rather than on prey taxonomic affiliation

A specialist predator that has a specialized diet, prey‐specific prey‐capture behaviour and a preference for a particular type of prey may or may not be specialized metabolically. Previous studies have shown that jumping spiders of the genus Portia prey on other spiders using prey‐specific prey‐capture behaviour, prefer spiders as prey to insects and gain long‐term benefits in terms of higher survival and growth rates on spider diets than on insect diets. However, it is unclear whether there are substances uniquely present in spiders on which Portia depends, or, alternatively, spiders and insects all contain more or less the same nutrients but the relative amounts of these substances are such that Portia perform better on a spider diet. These questions are addressed by testing the hypothesis that prey specialization includes metabolic adaptations that allow Portia an enhanced nutrient extraction or nutrient utilization efficiency when feeding on spider prey compared with insect prey. Three groups of Portia quei Zabka are fed either their preferred spider prey or one of two types of flies (Drosophila melanogaster Meigen) that differ in nitrogen and lipid content. Portia quei shows a higher feeding rate of high‐protein flies than of high‐lipid flies and spiders but, after 5 days of feeding, there is no significant difference in growth between treatments, and the diets lead to significant changes in the macronutrient composition of P. quei as a result of variable extraction and utilization of the prey. The short‐term utilization of spider prey is similar to that of high‐lipid flies and both differ in several respects from the utilization of high‐protein flies. Thus, the short‐term nutrient utilization is better explained by prey macronutrient content than by whether the prey is a spider or not. The results suggest that spider prey may have a more optimal macronutrient composition for P. quei and that P. quei does not depend on spider‐specific substances.     

Safety first: terrestrial predators drive selection of highly specific nesting sites in colonial‐breeding birds

Nesting is a critical yet hazardous life stage for many birds. For colonial‐breeding birds, the conspicuousness of the colony to predators suggests immense pressure to select optimal colonial nesting sites. But what drives selection of those sites? As with solitary nesting birds, reducing access by predators may be the single most important factor. If so, knowledge of the predators involved and the attributes of different potential colony sites can allow us to predict the features that make a site especially safe. We examined the attributes of trees used by breeding colonies of metallic starlings Aplonis metallica in tropical Australia, and experimentally tested if those attributes prevented nest access by predatory snakes. Our surveys confirmed that tree choice by starling nesting colonies is highly non‐random, with all colonies located in tall trees in rainforest clearings, with no low branches and smooth bark. Experimental tests demonstrated that the climbing ability of predatory snakes depends upon bark rugosity, and that colony access by snakes depends on tree attributes such as bark rugosity and canopy connectivity. Our study confirms that colonial‐nesting starlings select colony sites that provide a safe refuge from predation. Intense predation pressure may have driven the evolution of stringent breeding habitat criteria in many other species of colonial‐breeding birds.     

Developmental changes in factors limiting colony survival and growth of the leaf‐cutter ant Atta laevigata

Many species of leaf‐cutter ants (Atta and Acromyrmex) increase in abundance following natural or anthropogenic disturbances in the vegetation. However, the mechanisms responsible for such an increase are still poorly understood. We evaluated the effects of nesting site and the availability of palatable forage on survival and growth of Atta laevigata colonies at different developmental stages. Foundress queens transplanted into man‐made clearings (dirt roads) had a much higher survival than those transplanted into the adjacent undisturbed savannah vegetation. Similarly, incipient colonies (≥3‐months old) had significantly greater survival and growth rates in dirt roads. In contrast, nesting site did not influence performance of young colonies (≥15‐months old). Both incipient and young colonies responded strongly and positively to experimental supplementation of palatable forage, and this effect was independent of the nesting habitat. Colonies that received extra food grew faster and had a significantly greater survival rate than control colonies. These results suggest that performance of A. laevigata is affected by the generally greater availability of suitable nesting sites and palatable vegetation in disturbed habitats. This may explain how these ants maintain high densities in these habitats, and since the relative importance of these factors changed with colony ontogeny, our findings highlight the importance of evaluating potential limiting factors throughout the full range of an organism's developmental stages.