Stephan T. Leu

Environment modulates population social structure: Experimental evidence from replicated social networks of wild lizards

Social structure is a fundamental component of a population that drives ecological and evolutionary processes ranging from parasite transmission to sexual selection. Nevertheless, we have much to learn about factors that explain variation in social structure. We used advances in biologging and social network analysis to experimentally test how the local habitat, and specifically habitat complexity, modulates social structure at different levels in wild populations. Sleepy lizards, Tiliqua rugosa, establish nonrandom social networks that are characterized by avoidance of some neighbours and frequent interactions with one opposite-sex individual. Using synchronous GPS locations of all adult lizards, we constructed social networks based on spatial proximity of individuals. We increased habitat structural complexity in two study populations by adding 100 short fences across the landscape. We then compared the resulting movement behaviour and social structure between these populations and two unmanipulated populations. Social connectivity (network density) and social stability, measured at weekly intervals, were greater in populations with increased habitat structural complexity. The level of agonistic interaction (quantified as scale damage) was also higher, indicating a fitness cost of greater social connectivity. However, some network parameters were unaffected by increased complexity, including disassortative mixing by sex, and at the individual level, social differentiation among associates (coefficient of variation of edge weights) and maximal interaction frequencies (maximal edge weight). This suggests divergent effects of changed ecological conditions on individual association behaviour compared to the resulting social structure of the population. Our results contrast with those from studies of more gregarious species, in which higher structural complexity in the environment relaxed the social connectivity. This shows that the response to altered ecological conditions can differ fundamentally between species or between populations, and we suggest that it depends on their tendency for gregarious behaviour.

Socially interacting or indifferent neighbours? Randomization of movement paths to tease apart social preference and spatial constraints

Summary Understanding how animals interact with their physical and social environment is a major question in ecology, but separating between these factors is often challenging. Observed interaction rates may reflect social behaviour – preferences or avoidance of conspecifics or certain phenotypes. Yet, environmental spatiotemporal heterogeneity also affects individual space use and interaction rates. For instance, clumped and ephemeral resources may force individuals to aggregate independently of sociality. Proximity-based social networks (PBSNs) are becoming increasingly popular for studying social structures thanks to the parallel improvement of biotracking technologies and network randomization methods. While current methods focus on swapping individual identities among network nodes or in the data streams that underlies the network (e.g. individuals movement paths), we still need better tools to distinguish between the contribution of sociality and other factors towards those interactions. We propose a novel method that randomizes path segments among different time stamps within each individual separately (Part I). Temporal randomization of whole path segments (e.g. full days) retains their original spatial structure while decoupling synchronization among individuals. This allows researchers to compare observed dyadic association rates with those expected by chance given explicit space use of the individuals in each dyad. Further, since environmental changes are commonly much slower than the duration of social interactions, we can differentiate between these two factors (Part II). First, an individuals path is divided into successive time windows (e.g. weeks), and days are randomized within each time window. Then, by exploring how the deviations between randomized and observed networks change as a function of time window length, we can refine our null model to account also for temporal changes in the activity areas. We used biased-correlated random walk models to simulate populations of socially indifferent or sociable agents for testing our method for both false-positive and negative errors. Applying the method to a data set of GPS-tracked sleepy lizards (Tiliqua rugosa) demonstrated its ability to reveal the social organization in free-ranging animals while accounting for confounding factors of environmental spatiotemporal heterogeneity. We demonstrate that this method is robust to sampling bias and argue that it is applicable for a wide range of systems and tracking techniques, and can be extended to test for preferential phenotypic assortment within PBSNs.

When the going gets tough: behavioural type-dependent space use in the sleepy lizard changes as the season dries.

Understanding space use remains a major challenge for animal ecology, with implications for species interactions, disease spread, and conservation. Behavioural type (BT) may shape the space use of individuals within animal populations. Bolder or more aggressive individuals tend to be more exploratory and disperse further. Yet, to date we have limited knowledge on how space use other than dispersal depends on BT. To address this question we studied BT-dependent space-use patterns of sleepy lizards (Tiliqua rugosa) in southern Australia. We combined high-resolution global positioning system (GPS) tracking of 72 free-ranging lizards with repeated behavioural assays, and with a survey of the spatial distributions of their food and refuge resources. Bayesian generalized linear mixed models (GLMM) showed that lizards responded to the spatial distribution of resources at the neighbourhood scale and to the intensity of space use by other conspecifics (showing apparent conspecific avoidance). BT (especially aggressiveness) affected space use by lizards and their response to ecological and social factors, in a seasonally dependent manner. Many of these effects and interactions were stronger later in the season when food became scarce and environmental conditions got tougher. For example, refuge and food availability became more important later in the season and unaggressive lizards were more responsive to these predictors. These findings highlight a commonly overlooked source of heterogeneity in animal space use and improve our mechanistic understanding of processes leading to behaviourally driven disease dynamics and social structure.

Testing the robustness of transmission network models to predict ectoparasite loads. One lizard, two ticks and four years

Graphical abstract

Lizard movement tracks: variation in path re-use behaviour is consistent with a scent-marking function

Individual movement influences the spatial and social structuring of a population. Animals regularly use the same paths to move efficiently to familiar places, or to patrol and mark home ranges. We found that Australian sleepy lizards (Tiliqua rugosa), a monogamous species with stable pair-bonds, repeatedly used the same paths within their home ranges and investigated whether path re-use functions as a scent-marking behaviour, or whether it is influenced by site familiarity. Lizards can leave scent trails on the substrate when moving through the environment and have a well-developed vomeronasal system to detect and respond to those scents. Path re-use would allow sleepy lizards to concentrate scent marks along these well-used trails, advertising their presence. Hypotheses of mate attraction and mating competition predict that sleepy lizard males, which experience greater intra-sexual competition, mark more strongly. Consistent with those hypotheses, males re-used their paths more than females, and lizards that showed pairing behaviour with individuals of the opposite sex re-used paths more than unpaired lizards, particularly among females. Hinterland marking is most economic when home ranges are large and mobility is low, as is the case in the sleepy lizard. Consistent with this strategy, re-used paths were predominantly located in the inner 50% home range areas. Together, our detailed movement analyses suggest that path re-use is a scent marking behaviour in the sleepy lizard. We also investigated but found less support for alternative explanations of path re-use behaviour, such as site familiarity and spatial knowledge. Lizards established the same number of paths, and used them as often, whether they had occupied their home ranges for one or for more years. We discuss our findings in relation to maintenance of the monogamous mating system of this species, and the spatial and social structuring of the population.

Making Friends: Social Attraction in Larval Green and Golden Bell Frogs, Litoria aurea

Socio-ecological models combine environmental and social factors to explain the formation of animal groups. In anurans, tadpole aggregations have been reported in numerous species, but the factors driving this behaviour remain unclear. We conducted controlled choice experiments in the lab to determine whether green and golden bell frog (Litoria aurea) tadpoles are directly attracted to conspecifics (social factors) in the absence of environmental cues. Using repeated measures, we found that individual tadpoles strongly preferred associating with conspecifics compared to being alone. Furthermore, this preference was body size dependent, and associating tadpoles were significantly smaller than non-associating tadpoles. We suggest that small tadpoles are more vulnerable to predation and therefore more likely to form aggregations as an anti-predator behaviour. We demonstrate that tadpoles present an ideal model system for investigating how social and ecological factors influence group formation in vertebrates.

Artificial Water Point for Livestock Influences Spatial Ecology of a Native Lizard Species.

Pastoralism is a major agricultural activity in drier environments, and can directly and indirectly impact native species in those areas. We investigated how the supply of an artificial watering point to support grazing livestock affected movement and activity patterns of the Australian sleepy lizard (Tiliqua rugosa) during a drought year. We observed 23 adult lizards; six had access to a dam, whereas 17 lizards did not. Lizards with access to the dam had larger home ranges, were substantially active on more days (days with >100 steps), and moved more steps per day compared to lizards that did not have access to the dam, both during the early and late period of our observation. Furthermore, while the two groups of lizards had similar body condition early in the season, they differed later in the season. Lizards with dam access retained, whereas lizards without access lost body condition. Local heterogeneity in access to an artificial water resource resulted in spatially dependent behavioural variation among sleepy lizard individuals. This suggests that sleepy lizards have flexible responses to changing climatic conditions, depending on the availability of water. Furthermore, while reducing activity appears a suitable short term strategy, if harsh conditions persist, then access to dams could be of substantial benefit and could support sustained lizard activity and movement and allow maintenance of body condition. Hence, artificial watering points, such as the dams constructed by pastoralists, may provide local higher quality refugia for sleepy lizards and other species during drought conditions.

Advances from the nexus of animal behaviour and pathogen transmission: new directions and opportunities using contact networks

Contact network models have enabled significant advances in understanding the influence of behaviour on parasite and pathogen transmission. They are an important tool that links variation in individual behaviour, to epidemiological consequences at the population level. Here, in our introduction to this special issue, we highlight the importance of applying network approaches to disease ecological and epidemiological questions, and how this has provided a much deeper understanding of these research areas. Recent advances in tracking host behaviour (bio-logging: e.g., GPS tracking, barcoding) and tracking pathogens (high-resolution sequencing), as well as methodological advances (multi-layer networks, computational techniques) started producing exciting new insights into disease transmission through contact networks. We discuss some of the exciting directions that the field is taking, some of the challenges, and importantly the opportunities that lie ahead. For instance, we suggest to integrate multiple transmission pathways, multiple pathogens, and in some systems, multiple host species, into the next generation of network models. Corresponding opportunities exist in utilising molecular techniques, such as high-resolution sequencing, to establish causality in network connectivity and disease outcomes. Such novel developments and the continued integration of network tools offers a more complete understanding of pathogen transmission processes, their underlying mechanisms and their evolutionary consequences.

Lizards space use data for the Bayesian GLMM models

This file includes all the data used for modeling the space use by the lizards. It contains separates sheets for the Early and Late season and columns names are explained in a metadata sheet.