Heat stress from current and predicted increases in temperature impairs lambing rates and birth weights in the Australian sheep flock.

Livestock heat stress threatens production, particularly in semi-arid, arid and tropical regions. Using established temperature thresholds for sheep, we modelled +1 °C and +3 °C temperature increases over the historical baseline, estimating that 2.1 million potential lambs are lost annually due to heat stress alone, increasing to 2.5 and 3.3 million, respectively, as temperatures rise. Heat stress poses risks at key periods of the reproductive cycle, with consequences across the Australian sheep flock.

Heat stress conditions affect the social network structure of free-ranging sheep.

Extreme weather conditions, like heatwave events, are becoming more frequent with climate change. Animals often modify their behaviour to cope with environmental changes and extremes. During heat stress conditions, individuals change their spatial behaviour and increase the use of shaded areas to assist with thermoregulation. Here, we suggest that for social species, these behavioural changes and ambient conditions have the potential to influence an individual's position in its social network, and the social network structure as a whole. We investigated whether heat stress conditions (quantified through the temperature humidity index) and the resulting use of shaded areas, influence the social network structure and an individual's connectivity in it. We studied this in free-ranging sheep in the arid zone of Australia, GPS-tracking all 48 individuals in a flock. When heat stress conditions worsened, individuals spent more time in the shade and the network was more connected (higher density) and less structured (lower modularity). Furthermore, we then identified the behavioural change that drove the altered network structure and showed that an individual's shade use behaviour affected its social connectivity. Interestingly, individuals with intermediate shade use were most strongly connected (degree, strength, betweenness), indicating their importance for the connectivity of the social network during heat stress conditions. Heat stress conditions, which are predicted to increase in severity and frequency due to climate change, influence resource use within the ecological environment. Importantly, our study shows that these heat stress conditions also affect the animal's social environment through the changed social network structure. Ultimately, this could have further flow on effects for social foraging and individual health since social structure drives information and disease transmission.

The presence of informed conspecifics improves individual foraging efficiency in naïve sheep.

Knowledge about the environment is fundamentally important to move, find resources and forage efficiently. This information can either be acquired through individual exploration (personal information) or from other group members (social information). We experimentally assessed the use of social information and its influence on foraging efficiency in sheep, Ovis aries. Naïve individuals paired with an informed partner that knew the food patch location, found the patch significantly faster compared to naïve individuals paired with another naïve individual. Similarly, they spent a significantly lower proportion of time exploring areas away from the food patch. We further found that the outcome of using social information in one directly previous trial (success = access to feed vs failure = no access to feed) had no impact and sheep continued to use social information in the subsequent foraging trial and foraged similarly efficient. Our results suggest, naïve sheep that are unfamiliar with resource locations, forage more efficiently when informed individuals are present compared to when all individuals are naïve. If informed individuals play a similar role in larger groups, new management practices that integrate informed sheep could be developed to improve foraging efficiency when sheep are moved to new paddocks or in paddocks with heterogenous and dynamic resource distribution.

Correction to: 'Fission-fusion dynamics in sheep: the influence of resource distribution and temporal activity patterns' (2023) by Della Libera et al.

[This corrects the article DOI: 10.1098/10.1098/rsos.230402.][This corrects the article DOI: 10.1098/rspb.2021.1115.].

Fission-fusion dynamics in sheep: the influence of resource distribution and temporal activity patterns.

Fission-fusion events, i.e. changes to the size and composition of animal social groups, are a mechanism to adjust the social environment in response to short-term changes in the cost-benefit ratio of group living. Furthermore, the time and location of fission-fusion events provide insight into the underlying drivers of these dynamics. Here, we describe a method for identifying group membership over time and for extracting fission-fusion events from animal tracking data. We applied this method to high-resolution GPS data of free-ranging sheep (Ovis aries). Group size was highest during times when sheep typically rest (midday and at night), and when anti-predator benefits of grouping are high while costs of competition are low. Consistent with this, fission and fusion frequencies were highest during early morning and late evening, suggesting that social restructuring occurs during periods of high activity. However, fission and fusion events were not more frequent near food patches and water resources when adjusted for overall space use. This suggests a limited role of resource competition. Our results elucidate the dynamics of grouping in response to social and ecological drivers, and we provide a tool for investigating these dynamics in other species.

Personality, spatiotemporal ecological variation and resident/explorer movement syndromes in the sleepy lizard.

Individual variation in movement is profoundly important for fitness and offers key insights into the spatial and temporal dynamics of populations and communities. Nonetheless, individual variation in fine-scale movement behaviours is rarely examined even though animal tracking devices offer the long-term, high-resolution, repeatable data in natural conditions that are ideal for studying this variation. Furthermore, of the few studies that consider individual variation in movement, even fewer also consider the internal traits and environmental factors that drive movement behaviour which are necessary for contextualising individual differences in movement patterns. In this study, we GPS tracked a free-ranging population of sleepy lizards Tiliqua rugosa, each Austral spring over 5 years to examine consistent among-individual variation in movement patterns, as well as how these differences were mediated by key internal and ecological factors. We found that individuals consistently differed in a suite of weekly movement traits, and that these traits strongly covaried among-individuals, forming movement syndromes. Lizards fell on a primary movement continuum, from 'residents' that spent extended periods of time residing within smaller core areas of their home range, to 'explorers' that moved greater distances and explored vaster areas of the environment. Importantly, we also found that these consistent differences in lizard movement were related to two ecologically important animal personality traits (boldness and aggression), their sex, key features of the environment (including food availability, and a key water resource), habitat type and seasonal variation (cool/moist vs. hot/drier) in environmental conditions. Broadly, these movement specialisations likely reflect variation in life-history tactics including foraging and mating tactics that ultimately underlie key differences in space use. Such information can be used to connect phenotypic population structure to key ecological and evolutionary processes, for example social networks and disease-transmission pathways, further highlighting the value of examining individual variation in movement behaviour.

Revealing mechanisms of infectious disease spread through empirical contact networks.

The spread of pathogens fundamentally depends on the underlying contacts between individuals. Modeling the dynamics of infectious disease spread through contact networks, however, can be challenging due to limited knowledge of how an infectious disease spreads and its transmission rate. We developed a novel statistical tool, INoDS (Identifying contact Networks of infectious Disease Spread) that estimates the transmission rate of an infectious disease outbreak, establishes epidemiological relevance of a contact network in explaining the observed pattern of infectious disease spread and enables model comparison between different contact network hypotheses. We show that our tool is robust to incomplete data and can be easily applied to datasets where infection timings of individuals are unknown. We tested the reliability of INoDS using simulation experiments of disease spread on a synthetic contact network and find that it is robust to incomplete data and is reliable under different settings of network dynamics and disease contagiousness compared with previous approaches. We demonstrate the applicability of our method in two host-pathogen systems: Crithidia bombi in bumblebee colonies and Salmonella in wild Australian sleepy lizard populations. INoDS thus provides a novel and reliable statistical tool for identifying transmission pathways of infectious disease spread. In addition, application of INoDS extends to understanding the spread of novel or emerging infectious disease, an alternative approach to laboratory transmission experiments, and overcoming common data-collection constraints.

What Are Sheep Doing? Tri-Axial Accelerometer Sensor Data Identify the Diel Activity Pattern of Ewe Lambs on Pasture.

Monitoring activity patterns of animals offers the opportunity to assess individual health and welfare in support of precision livestock farming. The purpose of this study was to use a triaxial accelerometer sensor to determine the diel activity of sheep on pasture. Six Perendale ewe lambs, each fitted with a neck collar mounting a triaxial accelerometer, were filmed during targeted periods of sheep activities: grazing, lying, walking, and standing. The corresponding acceleration data were fitted using a Random Forest algorithm to classify activity (=classifier). This classifier was then applied to accelerometer data from an additional 10 ewe lambs to determine their activity budgets. Each of these was fitted with a neck collar mounting an accelerometer as well as two additional accelerometers placed on a head halter and a body harness over the shoulders of the animal. These were monitored continuously for three days. A classification accuracy of 89.6% was achieved for the grazing, walking and resting activities (i.e., a new class combining lying and standing activity). Triaxial accelerometer data showed that sheep spent 64% (95% CI 55% to 74%) of daylight time grazing, with grazing at night reduced to 14% (95% CI 8% to 20%). Similar activity budgets were achieved from the halter mounted sensors, but not those on a body harness. These results are consistent with previous studies directly observing daily activity of pasture-based sheep and can be applied in a variety of contexts to investigate animal health and welfare metrics e.g., to better understand the impact that young sheep can suffer when carrying even modest burdens of parasitic nematodes.

Review of the impact of heat stress on reproductive performance of sheep.

Heat stress significantly impairs reproduction of sheep, and under current climatic conditions is a significant risk to the efficiency of the meat and wool production, with the impact increasing as global temperatures rise. Evidence from field studies and studies conducted using environmental chambers demonstrate the effects of hot temperatures (≥ 32 °C) on components of ewe fertility (oestrus, fertilisation, embryo survival and lambing) are most destructive when experienced from 5 d before until 5 d after oestrus. Temperature controlled studies also demonstrate that ram fertility, as measured by rates of fertilisation and embryo survival, is reduced when mating occurs during the period 14 to 50 d post-heating. However, the contribution of the ram to heat induced reductions in flock fertility is difficult to determine accurately. Based primarily on temperature controlled studies, it is clear that sustained exposure to high temperatures (≥ 32 °C) during pregnancy reduces lamb birthweight and will, therefore, decrease lamb survival under field conditions. It is concluded that both ewe and ram reproduction is affected by relatively modest levels of heat stress (≥ 32 °C) and this is a concern given that a significant proportion of the global sheep population experiences heat stress of this magnitude around mating and during pregnancy. Despite this, strategies to limit the impacts of the climate on the homeothermy, behaviour, resource use and reproduction of extensively grazed sheep are limited, and there is an urgency to improve knowledge and to develop husbandry practices to limit these impacts.

Gastrointestinal nematode infection affects overall activity in young sheep monitored with tri-axial accelerometers.

Animals suffering from parasitism typically display altered grazing behaviour and a voluntary reduction in feed intake. These changes are potentially important as indicators of disease. Recent advances in sensor technologies provide the opportunity to objectively measure animal activity while on pasture. Tri-axial accelerometers measure body movement in terms of acceleration, which can then be used to estimate physical activity over time. This study investigated if tri-axial measures of overall activity can be used to assess the impact of gastrointestinal nematode (GIN) infection in young sheep. To address this, the overall activity, faecal nematode egg count (FEC) and body weight of two treatment groups of Romney X Suffolk ram lambs were compared. Animals were monitored for four days using tri-axial accelerometer sensors mounted on a ram mating harness after 42-days grazing on contaminated pasture. On Day 0, all lambs were given anthelmintics. Subsequently, a Suppressive Treatment Group (n = 12) was treated with anthelmintics every two weeks. An Untreated Group (n = 12) did not receive further anthelmintics. Overall activity levels were monitored from Day 42 - 46. Activity level was calculated as vectorial dynamic body acceleration (VeDBA). Anthelmintic treatment had a significant effect on FEC but there was no evidence found for a treatment effect on body weight growth over the 42-day period. An effect of treatment and lamb starting weight on overall activity was found (beta = -0.74, 95 % CI -1.17 to -0.30, p =  0.002), identifying a negative impact of parasitism on activity in heavier animals. These results highlight the usefulness of this approach in assessing the effect of GIN parasitism on sheep monitored remotely. If a threshold value of activity could be determined, it could provide a useful tool for farmers and managers that serves as an early indicator of parasitism in sheep.

Social Barriers in Ecological Landscapes: The Social Resistance Hypothesis.

Across animal societies, individuals invest time and energy in social interactions. The social landscape that emerges from these interactions can then generate barriers that limit the ability of individuals to disperse to, and reproduce in, groups or populations. Therefore, social barriers can contribute to the difference between the physical capacity for movement through the habitat and subsequent gene flow. We call this contributing effect 'social resistance'. We propose that social resistance can act as an agent of selection on key life-history strategies and promote the evolution of social strategies that facilitate effective dispersal. By linking landscape genetics and social behaviour, the social resistance hypothesis generates predictions integrating dispersal, connectivity, and life-history evolution.

Unraveling the disease consequences and mechanisms of modular structure in animal social networks.

Disease risk is a potential cost of group living. Although modular organization is thought to reduce this cost in animal societies, empirical evidence toward this hypothesis has been conflicting. We analyzed empirical social networks from 43 animal species to motivate our study of the epidemiological consequences of modular structure in animal societies. From these empirical studies, we identified the features of interaction patterns associated with network modularity and developed a theoretical network model to investigate when and how subdivisions in social networks influence disease dynamics. Contrary to prior work, we found that disease risk is largely unaffected by modular structure, although social networks beyond a modular threshold experience smaller disease burden and longer disease duration. Our results illustrate that the lowering of disease burden in highly modular social networks is driven by two mechanisms of modular organization: network fragmentation and subgroup cohesion. Highly fragmented social networks with cohesive subgroups are able to structurally trap infections within a few subgroups and also cause a structural delay to the spread of disease outbreaks. Finally, we show that network models incorporating modular structure are necessary only when prior knowledge suggests that interactions within the population are highly subdivided. Otherwise, null networks based on basic knowledge about group size and local contact heterogeneity may be sufficient when data-limited estimates of epidemic consequences are necessary. Overall, our work does not support the hypothesis that modular structure universally mitigates the disease impact of group living.

What's your move? Movement as a link between personality and spatial dynamics in animal populations.

Recent studies have established the ecological and evolutionary importance of animal personalities. Individual differences in movement and space-use, fundamental to many personality traits (e.g. activity, boldness and exploratory behaviour) have been documented across many species and contexts, for instance personality-dependent dispersal syndromes. Yet, insights from the concurrently developing movement ecology paradigm are rarely considered and recent evidence for other personality-dependent movements and space-use lack a general unifying framework. We propose a conceptual framework for personality-dependent spatial ecology. We link expectations derived from the movement ecology paradigm with behavioural reaction-norms to offer specific predictions on the interactions between environmental factors, such as resource distribution or landscape structure, and intrinsic behavioural variation. We consider how environmental heterogeneity and individual consistency in movements that carry-over across spatial scales can lead to personality-dependent: (1) foraging search performance; (2) habitat preference; (3) home range utilization patterns; (4) social network structure and (5) emergence of assortative population structure with spatial clusters of personalities. We support our conceptual model with spatially explicit simulations of behavioural variation in space-use, demonstrating the emergence of complex population-level patterns from differences in simple individual-level behaviours. Consideration of consistent individual variation in space-use will facilitate mechanistic understanding of processes that drive social, spatial, ecological and evolutionary dynamics in heterogeneous environments.

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.

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.

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.

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.

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

We investigated transmission pathways for two tick species, Bothriocroton hydrosauri and Amblyomma limbatum, among their sleepy lizard (Tiliqua rugosa) hosts in a natural population in South Australia. Our aim was to determine whether a transmission network model continued to predict parasite load patterns effectively under varying ecological conditions. Using GPS loggers we identified the refuge sites used by each lizard on each day. We estimated infectious time windows for ticks that detached from a lizard in a refuge. Time windows were from the time when a detached tick molted and become infective, until the time it died from desiccation while waiting for a new host. Previous research has shown that A. limbatum molts earlier and survives longer than B. hydrosauri. We developed two transmission network models based on these differences in infective time windows for the two tick species. Directed edges were generated in the network if one lizard used a refuge that had previously been used by another lizard within the infectious time window. We used those models to generate values of network node in-strength for each lizard, a measure of how strongly connected an individual is to other lizards in the transmission network, and a prediction of infection risk for each host. The consistent correlations over time between B. hydrosauri infection intensity and network derived infection risk suggest that network models can be robust to environmental variation among years. However, the contrasting lack of consistent correlation in A. limbatum suggests that the utility of the same network models may depend on the specific biology of a parasite species.

The influence of refuge sharing on social behaviour in the lizard Tiliqua rugosa.

Refuge sharing by otherwise solitary individuals during periods of inactivity is an integral part of social behaviour and has been suggested to be the precursor to more complex social behaviour. We compared social association patterns of active versus inactive sheltering individuals in the social Australian sleepy lizard, Tiliqua rugosa, to empirically test the hypothesis that refuge sharing facilitates social associations while individuals are active. We fitted 18 neighbouring lizards with Global Positioning System (GPS) recorders to continuously monitor social associations among all individuals, based on location records taken every 10 min for 3 months. Based on these spatial data, we constructed three weighted, undirected social networks. Two networks were based on empirical association data (one for active and one for inactive lizards in their refuges), and a third null model network was based on hypothetical random refuge sharing. We found patterns opposite to the predictions of our hypothesis. Most importantly, association strength was higher in active than in inactive sheltering lizards. That is, individual lizards were more likely to associate with other lizards while active than while inactive and in shelters. Thus, refuge sharing did not lead to increased frequencies of social associations while lizards were active, and we did not find any evidence that refuge sharing was a precursor to sleepy lizard social behaviour. Our study of an unusually social reptile provides both quantitative data on the relationship between refuge sharing and social associations during periods of activity and further insights into the evolution of social behaviour in vertebrates.

Refuge sharing network predicts ectoparasite load in a lizard.

Living in social groups facilitates cross-infection by parasites. However, empirical studies on indirect transmission within wildlife populations are scarce. We investigated whether asynchronous overnight refuge sharing among neighboring sleepy lizards, Tiliqua rugosa, facilitates indirect transmission of its ectoparasitic tick, Amblyomma limbatum. We fitted 18 neighboring lizards with GPS recorders, observed their overnight refuge use each night over 3 months, and counted their ticks every fortnight. We constructed a transmission network to estimate the cross-infection risk based on asynchronous refuge sharing frequencies among all lizards and the life history traits of the tick. Although self-infection was possible, the network provided a powerful predictor of measured tick loads. Highly connected lizards that frequently used their neighbors' refuges were characterized by higher tick loads. Thus, indirect contact had a major influence on transmission pathways and parasite loads. Furthermore, lizards that used many different refuges had lower cross- and self-infection risks and lower tick loads than individuals that used relatively fewer refuges. Increasing the number of refuges used by a lizard may be an important defense mechanism against ectoparasite transmission in this species. Our study provides important empirical data to further understand how indirectly transmitted parasites move through host populations and influence individual parasite loads.