Experimental manipulation of food availability and macroparasite prevalence reveal differential effects on space use in wild rodents.

Research Highlight: Mistrick, J., Veitch, J. S. M., Kitchen, S. M., Clague, S., Newman, B. C., Hall, R. J., Budischak, S. A., Forbes, K. M., & Craft, M. E. (2024). Effects of food supplementation and helminth removal on space use and spatial overlap in wild rodent populations. Journal of Animal Ecology. http://doi.org/10.1111/1365-2656.14067. The spread of pathogens has been of long-standing interest, even before dramatic outbreaks of avian influenza and the coronavirus pandemic spiked broad public interest. However, the dynamics of pathogen spread in wild populations are complex, with multiple effects shaping where animals go (their space use), population density and, more fundamentally, the resultant patterns of contacts (direct or indirect) among individuals. Thus, experimental studies exploring the dynamics of contact under different sets of conditions are needed. In the current field study, Mistrick et al. (2024) used a multifactorial experimental design, manipulating food availability and individual pathogen infection state in wild bank voles (Clethrionomys glareolus). They found that while food availability, individual traits and seasonality can affect how far individual voles moved, the degree of overlap between individual voles remained largely the same despite a high variation in population density-which itself was affected by food availability. These results highlight how biotic and abiotic factors can shape patterns of space use and balance the level of spatial overlap through multiple pathways.

The presence of air sac nematodes in passerines and near-passerines in southern Germany.

Major climatic changes in conjunction with animal movement may be associated with the spread of parasites and their vectors into new populations, with potentially important consequences for population persistence. Parasites can evolve to adapt to unsuitable ecological conditions and take up refuge within new host species, with consequences for the population growth of the new host species. One parasite species that has likely been increasing its geographic range, and potentially infecting new hosts, is the recently described air sac nematode Serratospiculoides amaculata, in great tits (Parus major) in Slovakia. In this study, we screened wild birds for potential air sac nematode infection in a woodland area of southern Germany. We identified four additional host species: Eurasian nuthatch, great spotted woodpecker, greenfinch and robin. As infection by this group of nematodes can be highly pathogenic, we recommend further investigation into its potential risk to these populations.

The performance of field sampling for parasite detection in a wild passerine.

Parasites can impact the behavior of animals and alter the interplay with ecological factors in their environment. Studying the effects that parasites have on animals thus requires accurate estimates of infections in individuals. However, quantifying parasites can be challenging due to several factors. Laboratory techniques, physiological fluctuations, methodological constraints, and environmental influences can introduce measurement errors, in particular when screening individuals in the wild. These issues are pervasive in ecological studies where it is common to sample study subjects only once. Such factors should be carefully considered when choosing a sampling strategy, yet presently there is little guidance covering the major sources of error. In this study, we estimate the reliability and sensitivity of different sampling practices at detecting two internal parasites-Serratospiculoides amaculata and Isospora sp.-in a model organism, the great tit Parus major. We combine field and captive sampling to assess whether individual parasite infection status and load can be estimated from single field samples, using different laboratory techniques-McMaster and mini-FLOTAC. We test whether they vary in their performance, and quantify how sample processing affects parasite detection rates. We found that single field samples had elevated rates of false negatives. By contrast, samples collected from captivity over 24 h were highly reliable (few false negatives) and accurate (repeatable in the intensity of infection). In terms of methods, we found that the McMaster technique provided more repeatable estimates than the mini-FLOTAC for S. amaculata eggs, and both techniques were largely equally suitable for Isospora oocysts. Our study shows that field samples are likely to be unreliable in accurately detecting the presence of parasites and, in particular, for estimating parasite loads in songbirds. We highlight important considerations for those designing host-parasite studies in captive or wild systems giving guidance that can help select suitable methods, minimize biases, and acknowledge possible limitations.

The social transmission of stress in animal collectives.

The stress systems are powerful mediators between the organism's systemic dynamic equilibrium and changes in its environment beyond the level of anticipated fluctuations. Over- or under-activation of the stress systems' responses can impact an animal's health, survival and reproductive success. While physiological stress responses and their influence on behaviour and performance are well understood at the individual level, it remains largely unknown whether-and how-stressed individuals can affect the stress systems of other group members, and consequently their collective behaviour. Stressed individuals could directly signal the presence of a stressor (e.g. via an alarm call or pheromones), or an acute or chronic activation of the stress systems could be perceived by others (as an indirect cue) and spread via social contagion. Such social transmission of stress responses could then amplify the effects of stressors by impacting social interactions, social dynamics and the collective performance of groups. As the neuroendocrine pathways of the stress response are highly conserved among vertebrates, transmission of physiological stress states could be more widespread among non-human animals than previously thought. We therefore suggest that identifying the extent to which stress transmission modulates animal collectives represents an important research avenue.

Wild zebra finches that nest synchronously have long-term stable social ties.

Many animals live and breed in colonies, and yet, with just a few exceptions, the value of the social bonds between colony members has rarely been examined. Social ties are important for group coordination at collective tasks, and social coordination can facilitate synchronized reproduction among colony members. Synchronized reproduction in turn can amplify the benefits of coloniality, such as social foraging and predator avoidance. We conducted a field study to investigate whether synchronized reproduction among individuals in replicated colonies is linked to the strength of their social bond, and whether these strong bonds are maintained beyond the reproductive period. We PIT-tagged wild zebra finches (Taeniopygia guttata), monitoring their reproduction and social foraging over two consecutive years. We then used social network analysis to characterize the strength of social bonds among birds in the population. We show that birds that are more synchronized in their reproductive timing (and breed in the same colony) had significantly stronger social ties both during and after reproduction than expected by chance. Our long-term sampling also revealed that the strong social ties between synchronized breeders were carried over across years. Our study reveals a strong correspondence between synchronized breeding and the social structure of the breeding colony. This suggests that the synchrony between pairs is not a simple process based on opportunity, but a mechanism underpinned by more complex sociality, which could be carried over to other behavioural contexts. The maintenance of cross-contextual social ties across years suggests that social structure could have extensive consequences on the overall life history of individuals in addition to playing a key role for the reproductive dynamics of colonial breeders.

The importance of individual-to-society feedbacks in animal ecology and evolution.

The social decisions that individuals make-who to interact with and how frequently-give rise to social structure. The resulting social structure then determines how individuals interact with their surroundings-resources and risks, pathogens and predators, competitors and cooperators. However, despite intensive research on (a) how individuals make social decisions and (b) how social structure shapes social processes (e.g. cooperation, competition and conflict), there are still few studies linking these two perspectives. These perspectives represent two halves of a feedback loop: individual behaviour scales up to define the social environment, and this environment, in turn, feeds back by shaping the selective agents that drive individual behaviour. We first review well-established research areas that have captured both elements of this feedback loop-host-pathogen dynamics and cultural transmission. We then highlight areas where social structure is well studied but the two perspectives remain largely disconnected. Finally, we synthesise existing research on 14 distinct research topics to identify new prospects where the interplay between social structure and social processes are likely to be important but remain largely unexplored. Our review shows that the inherent links between individuals' traits, their social decisions, social structure and social evolution, warrant more consideration. By mapping the existing and missing connections among many research areas, our review highlights where explicitly considering social structure and the individual-to-society feedbacks can reveal new dimensions to old questions in ecology and evolution.

Family matters: skin microbiome reflects the social group and spatial proximity in wild zebra finches.

BACKGROUND: So far, large numbers of studies investigating the microbiome have focused on gut microbiota and less have addressed the microbiome of the skin. Especially in avian taxa our understanding of the ecology and function of these bacteria remains incomplete. The involvement of skin bacteria in intra-specific communication has recently received attention, and has highlighted the need to understand what information is potentially being encoded in bacterial communities. Using next generation sequencing techniques, we characterised the skin microbiome of wild zebra finches, aiming to understand the impact of sex, age and group composition on skin bacteria communities. For this purpose, we sampled skin swabs from both sexes and two age classes (adults and nestlings) of 12 different zebra finch families and analysed the bacterial communities. RESULTS: Using 16S rRNA sequencing we found no effect of age, sex and family on bacterial diversity (alpha diversity). However, when comparing the composition (beta diversity), we found that animals of social groups (families) harbour highly similar bacterial communities on their skin with respect to community composition. Within families, closely related individuals shared significantly more bacterial taxa than non-related animals. In addition, we found that age (adults vs. nestlings) affected bacterial composition. Finally, we found that spatial proximity of nest sites, and therefore individuals, correlated with the skin microbiota similarity. CONCLUSIONS: Birds harbour very diverse and complex bacterial assemblages on their skin. These bacterial communities are distinguishable and characteristic for intraspecific social groups. Our findings are indicative for a family-specific skin microbiome in wild zebra finches. Genetics and the (social) environment seem to be the influential factors shaping the complex bacterial communities. Bacterial communities associated with the skin have a potential to emit volatiles and therefore these communities may play a role in intraspecific social communication, e.g. via signalling social group membership.

Under the weather: Corticosterone levels in wild nestlings are associated with ambient temperature and wind.

Animals time reproductive events to overlap with periods of favorable environmental conditions. However, weather conditions can be unpredictable. Young animals may be particularly susceptible to extreme weather during sensitive developmental periods. Here, we investigated the effects of adverse weather conditions on corticosterone levels (a hormone linked to the avian stress response) and body condition of wild nestling zebra finches (Taeniopygia guttata). We sought to tease apart the direct versus indirect (i.e. parental) effects of weather on nestling physiology and condition by increasing parental work load with a clutch manipulation experiment. We found that high temperatures were associated with lower levels of restraint-induced corticosterone and high wind speeds were associated with higher levels of baseline corticosterone. We found no associations between weather and nestling body condition. However, clutch manipulation did affect body condition, with nestlings from experimentally enlarged clutches in worse condition compared to nestlings from experimentally reduced clutches. Our findings suggest that weather can directly affect wild nestlings via changes in corticosterone levels. Further research is needed to understand how changes in corticosterone levels affect phenotype and survival in wild nestlings. Understanding how developing animals respond to changes in environmental predictability and extreme weather is vital for understanding the potential for rapid adaptation in the face of changing climatic conditions.

Early-life social environment predicts social network position in wild zebra finches.

Early-life experience can fundamentally shape individual life-history trajectories. Previous research has suggested that exposure to stress during development causes differences in social behaviour later in life. In captivity, juvenile zebra finches exposed to elevated corticosterone levels were less socially choosy and more central in their social networks when compared to untreated siblings. These differences extended to other aspects of social life, with 'stress-exposed' juveniles switching social learning strategies and juvenile males less faithfully learning their father's song. However, while this body of research suggests that the impacts of early-life stress could be profound, it remains unknown whether such effects are strong enough to be expressed under natural conditions. Here, we collected data on social associations of zebra finches in the Australian desert after experimentally manipulating brood sizes. Juveniles from enlarged broods experienced heightened sibling competition, and we predicted that they would express similar patterns of social associations to stress-treated birds in the captive study by having more, but less differentiated, relationships. We show striking support for the suggested consequences of developmental stress on social network positions, with our data from the wild replicating the same results in 9 out of 10 predictions previously tested in captivity. Chicks raised in enlarged broods foraged with greater numbers of conspecifics but were less 'choosy' and more central in the social network. Our results confirm that the natural range of variation in early-life experience can be sufficient to predict individuals' social trajectories and support theory highlighting the potential importance of developmental conditions on behaviour.

Composition of Bacterial Assemblages in Different Components of Reed Warbler Nests and a Possible Role of Egg Incubation in Pathogen Regulation.

Bacteria play a central role in animal health. Yet, little is known about the acquisition of bacteria and the extent to which bacteria are acquired from different environmental sources. For example, bird nests host diverse bacteria associated with the eggs, nestlings and nesting material, but previous research has typically focussed on only a limited number of nest components at a time. It therefore remains unknown to what extent bacteria are transmitted between these components. Using both molecular and culture techniques, we characterised nest-associated bacterial assemblages throughout the entire nesting cycle of reed warblers by sampling bacteria on eggs before and during incubation, within nestling faeces, and on the nesting material of post-breeding nests. We found that bacterial assemblages clustered by nest component. Yet some overlap existed between nest components, suggesting that bacterial transmission across components is likely to occur. Eggs and nestlings from the same nest harboured more similar bacteria than expected by chance, suggesting an influence of environment or genetics on bacterial assemblages. Bacterial loads were not lower on incubated eggs. Instead, incubation was associated with a change in the structure of assemblages, including a decrease in potentially-harmful Gram-negative bacteria. In addition we show for the first time, that incubation is associated with the complete extinction of harmful haemolytic bacteria. Overall, our study appears to be the first to demonstrate differences in bacterial assemblages between bird nest components. In addition, we highlight the complexity of nest bacterial assemblages and provide new insights into the benefits of incubation.

Age-related differences in the cloacal microbiota of a wild bird species.

BACKGROUND: Gastrointestinal bacteria play a central role in the health of animals. The bacteria that individuals acquire as they age may therefore have profound consequences for their future fitness. However, changes in microbial community structure with host age remain poorly understood. We characterised the cloacal bacteria assemblages of chicks and adults in a natural population of black-legged kittiwakes (Rissa tridactyla), using molecular methods. RESULTS: We show that the kittiwake cloaca hosts a diverse assemblage of bacteria. A greater number of total bacterial OTUs (operational taxonomic units) were identified in chicks than adults, and chicks appeared to host a greater number of OTUs that were only isolated from single individuals. In contrast, the number of bacteria identified per individual was higher in adults than chicks, while older chicks hosted more OTUs than younger chicks. Finally, chicks and adults shared only seven OTUs, resulting in pronounced differences in microbial assemblages. This result is surprising given that adults regurgitate food to chicks and share the same nesting environment. CONCLUSIONS: Our findings suggest that chick gastrointestinal tracts are colonised by many transient species and that bacterial assemblages gradually transition to a more stable adult state. Phenotypic differences between chicks and adults may lead to these strong differences in bacterial communities. These data provide the framework for future studies targeting the causes and consequences of variation in bacterial assemblages in wild birds.

The Homing Frog: High Homing Performance in a Territorial Dendrobatid Frog Allobates femoralis (Dendrobatidae).

Dendrobatidae (dart-poison frogs) exhibit some of the most complex spatial behaviors among amphibians, such as territoriality and tadpole transport from terrestrial clutches to widely distributed deposition sites. In species that exhibit long-term territoriality, high homing performance after tadpole transport can be assumed, but experimental evidence is lacking, and the underlying orientation mechanisms are unknown. We conducted a field translocation experiment to test whether male Allobates femoralis, a dendrobatid frog with paternal extra-territorial tadpole transport, are capable of homing after experimental removal, as well as to quantify homing success and speed. Translocated individuals showed a very high homing success for distances up to 200 m and successfully returned from up to 400 m. We discuss the potential orientation mechanisms involved and selective forces that could have shaped this strong homing ability.