bioRxiv Science⌕ Search

Biology subjects

Pinter-Wollman, N.

Publications and source records attributed to Pinter-Wollman, N..

12 recordsLinked to original sources

Factors affecting the individual probability of infection with a prevalent pathogen (Mycoplasma) and the effect on Griffon vultures' movement behavior

Mycoplasmas are known as commensals and pathogenic bacteria of various raptor species causing clinical or subclinical infections. However, little is known about the prevalence of mycoplasma in captive and wild raptors and its significance to their health. In Israel, the Griffon vulture (Gyps fulvus; hereafter Griffons) is considered critically endangered, and its intensive management program includes population monitoring and restocking (captive-born or imported rehabilitated wild Spanish Griffons). Here we survey the prevalence of Mycoplasma species in both the wild and captive populations. During 2019-2020, we collected 244 tracheal swab samples from 167 unique individuals. We used PCR analysis to identify Mycoplasma species. First, we identified nine spp., including species not yet described in Israel or for Griffon vultures. Second, imported Griffons showed a higher prevalence and a different diversity of species in comparison to the local ones, suggesting that at least one Mycoplasma species (Sp 18b) was introduced into the native population. Third, juvenile Griffons had a higher prevalence, different species composition, and stronger reduction in movement compared to adults, confirming the susceptibility of this group to mycoplasma infections. GPS-tracking of 60 free-ranging individuals showed that even in the absence of apparent clinical signs, Griffons infected with mycoplasma, and especially sub-adults flew less (shorter distances and periods). These findings underscore the importance of considering potential pathogen introductions in population reinforcement and reintroduction initiatives, providing valuable insights for similar conservation programs globally. Further, they demonstrate the potential of long-term tracking for detecting subclinical effects that are unnoticeable in clinical examination.

ecology↗

Extreme temperatures impede the release success of captive-bred avian scavengers

Conservation translocations (reinforcements and reintroductions) are central for managing various endangered species, yet, their implementation is logistically and financially challenging. Because many translocations fail due to the mortality of released individuals, identifying and preventing these factors is crucial. Here we examine risk factors affecting the post-release survival of the Griffon vulture (Gyps fulvus). The Israeli population is facing extinction, and the recovery efforts by the local Nature and Parks Authority include supplemental releases of individuals from captive-breeding or rehabilitated birds (mostly imported from Spain). We use GPS tracking and thermometers to compare movement, behavior, and weather conditions experienced by released and wild-born individuals active in the same area and time. Our results show that the Judean Desert release site had a significantly lower survival rate than other release sites included in the program. After excluding several possible factors (e.g. known pathogens) with pathological examinations, we found that released individuals at this area were exposed to higher temperatures preceding their death (compared to wild-born griffons nearby), suggesting heat stress as the cause of death. Arguably, they failed to avoid the harsh environmental conditions, resulting in overheating due to their inexperience and undeveloped flight ability, as reflected by their lower probabilities of flying and shorter travel distances per day compared to wild-born vultures. These findings have led to adjustments of the local release protocol, (namely winter releases) resulting in a significant improvement in the early survival of translocated Griffons in the Judean Desert. Accounting for the harmful effects of extreme weather conditions is particularly important in a world facing climate change. More broadly, this sequence of scientific investigation with data integration from ecological, clinical, and biotelemetry sources, leading to improvement in translocation success demonstrates how conservation practices can be optimized by supporting studies to ensure the survival of endangered species in the wild.

ecology↗

Social interactions are impacted by food availability, food type, and group size

Social interactions are important for how societies function, conferring robustness and resilience to environmental changes. The structure of social interactions can shape the dynamics of information and goods transmission. In addition, the availability and type of resources that are transferred might impact the structure of interaction networks. For example, storable resources might reduce the required speed of distribution and altering interaction structure can facilitate such change. Here we use ants as a model system to examine how social interactions are impacted by group size, food availability, and food type. We compare global- and individual-level network measures across experiments in which groups of different sizes received limited or unlimited food that is either favorable and cannot be stored (carbohydrates), or unfavorable but with a potential of being stored (protein). We found that as group size increased, individuals interacted with more social partners and interaction networks became more compartmentalized. Furthermore, group compartmentalization increased when food was limited and when transferring storable goods. Our findings highlight how biological systems can adjust their interaction networks in ways that relate to their function. The study of such biological flexibility can inspire novel and important solutions to the design of robust and resilient supply chains.

animal behavior and cognition↗

Modularity and connectivity of nest structure scale with colony size

Large body sizes have evolved structures to facilitate resource transport. Like unitary organisms, social insect colonies must transport information and resources. Colonies with more individuals may experience transport challenges similar to large-bodied organisms. In ant colonies, transport occurs in the nest, which may consist of structures that facilitate movement. We examine three attributes of nests that might have evolved to mitigate transport challenges related to colony size: (1) subdivision - nests of species with large colonies are more subdivided to reduce crowd viscosity; (2) branching - nest tunnels increase branching in species with large colonies to reduce travel distances; and (3) short-cuts - nests of species with large colonies have cross-linking tunnels to connect distant parts of the nest and create alternative routes. We test these hypotheses by comparing nest structures of species with different colony sizes in phylogenetically controlled meta-analyses. Our findings support the hypothesis that nest subdivision and branching evolved to mitigate transport challenges related to colony size. Nests of species with large colonies contain more chambers and branching tunnels. The similarity in how ant nests and bodies of unitary organisms have evolved in response to increasing size suggests common solutions across taxa and levels of biological organization.

evolutionary biology↗

The effect of individual learning on collective foraging in honey bees in complex environments

The trade-off between exploiting known resources and exploring for new ones is a complex decision-making challenge, particularly when resource patches are variable in quality and heterogeneously distributed in the landscape. Social insect colonies navigate this challenge, in the absence of centralized control, by allocating different individuals to each of these tasks based on variation in individual behavior. To investigate how heritable differences in individual learning affect a colonys collective ability to locate and choose among different quality food resources, we develop an agent based model and test its predictions using two genetic lines of honey bees, selected for differences in their learning behavior. Here we show that, paradoxically, colonies containing individuals that are better at learning to ignore unrewarding stimuli are worse at choosing the highest quality resource at the collective level. This work highlights the importance of individual variation within groups on the emergence of collective behavior.

animal behavior and cognition↗

Comparative genomics identifies putative signatures of sociality in spiders

Comparative genomics has begun to elucidate the genomic basis of social life in insects but insight into the genomic basis of spider sociality has lagged behind. To begin to characterize genomic signatures associated with the evolution of social life in spiders, we performed one of the first spider comparative genomics studies including five solitary species and two social species, representing two independent origins of sociality in the genus Stegodyphus. We found that the two social spider species had a large expansion of gene families associated with transport and metabolic processes and an elevated genome-wide rate of molecular evolution compared with the five solitary spider species. Genes that were rapidly evolving in the two social species relative to the five solitary species were enriched for transport, behavior, and immune functions, while genes that were rapidly evolving in the solitary species were enriched for energy metabolism processes. Most rapidly evolving genes in the social species S. dumicola were broadly expressed across four tissues and enriched for transport functions, but 12 rapidly evolving genes showed brain-specific expression and were enriched for social behavioral processes. Altogether, our study identifies putative genomic signatures and potential candidate genes associated with spider sociality. These results indicate that future spider comparative genomic studies, including broader sampling and additional independent origins of sociality, can further clarify the genomic causes and consequences of social life.

evolutionary biology↗

Heritable Variation in Learning Phenotypes Drive Collective Cognition

Variation in cognition can influence how individuals respond to and communicate about their environment, which may scale to shape how a collective solves a cognitive task. However, few empirical examples of variation in collective cognition emerges from variation in individual cognition exist. Here, we show that interactions among individuals that differ in the performance of a cognitive task drives collective foraging behavior in honey bee colonies by utilizing a naturally variable and heritable learning behavior called latent inhibition (LI). We artificially selected two distinct phenotypes: high LI bees that are better at ignoring previously unrewarding familiar stimuli, and low LI bees that can learn previously unrewarding and novel stimuli equally well. We then provided colonies composed of these distinct phenotypes with a choice between a familiar feeder or a novel feeder. Colonies of high LI individuals preferred to visit familiar food locations, while low LI colonies visited novel and familiar food locations equally. However, in colonies of mixed learning phenotypes, the low LI bees showed a preference to visiting familiar feeders, which contrasts with their behavior when in a uniform low LI group. We show that the shift in feeder preference of low LI bees is driven by foragers of the high LI phenotype dancing more intensely and attracting more followers. Our results reveal that cognitive abilities of individuals and their interactions drive emergent collective outcomes. Significance StatementVariation in individual cognition affects how animals perceive their environment and which information they share with others. Here we provide empirical evidence that how individual honey bees learn contributes to collective cognition of a colony. By creating colonies of distinct learning phenotypes, we evaluated how bees make foraging choices in the field. Colonies containing individuals that learn to ignore unimportant information preferred familiar food locations, however colonies of individuals that are unable to ignore familiar information visit novel and familiar feeders equally. A 50/50 mix of these phenotypes prefer familiar food locations, because individuals who learn the familiar location recruit nestmates by dancing more intensely. Our results reveal that variation in individual cognition scales non-linearly to shape collective outcomes.

animal behavior and cognition↗

DIVISION OF LABOR INCREASES WITH COLONY SIZE, REGARDLESS OF GROUP COMPOSITION, IN THE SOCIAL SPIDER STEGODYPHUS DUMICOLA

AO_SCPLOWBSTRACTC_SCPLOWDivision of labor (DOL) is a pattern of work organization where individual group members specialize on different tasks. DOL is argued to have been instrumental for the success of eusocial insects, where it scales positively with group size both within and across species. Here we evaluate whether DOL scales positively with group size in a society of cooperative breeders (social spiders) and whether this pattern is impacted by the behavioral composition of the group. To do this we engineered experimental colonies of contrasting group sizes and behavioral compositions and tracked individuals participation in two colony maintenance tasks: prey capture and web construction. As with some eusocial insects, we found that larger groups exhibited DOL metrics up to 10-times greater than smaller groups, conveying that individuals specialize on particular tasks more in larger colonies. This scalar relationship did not differ by a groups behavioral composition, though groups composed of only bold spiders exhibited reduced DOL relative to all-shy or mixed groups. We also found that per capita participation in prey capture, but not web construction, decreased as a function of group size. This suggests that individuals in larger groups may save energy by reducing their involvement in some tasks. Together, our results convey that similar scalar relationships between DOL and group size can emerge both inside and outside the eusocial insects. Thus, theory developed for understanding DOL in eusocial societies may inform our understanding of group function in a larger swath of animal social diversity than is broadly appreciated.\n\nSO_SCPLOWIGNIFICANCEC_SCPLOW SO_SCPLOWTATEMENTC_SCPLOWDivision of labor (DOL) has been a major area of research in the eusocial insects for decades, and is argues to underlie their ecological success. Only recently have other social arthropods, such as social spiders, been considered for studies concerning DOL. Given their smaller colony sizes, and absence of morphological castes, DOL was not thought to be an important facet of spider societies. However, we found that spider societies do indeed exhibit high degrees of DOL that is positively correlated to colony size, as seen in many eusocial insects. These findings suggest that the scalar relationship between group size and social organization seen in social insects is likely generalizable to a larger diversity of social taxa, and that cooperative breeders can show levels of division of labor equaling or exceeding those of eusocial systems evaluated to date.

animal behavior and cognition↗

Multilevel selection in groups of groups

Natural selection occurs at many levels. We evaluated selection acting on collectives at a level of multilevel selection analysis not yet quantified: within and between clusters of groups. We did so by monitoring the performance of natural colonies of social spiders with contrasting foraging aggressiveness in clusters of various sizes. Within-clusters, growth rates were suppressed when colonies were surrounded by more rival groups, conveying that competition is greater. When colonies were surrounded by few rivals, the more aggressive colonies in a cluster were more successful. In contrast, relatively non-aggressive colonies performed better when surrounded by many rivals. Patterns of selection between-clusters depended on the performance metric considered, but cluster-wide aggressiveness was always favored in small clusters. Together, selection both within-and between natural clusters of colonies was detectable, but highly contingent on the number of competing colonies.

evolutionary biology↗

Predictors of colony extinction vary by habitat type in social spiders

Many animal societies are susceptible to mass mortality events and collapse. Elucidating how environmental pressures determine patterns of collapse is key for our understanding of social evolution. Using the social spider Stegodyphus dumicola we investigated the environmental drivers of colony extinction along two precipitation gradients across southern Africa, using the Namib and Kalahari deserts versus wetter savanna habitats to the north and east. We deployed experimental colonies (n = 242) along two 800km transects and returned to assess colony success in the field after two months. Specifically, we noted colony extinction events after the two-month duration and collected environmental data on the correlates of those extinction events (e.g., evidence of ant attacks, # prey captured). We found that colony extinction events at desert sites were more frequently associated with attacks by predatory ants as compared to savanna sites, while colony extinctions in wetter savannas sites were more tightly associated with fungal outbreaks. Our findings support the hypothesis that environments vary in the selection pressures that they impose on social organisms, which may explain why different social phenotypes are often favored in each habitat.

ecology↗

Resting networks and personality predict attack speed in social spiders

Groups of social predators capture large prey items collectively, and their social interaction patterns may impact how quickly they can respond to time-sensitive predation opportunities. We investigated whether various organizational levels of resting interactions (individual, sub-group, group), observed at different intervals leading up to a collective prey attack, impacted the predation speed of colonies of the social spider Stegodyphus dumicola. We found that in adult spiders overall group connectivity (average degree) increased group attack speed. However, this effect was detected only immediately before the predation event; connectivity two and four days before prey capture had little impact on the collective dynamics. Significantly, lower social proximity of the groups boldest individual to other group members (closeness centrality) immediately prior and two days before prey capture was associated with faster attack speeds. These results suggest that for adult spiders, the long-lasting effects of the boldest individual on the groups attack dynamics are mediated by its role in the social network, and not only by its boldness. This suggests that behavioural traits and social network relationships should be considered together when defining keystone individuals in some contexts. By contrast, for subadult spiders, while the group maximum boldness was negatively correlated with latency to attack, no significant resting network predictors of latency to attack were found. Thus, separate behavioural mechanisms might play distinctive roles in determining collective outcomes at different developmental stages, timescales, and levels of social organization.\n\nSignificance statementCertain animals in a group, such as leaders, may have a more important role than other group members in determining their collective behavior. Often these individuals are defined by their behavioral attributes, for example, being bolder than others. We show that in social spiders both the behavioral traits of the influential individual, and its interactions with other group members, shape its role in affecting how quickly the group collectively attacks prey.

animal behavior and cognition↗

Underlying mechanisms and ecological consequences of variation in exploratory behavior of the Argentine ant, Linepithema humile

Uncovering how and why animals explore their environment is fundamental for understanding population dynamics, the spread of invasive species, species interactions etc. In social animals, individuals within a group can vary in their exploratory behavior and the behavioral composition of the group can determine its collective success. Workers of the invasive Argentine ant (Linepithema humile) exhibit individual variation in exploratory behavior, which affects the colonys collective nest selection behavior. Here we examine the mechanisms underlying this behavioral variation in exploratory behavior and determine its implications for the ecology of this species. We first establish that individual variation in exploratory behavior is repeatable and consistent across situations. We then show a relationship between exploratory behavior and the expression of genes that have been previously linked with other behaviors in social insects. Specifically, we find a negative relationship between exploratory behavior and the expression of the FOR gene. Finally, we determine how colonies allocate exploratory individuals in natural conditions. We find that ants from inside the nest are the least exploratory individuals, while workers on newly formed foraging trails are the most exploratory individuals. Furthermore, workers in the spring, when new resources emerge, are more exploratory than workers in the winter, potentially allowing the colony to find and exploit new resources. These findings reveal the importance of individual variation in behavior for the ecology of social animals and provide mechanistic and functional explanations for how such behavioral variation can emerge.

animal behavior and cognition↗