The effects of plastic additives on swimming activity and startle response in marine amphipod Echinogammarus marinus.

Plastic additives are widely used in plastic production and are found in the environment owing to their widespread applications. Among these additives, N-butyl benzenesulfonamide (NBBS) and triphenyl phosphate (TPHP) are under international watchlist for evaluation, with limited studies on amphipods. Di-ethylhexyl phthalate (DEHP) and dibutyl phthalate (DBP) are banned in some countries and categorised as substances of very high concern. This study aimed to investigate the effects of NBBS, TPHP, DEHP and DBP on the swimming activity of a coastal intertidal marine amphipod, Echinogammarus marinus. Furthermore, this study is the first to quantify startle response in E. marinus in response to light stimuli. Amphipods were exposed to 0, 0.5, 5, 50 and 500 µg/l concentrations of all test compounds. Swimming activity and startle responses were assessed by video tracking and analysis using an 8-min alternating dark and light protocol after exposure on days 7 and 14. We observed an overall compound and light effect on the swimming activity of E. marinus. A significant decrease in swimming distance was found in 500 µg/l NBBS and TPHP. We observed that the startle response in E. marinus had a latency period of >2 s and animals were assessed at 1 s and the sum of the first 5 s. There was a clear startle response in E. marinus during dark to light transition, evident with increased swimming distance. NBBS exposure significantly increased startle response at environmental concentrations, while significant effects were only seen in 500 µg/l TPHP at 5 s. We found no significant effects of DEHP and DBP on swimming behaviour at the concentrations assessed. The findings of this study affirm the necessity for a continuous review of plastic additives to combat adverse behavioural effects that may be transferable to the population levels.

Evaluation of precopulatory pairing behaviour and male fertility in a marine amphipod exposed to plastic additives.

Plastics contain a mixture of chemical additives that can leach into the environment and potentially cause harmful effects on reproduction and the endocrine system. Two of these chemicals, N-butyl benzenesulfonamide (NBBS) and triphenyl phosphate (TPHP), are among the top 30 organic chemicals detected in surface and groundwater and are currently placed on international watchlist for evaluation. Although bans have been placed on legacy pollutants such as diethylhexyl phthalate (DEHP) and dibutyl phthalate (DBP), their persistence remains a concern. This study aimed to examine the impact of plastic additives, including NBBS, TPHP, DBP, and DEHP, on the reproductive behaviour and male fertility of the marine amphipod Echinogammarus marinus. Twenty precopulatory pairs of E. marinus were exposed to varying concentrations of the four test chemicals to assess their pairing behaviour. A high-throughput methodology was developed and optimised to record the contact time and re-pair time within 15 min and additional point observations for 96 h. The study found that low levels of NBBS, TPHP, and DEHP prolonged the contact and re-pairing time of amphipods and the proportion of pairs reduced drastically with re-pairing success ranging from 75% to 100% in the control group and 0%-85% in the exposed groups at 96 h. Sperm count declined by 40% and 60% in the 50 µg/l and 500 µg/l DBP groups, respectively, whereas TPHP resulted in significantly lower sperms in 50 µg/l exposed group. Animals exposed to NBBS and DEHP showed high interindividual variability in all exposed groups. Overall, this study provides evidence that plastic additives can disrupt the reproductive mechanisms and sperm counts of amphipods at environmentally relevant concentrations. Our research also demonstrated the usefulness of the precopulatory pairing mechanism as a sensitive endpoint in ecotoxicity assessments to proactively mitigate population-level effects in the aquatic environment.

Behaviour, Furnishing and Vertical Space Use of Captive Callimico (Callimico goeldii): Implications for Welfare.

Provision of optimal captive care should be supported by species-specific evidence. Callimico (Callimico goeldii) is a small South American callitrichid primate. This study sought to address gaps in species-specific knowledge and captive management research by examining differences in callimico behaviour across multiple collections, investigating vertical enclosure use and a possible association between specific behaviours and vertical zones. Observational research was conducted at five European Association of Zoos and Aquaria (EAZA) organisations, in exhibits that were visually divided into four vertical zones. Instantaneous scan sampling was used to record behaviour and location of callimico over a six-day period at each collection, exceeding 160 observational hours. Significant differences were observed in foraging between collections and were much lower than the recommendations in Best Practice Guidelines, although near-wild levels were recorded in one enclosure. At an average height of 2 m, callimico utilized a similar vertical space across very different enclosures, regardless of overall available height, reflective of their natural ecology. The association between whole food items and increased foraging time, horizontal branches and locomotion and deep substrate and diversity of behaviours, offers further species-specific evidence of how the callimico use their captive environment. Our findings complement current EAZA guidelines to support species appropriate care for callimico and makes specific recommendations for further research.

Group-Living Spider Cyrtophora citricola as a Potential Novel Biological Control Agent of the Tomato Pest Tuta absoluta.

Group-living spiders may be uniquely suited for controlling flying insect pests, as their high tolerance for conspecifics and low levels of cannibalism result in large, predator dense capture webs. In laboratory settings, we tested the ability of the facultatively communal spider, Cyrtophora citricola, to control the tomato leafminer, Tuta absoluta; a major pest of tomato crops worldwide. We tested whether prey capture success was affected by spider body size, and whether prey capture differed among T. absoluta, flightless fruit flies (Drosophila hydei), and larger black soldier flies (Hermetia illucens). We found that larger spiders generally caught more prey, and that prey capture success was similar for T. absoluta and easily caught fruit flies, while black soldier flies were rarely caught. We further investigated the seasonal variations in web sizes in southern Spain, and found that pest control would be most effective in the tomato planting and growing season. Finally, we show that C. citricola in Spain have >50% infection rates of an egg predatory wasp, Philolema palanichamyi, which may need controlling to maintain pest control efficacy. These results suggest that using C. citricola as a biological control agent in an integrated pest management system could potentially facilitate a reduction of pesticide reliance in the future.

Prey to predator body size ratio in the evolution of cooperative hunting-a social spider test case.

One of the benefits of cooperative hunting may be that predators can subdue larger prey. In spiders, cooperative, social species can capture prey many times larger than an individual predator. However, we propose that cooperative prey capture does not have to be associated with larger caught prey per se, but with an increase in the ratio of prey to predator body size. This can be achieved either by catching larger prey while keeping predator body size constant, or by evolving a smaller predator body size while maintaining capture of large prey. We show that within a genus of relatively large spiders, Stegodyphus, subsocial spiders representing the ancestral state of social species are capable of catching the largest prey available in the environment. Hence, within this genus, the evolution of cooperation would not provide access to otherwise inaccessible, large prey. Instead, we show that social Stegodyphus spiders are smaller than their subsocial counterparts, while catching similar sized prey, leading to the predicted increase in prey-predator size ratio with sociality. We further show that in a genus of small spiders, Anelosimus, the level of sociality is associated with an increased size of prey caught while predator size is unaffected by sociality, leading to a similar, predicted increase in prey-predator size ratio. In summary, we find support for our proposed 'prey to predator size ratio hypothesis' and discuss how relaxed selection on large body size in the evolution of social, cooperative living may provide adaptive benefits for ancestrally relatively large predators.

Two hymenopteran egg sac associates of the tent-web orbweaving spider, Cyrtophora citricola (Forskål, 1775) (Araneae, Araneidae).

We report the discovery of two wasp species emerging from egg sacs of the spider Cyrtophora citricola (Forskål 1775) collected from mainland Spain and the Canary Islands. We identify one as Philolema palanichamyi (Narendran 1984) (Hymenoptera, Eurytomidae) and the other as a member of the Pediobius pyrgo (Walker 1839) species group (Hymenoptera, Eulophidae). This is the first report of Philolema in Europe, and the first documentation of hymenopteran egg predators of C. citricola. The latter finding is particularly relevant, given the multiple invasive populations of C. citricola in the Americas and the Caribbean, where neither egg sac predation nor parasitism is known to occur. We describe rates of emergence by Ph. palanichamyi from spider egg sacs collected from the southern coast of Spain and estimate sex ratios and body size variation among males and females. We also re-describe Ph. palanichamyi based on the female holotype and male paratype specimens.

Partner choice correlates with fine scale kin structuring in the paper wasp Polistes dominula.

Cooperation among kin is common in animal societies. Kin groups may form by individuals directly discriminating relatives based on kin recognition cues, or form passively through natal philopatry and limited dispersal. We describe the genetic landscape for a primitively eusocial wasp, Polistes dominula, and ask whether individuals choose cooperative partners that are nearby and/or that are genetic relatives. Firstly, we genotyped an entire sub-population of 1361 wasps and found genetic structuring on an extremely fine scale: the probability of finding genetic relatives decreases exponentially within just a few meters of an individual's nest. At the same time, however, we found a lack of genetic structuring between natural nest aggregations within the population. Secondly, in a separate dataset where ~2000 wasps were genotyped, we show that wasps forced experimentally to make a new nest choice tended to choose new nests near to their original nests, and that these nests tended to contain some full sisters. However, a significant fraction of wasps chose nests that did not contain sisters, despite sisters being present in nearby nests. Although we cannot rule out a role for direct kin recognition or natal nest-mate recognition, our data suggest that kin groups may form via a philopatric rule-of-thumb, whereby wasps simply select groups and nesting sites that are nearby. The result is that most subordinate helpers obtain indirect fitness benefits by breeding cooperatively.

Evolutionary drivers of group foraging: A new framework for investigating variance in food intake and reproduction.

A proposed fundamental driver of group living is more reliable, predictable foraging and reproduction, i.e., reduced variance in food intake and reproductive output. However, existing theories on variance reduction in group foraging are simplistic, refer to variance at the level of individuals and groups without linking the two, and do not spell out crucial underlying assumptions. We provide a new, widely applicable framework for identifying when variance reduction conveys fitness benefits of group foraging in a wide range of organisms. We discuss critical limitations of established theories, the Central Limit Theorem and Risk-Sensitive Foraging Theory applied to group foraging, and incorporate them into our framework while addressing the confusion over the levels of variance and identifying previously unaddressed assumptions. Through a field study on colonial spiders, Cyrtophora citricola, we demonstrate the importance of evaluating the level of food sharing as a critical first step, previously overlooked in the literature. We conclude that variance reduction provides selective advantages only under narrow conditions and does not provide a universal benefit to group foraging as previously proposed. Our framework provides an important tool for identifying evolutionary drivers of group foraging and understanding the role of fitness variance in the evolution of group living.

Predictors of nest growth: diminishing returns for subordinates in the paper wasp Polistes dominula.

ABSTRACT: In cooperative breeders, subordinates that have alternative reproductive options are expected to stay and help dominant breeders only as long as they contribute to group productivity, if their fitness is linked with colony success. Female Polistes dominula paper wasps live as cooperative breeders in small groups of typically fewer than 10 females. Subordinates tend to have high-quality outside options, and so could choose alternative breeding tactics if their work efforts increased productivity negligibly. In the founding stage before workers emerge, we tested the effect of various predictors on nest growth, as a proxy for group productivity, and explored the shape of the relationship between group size and nest growth. We found group size to be the only significant predictor of nest growth: variation among body sizes within the group showed no effect, suggesting a lack of size-dependent task specialization in this species. Average body size and average genetic relatedness between group members similarly showed no effects on nest growth. Group size had a non-linear effect so that per-capita benefits to nest growth decreased in larger groups, and groups of 10 or more would benefit negligibly from additional group members. Hence, females might be better off pursuing other options than joining a large group. This finding helps to explain why P. dominula groups are usually relatively small in our study population. Further studies may illuminate the mechanisms behind the smaller per-capita nest growth that we found in larger groups. SIGNIFICANCE STATEMENT: Identifying which factors influence the productivity of animal groups is key to understanding why different species breed cooperatively in groups of varying sizes. In the paper wasp Polistes dominula, we investigated the growth rate of nests as a measure of group productivity. We found that average body size, the variation in body sizes within the group, and average genetic relatedness between group members did not affect nest growth, while group size had a strong, positive effect: nests grew faster with more group members, but the per-capita benefit decreased in larger groups. The addition of extra group members in groups of 10 or more had negligible effects on nest growth. Hence, wasps may be better off pursuing other options than joining large groups. This finding helps to explain why groups normally consist of fewer than 10 wasps in this population.

Biological markets in cooperative breeders: quantifying outside options.

A major aim in evolutionary biology is to understand altruistic help and reproductive partitioning in cooperative societies, where subordinate helpers forego reproduction to rear dominant breeders' offspring. Traditional models of cooperation in these societies typically make a key assumption: that the only alternative to staying and helping is solitary breeding, an often unfeasible task. Using large-scale field experiments on paper wasps (Polistes dominula), we show that individuals have high-quality alternative nesting options available that offer fitness payoffs just as high as their actual chosen options, far exceeding payoffs from solitary breeding. Furthermore, joiners could not easily be replaced if they were removed experimentally, suggesting that it may be costly for dominants to reject them. Our results have implications for expected payoff distributions for cooperating individuals, and suggest that biological market theory, which incorporates partner choice and competition for partners, is necessary to understand helping behaviour in societies like that of P. dominula Traditional models are likely to overestimate the incentive to stay and help, and therefore the amount of help provided, and may underestimate the size of reproductive concession required to retain subordinates. These findings are relevant for a wide range of cooperative breeders where there is dispersal between social groups.

Market forces influence helping behaviour in cooperatively breeding paper wasps.

Biological market theory is potentially useful for understanding helping behaviour in animal societies. It predicts that competition for trading partners will affect the value of commodities exchanged. It has gained empirical support in cooperative breeders, where subordinates help dominant breeders in exchange for group membership, but so far without considering one crucial aspect: outside options. We find support for a biological market in paper wasps, Polistes dominula. We first show that females have a choice of cooperative partners. Second, by manipulating entire subpopulations in the field, we increase the supply of outside options for subordinates, freeing up suitable nesting spots and providing additional nesting partners. We predicted that by intensifying competition for help, our manipulation would force dominants to accept a lower price for group membership. As expected, subordinates reduce their foraging effort following our treatments. We conclude that to accurately predict the amount of help provided, social units cannot be viewed in isolation: the surrounding market must also be considered.

Animal behaviour: task differentiation by personality in spider groups.

In social animals, group efficiency is often assumed to increase with task differentiation, but this requires that individuals are better than generalists at the task they specialize in. A new study finds that individual Anelosimus studiosus spiders do predominantly perform the task they excel at, in line with their individual personality type, when they are placed in groups.

Cooperative breeding favors maternal investment in size over number of eggs in spiders.

The transition to cooperative breeding may alter maternal investment strategies depending on density of breeders, extent of reproductive skew, and allo-maternal care. Change in optimal investment from solitary to cooperative breeding can be investigated by comparing social species with nonsocial congeners. We tested two hypotheses in a mainly semelparous system: that social, cooperative breeders, compared to subsocial, solitarily breeding congeners, (1) lay fewer and larger eggs because larger offspring compete better for limited resources and become reproducers; (2) induce egg size variation within clutches as a bet-hedging strategy to ensure that some offspring become reproducers. Within two spider genera, Anelosimus and Stegodyphus, we compared species from similar habitats and augmented the results with a mini-meta-analysis of egg numbers depicted in phylogenies. We found that social species indeed laid fewer, larger eggs than subsocials, while egg size variation was low overall, giving no support for bet-hedging. We propose that the transition to cooperative breeding selects for producing few, large offspring because reproductive skew and high density of breeders and young create competition for resources and reproduction. Convergent evolution has shaped maternal strategies similarly in phylogenetically distant species and directed cooperatively breeding spiders to invest in quality rather than quantity of offspring.

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.

Subsocial behaviour and brood adoption in mixed-species colonies of two theridiid spiders.

Cooperation and group living often evolves through kin selection. However, associations between unrelated organisms, such as different species, can evolve if both parties benefit from the interaction. Group living is rare in spiders, but occurs in cooperative, permanently social spiders, as well as in territorial, colonial spiders. Mixed species spider colonies, involving closely related species, have rarely been documented. We examined social interactions in newly discovered mixed-species colonies of theridiid spiders on Bali, Indonesia. Our aim was to test the degree of intra- and interspecific tolerance, aggression and cooperation through behavioural experiments and examine the potential for adoption of foreign brood. Morphological and genetic analyses confirmed that colonies consisted of two related species Chikunia nigra (O.P. Cambridge, 1880) new combination (previously Chrysso nigra) and a yet undescribed Chikunia sp. Females defended territories and did not engage in cooperative prey capture, but interestingly, both species seemed to provide extended maternal care of young and indiscriminate care for foreign brood. Future studies may reveal whether these species adopt only intra-specific young, or also inter-specifically. We classify both Chikunia species subsocial and intra- and interspecifically colonial, and discuss the evolutionary significance of a system where one or both species may potentially benefit from mutual tolerance and brood adoption.

Wax on, wax off: nest soil facilitates indirect transfer of recognition cues between ant nestmates.

Social animals use recognition cues to discriminate between group members and non-members. These recognition cues may be conceptualized as a label, which is compared to a neural representation of acceptable cue combinations termed the template. In ants and other social insects, the label consists of a waxy layer of colony-specific hydrocarbons on the body surface. Genetic and environmental differences between colony members may confound recognition and social cohesion, so many species perform behaviors that homogenize the odor label, such as mouth-to-mouth feeding and allogrooming. Here, we test for another mechanism of cue exchange: indirect transfer of cuticular hydrocarbons via the nest material. Using a combination of chemical analysis and behavioral experiments with Camponotus aethiops ants, we show that nest soil indirectly transfers hydrocarbons between ants and affects recognition behavior. We also found evidence that olfactory cues on the nest soil influence nestmate recognition, but this effect was not observed in all colonies. These results demonstrate that cuticular hydrocarbons deposited on the nest soil are important in creating uniformity in the odor label and may also contribute to the template.