Nutritional needs and mortality risk combine to shape foraging decisions in ants.

When foraging, internal needs for particular nutrients might affect food choice, and external constraints, such as predation risk, might impact trade-offs between foraging and risk avoidance. Examining both internal and external constraints simultaneously can provide important insights into how animals make decisions. We examined how internal nutritional needs and external cues of mortality risk jointly impact the foraging behavior of ants. Ant colonies require carbohydrates to support workers energetically and proteins to raise brood. Furthermore, colonies adjust their foraging activity in response to the environment, such as food availability and the presence of predators or heterospecifics. Here we examine the foraging decisions of groups of Argentine ants Linepithema humile, which differ in their nutritional needs in high-risk environments. We starved groups of ants for either proteins or carbohydrates and determined the foraging choices that ants made when cues of heterospecifics were present. We found that ants preferentially forage for carbohydrates in high-risk conditions. Furthermore, starvation for carbohydrates increased the ants' preference for carbohydrates, even when cues of heterospecifics were present at both carbohydrates and protein resources. Starvation for protein also resulted in preferential foraging for carbohydrates, but it increased visitation to a protein food source in high-risk environments compared to when ants were starved for carbohydrates or for both resources. Examining the effect of both nutrition and mortality risk on foraging simultaneously provides insights about state-dependent risk-taking behavior that may have important implications for predicting the invasion of species into novel habitats.

Colonies of ants allocate exploratory individuals to where they are ecologically needed.

Individual differences in behavior have large consequences for the way in which ecology impacts fitness. Individuals differ in how they explore their environment and how exploratory behavior benefits them. In group-living animals, behavioral heterogeneity can be beneficial because different individuals perform different tasks. For example, exploratory individuals may discover new food sources and recruit group members to exploit the food, while less exploratory individuals forgo the risks of exploration. Here we ask how individual variation in exploratory behavior affects the ability of Argentine ant Linepithema humile colonies to (1) locate novel food sources, (2) exploit known food resources, and (3) respond to disruptions while foraging. To address these questions, we conducted field experiments on L. humile foraging trails in which we manipulated food availability near and at the foraging trails and disrupted the foraging trails. We sampled individuals based on their response to the perturbations in the field and tested their exploratory behavior in the lab. We found that exploratory individuals benefit the colony by locating novel foods and increasing resource exploitation, but they do not play an important role in the recovery of a foraging trail after disruption. Thus, the benefits of behavioral heterogeneity to the group, specifically in exploratory behavior, differ across ecological contexts.

Foraging behaviour affects nest architecture in a cross-species comparison of ant nests.

Animals construct and inhabit nests that can exhibit dramatic intra- and interspecific variation due to differences in behaviour, the biotic and abiotic environment, and evolutionary history. In ants, variation in nest architecture reflects both differences in ecology and in the collective behaviour of the colonies that live in the nests. Each component of the nest (such as depth, and the number, size and connectivity of chambers) reflects selective pressures for different functions, or structural constraints that are imposed by the environment or evolutionary history. To determine potential drivers of nest structure variation in subterranean nests, we performed a meta-analysis of measures of published ant nests to compare different structural elements within and across species. We complemented this survey with 42 nest casts of two closely related species. We quantified nest features that can potentially impact ant foraging behaviour and examined whether phylogeny or foraging strategy are better explanatory variables for the variation we observed. We found that foraging strategy better explained nest features than evolutionary history. Our work reveals the importance of ecology in shaping nest structure and provides an important foundation for future investigations into the selective pressures that have shaped ant nest architecture. This article is part of the theme issue 'The evolutionary ecology of nests: a cross-taxon approach'.

Social situations differ in their contribution to population-level social structure in griffon vultures.

Social relationships among animals emerge from interactions in multiple ecological and social situations. However, we seldom ask how each situation contributes to the global structure of a population, and whether different situations contribute different information about social relationships and the position of individuals within the social fabric. Griffon vultures (Gyps fulvus) interact socially in multiple situations, including communal roosting, joint flights, and co-feeding. These social interactions can influence population-level outcomes, such as disease transmission and information sharing that determine survival and response to changes. We examined the unique contribution of each social and ecological situation to the social structure of the population and individuals' positions within the overall social network using high-resolution GPS tracking. We found that the number of individuals each vulture interacted with (degree) was best predicted by diurnal interactions-both during flights and on the ground (such as when feeding). However, the strength of social bonds, that is, the number of interactions an individual had (strength), was best predicted by interactions on the ground-both during the day (e.g., while feeding) and at night (e.g., while roosting) but not by interactions while flying. Thus, social situations differ in their impact on the relationships that individuals form. By incorporating the ecological situations in which social interactions occur we gain a more complete view of how social relationships are formed and which situations are important for different types of interactions.

Behavioural ecology at the spatial-social interface.

Spatial and social behaviour are fundamental aspects of an animal's biology, and their social and spatial environments are indelibly linked through mutual causes and shared consequences. We define the 'spatial-social interface' as intersection of social and spatial aspects of individuals' phenotypes and environments. Behavioural variation at the spatial-social interface has implications for ecological and evolutionary processes including pathogen transmission, population dynamics, and the evolution of social systems. We link spatial and social processes through a foundation of shared theory, vocabulary, and methods. We provide examples and future directions for the integration of spatial and social behaviour and environments. We introduce key concepts and approaches that either implicitly or explicitly integrate social and spatial processes, for example, graph theory, density-dependent habitat selection, and niche specialization. Finally, we discuss how movement ecology helps link the spatial-social interface. Our review integrates social and spatial behavioural ecology and identifies testable hypotheses at the spatial-social interface.

Social consequences of rapid environmental change.

While direct influences of the environment on population growth and resilience are well studied, indirect routes linking environmental changes to population consequences are less explored. We suggest that social behavior is key for understanding how anthropogenic environmental changes affect the resilience of animal populations. Social structures of animal groups are evolved and emergent phenotypes that often have demographic consequences for group members. Importantly, environmental drivers may directly influence the consequences of social structure or indirectly influence them through modifications to social interactions, group composition, or group size. We have developed a framework to study these demographic consequences. Estimating the strength of direct and indirect pathways will give us tools to understand, and potentially manage, the effect of human-induced rapid environmental changes.

Predicting the impacts of chemical pollutants on animal groups.

Chemical pollution is among the fastest-growing agents of global change. Synthetic chemicals with diverse modes-of-action are being detected in the tissues of wildlife and pervade entire food webs. Although such pollutants can elicit a range of sublethal effects on individual organisms, research on how chemical pollutants affect animal groups is severely lacking. Here we synthesise research from two related, but largely segregated fields - ecotoxicology and behavioural ecology - to examine pathways by which chemical contaminants could disrupt processes that govern the emergence, self-organisation, and collective function of animal groups. Our review provides a roadmap for prioritising the study of chemical pollutants within the context of sociality and highlights important methodological advancements for future research.

Harvester ant nest architecture is more strongly affected by intrinsic than extrinsic factors.

Behavior is shaped by genes, environment, and evolutionary history in different ways. Nest architecture is an extended phenotype that results from the interaction between the behavior of animals and their environment. Nests built by ants are extended phenotypes that differ in structure among species and among colonies within a species, but the source of these differences remains an open question. To investigate the impact of colony identity (genetics), evolutionary history (species), and the environment on nest architecture, we compared how two species of harvester ants, Pogonomyrmex californicus and Veromessor andrei, construct their nests under different environmental conditions. For each species, we allowed workers from four colonies to excavate nests in environments that differed in temperature and humidity for seven days. We then created casts of each nest to compare nest structures among colonies, between species, and across environmental conditions. We found differences in nest structure among colonies of the same species and between species. Interestingly, however, environmental conditions did not have a strong influence on nest structure in either species. Our results suggest that extended phenotypes are shaped more strongly by internal factors, such as genes and evolutionary history, and are less plastic in response to the abiotic environment, like many physical and physiological phenotypes.

The effect of resource availability on interspecific competition between a native and an invasive ant.

Interspecific competition influences the composition of ecological communities. Species may differ in their needs for different resources, therefore resource availability may determine the outcome of interspecific interactions. Species often compete over food, shelter or both. When more than one resource is limited, different species may prioritize different resources. To determine the impact of resource availability on the competitive relationship between an invasive and a native species, we examined interactions between groups of the invasive Argentine ant (Linepithema humile) and the native odorous ant (Tapinoma sessile) over (1) food, (2) shelter or (3) both simultaneously. We further examined the mechanisms underlying the competitive relationship, asking whether aggressive interactions, exploratory behaviour or the order of arrival at a resource explained resource use. Shelter was preferred by both species when no competitors were present. In a competitive setting, L. humile groups controlled shelter through aggressive displacement but lost control over food due to investment of workers in the control of shelter. Thus, there are tradeoffs when competing over multiple resources and aggressive interactions allow invasive species to displace native species from a preferred resource. This article is part of the theme issue 'Intergroup conflict across taxa'.

Queen succession in the Indian paper wasp Ropalidia marginata: On the trail of the potential queen.

Ropalidia marginata is a common primitively eusocial wasp in peninsular India. Their colonies contain a single egg-laying queen and several non-egg-laying workers. Queens and workers are morphologically indistinguishable, and individuals can change from one role to the other. Unlike most primitively eusocial species, queens of R. marginata are docile, non-aggressive and non-interactive. Nevertheless, the queens maintain a complete reproductive monopoly mediated by non-volatile pheromones. Upon the death or removal of the queen, one worker becomes temporarily hyper-aggressive and becomes the next queen within about a week; we refer to her as the 'potential queen'. Because only one individual becomes hyper-aggressive and reveals herself as the potential queen, and the other wasps never challenge her, we have been much interested in identifying the potential queen in the presence of the queen. However, we have failed to do so until recently. Here, we recount the four decades of search for the potential queen, ending with the recent resolution that emerged from applying the novel technique of multilayer network analysis. Identifying the potential queen in the presence of the previous queen is now possible by integrating behavioural information from multiple social situations to form a holistic view of the social structure of the wasps.

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) shortcuts-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.

Understanding Drivers of Variation and Predicting Variability Across Levels of Biological Organization.

Differences within a biological system are ubiquitous, creating variation in nature. Variation underlies all evolutionary processes and allows persistence and resilience in changing environments; thus, uncovering the drivers of variation is critical. The growing recognition that variation is central to biology presents a timely opportunity for determining unifying principles that drive variation across biological levels of organization. Currently, most studies that consider variation are focused at a single biological level and not integrated into a broader perspective. Here we explain what variation is and how it can be measured. We then discuss the importance of variation in natural systems, and briefly describe the biological research that has focused on variation. We outline some of the barriers and solutions to studying variation and its drivers in biological systems. Finally, we detail the challenges and opportunities that may arise when studying the drivers of variation due to the multi-level nature of biological systems. Examining the drivers of variation will lead to a reintegration of biology. It will further forge interdisciplinary collaborations and open opportunities for training diverse quantitative biologists. We anticipate that these insights will inspire new questions and new analytic tools to study the fundamental questions of what drives variation in biological systems and how variation has shaped life.

A guide to choosing and implementing reference models for social network analysis.

Analysing social networks is challenging. Key features of relational data require the use of non-standard statistical methods such as developing system-specific null, or reference, models that randomize one or more components of the observed data. Here we review a variety of randomization procedures that generate reference models for social network analysis. Reference models provide an expectation for hypothesis testing when analysing network data. We outline the key stages in producing an effective reference model and detail four approaches for generating reference distributions: permutation, resampling, sampling from a distribution, and generative models. We highlight when each type of approach would be appropriate and note potential pitfalls for researchers to avoid. Throughout, we illustrate our points with examples from a simulated social system. Our aim is to provide social network researchers with a deeper understanding of analytical approaches to enhance their confidence when tailoring reference models to specific research questions.

Trade-offs between fighting and breeding: a social network analysis of bison male interactions.

In most polygynous species, males compete for access to females using agonistic interactions to establish dominance hierarchies. Typically, larger and stronger males become more dominant and thus gain higher mating and reproductive success over subordinate males. However, there is an inherent trade-off between time and energy invested in dominance interactions versus courtship and mating activities. Individuals may overcome this trade-off by selectively engaging in more effective mating tactics. North American bison (Bison bison) are a species of conservation concern that exhibit female-defense polygyny with two predominant mating tactics: (1) tending individual females; or (2) challenging tending males as a satellite and then mating opportunistically. Here, we use social network analysis to examine the relationship between position in the agonistic interaction network of bison males and their mating, reproductive success, and reproductive tactics and effort. To assess the potential for social network analysis to generate new insights, we compare male (node) centrality in the interaction network with traditional David's score and Elo-rating dominance rankings. Local and global node centrality and dominance rankings were positively associated with prime-aged, heavy males with the most mating success and offspring sired. These males invested more effort in the "tending" tactic versus the "satellite" tactic, and they tended more females for longer periods during peak rut, when most females were receptive. By engaging in the most effective mating tactic, dominant males may mitigate the trade-off between allocating time and energy to agonistic interactions that establish dominance, versus courtship and mating. While less dominant males participated more in the alternative mating tactic, network analysis demonstrated that they were still important to the interaction network on both a local and global scale.

Using multilayer network analysis to explore the temporal dynamics of collective behavior.

Social organisms often show collective behaviors such as group foraging or movement. Collective behaviors can emerge from interactions between group members and may depend on the behavior of key individuals. When social interactions change over time, collective behaviors may change because these behaviors emerge from interactions among individuals. Despite the importance of, and growing interest in, the temporal dynamics of social interactions, it is not clear how to quantify changes in interactions over time or measure their stability. Furthermore, the temporal scale at which we should observe changes in social networks to detect biologically meaningful changes is not always apparent. Here we use multilayer network analysis to quantify temporal dynamics of social networks of the social spider Stegodyphus dumicola and determine how these dynamics relate to individual and group behaviors. We found that social interactions changed over time at a constant rate. Variation in both network structure and the identity of a keystone individual was not related to the mean or variance of the collective prey attack speed. Individuals that maintained a large and stable number of connections, despite changes in network structure, were the boldest individuals in the group. Therefore, social interactions and boldness are linked across time, but group collective behavior is not influenced by the stability of the social network. Our work demonstrates that dynamic social networks can be modeled in a multilayer framework. This approach may reveal biologically important temporal changes to social structure in other systems.

Observing the unwatchable: Integrating automated sensing, naturalistic observations and animal social network analysis in the age of big data.

In the 4.5 decades since Altmann (1974) published her seminal paper on the methods for the observational study of behaviour, automated detection and analysis of social interaction networks have fundamentally transformed the ways that ecologists study social behaviour. Methodological developments for collecting data remotely on social behaviour involve indirect inference of associations, direct recordings of interactions and machine vision. These recent technological advances are improving the scale and resolution with which we can dissect interactions among animals. They are also revealing new intricacies of animal social interactions at spatial and temporal resolutions as well as in ecological contexts that have been hidden from humans, making the unwatchable seeable. We first outline how these technological applications are permitting researchers to collect exquisitely detailed information with little observer bias. We further recognize new emerging challenges from these new reality-mining approaches. While technological advances in automating data collection and its analysis are moving at an unprecedented rate, we urge ecologists to thoughtfully combine these new tools with classic behavioural and ecological monitoring methods to place our understanding of animal social networks within fundamental biological contexts.

Individual learning phenotypes drive collective behavior.

Individual differences in learning can influence how animals respond to and communicate about their environment, which may nonlinearly shape how a social group accomplishes a collective task. There are few empirical examples of how differences in collective dynamics emerge from variation among individuals in cognition. Here, we use a naturally variable and heritable learning behavior called latent inhibition (LI) to show that interactions among individuals that differ in this cognitive ability drive collective foraging behavior in honey bee colonies. We artificially selected two distinct phenotypes: high-LI bees that ignore previously familiar stimuli in favor of novel ones and low-LI bees that learn familiar and novel stimuli equally well. We then provided colonies differentially composed of different ratios of these phenotypes with a choice between familiar and novel feeders. Colonies of predominantly high-LI individuals preferred to visit familiar food locations, while low-LI colonies visited novel and familiar food locations equally. Interestingly, in colonies of mixed learning phenotypes, the low-LI individuals 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 social interactions, which we argue relate to differences in attention, drive emergent collective outcomes.

Physical and social cues shape nest-site preference and prey capture behavior in social spiders.

Animals often face conflicting demands when making movement decisions. To examine the decision process of social animals, we evaluated nest-site preferences of the social spider Stegodyphus dumicola. Colonies engage in collective web building, constructing 3D nests and 2D capture webs on trees and fences. We examined how individuals and groups decide where to construct a nest based on habitat structure and conspecific presence. Individuals had a strong preference for 3D substrates and conspecific presence. Groups were then provided with conflicting options of 3D substrates versus 2D substrates with a conspecific. Groups preferred the 3D structures without presettled conspecifics over a 2D substrate with conspecifics. When a group fragmented and individuals settled on both substrates, the minority group eventually joined the majority. Before rejoining, the collective prey capture behavior of divided groups improved with the size of the majority fragment. The costs of slow responses to prey for split groups and weak conspecific attraction may explain why dispersal is rare in these spiders.

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 important for understanding how such societies function and evolve. 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 ~ 800-km transects and returned to assess colony success in the field after 2 months. Specifically, we noted colony extinction events after the 2-month duration and collected environmental data on the correlates of those extinction events (e.g., evidence of ant attacks, no. of prey captured). We found that colony extinction events at desert sites were more frequently associated with attacks by predatory ants as compared with 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.