Showing papers in "Journal of Animal Ecology in 2018"

A computer vision for animal ecology.

Abstract: 1.A central goal of animal ecology is to observe species in the natural world. The cost and challenge of data collection often limit the breadth and scope of ecological study. Ecologists often use image capture to bolster data collection in time and space. However, the ability to process these images remains a bottleneck. 2.Computer vision can greatly increase the efficiency, repeatability, and accuracy of image review. Computer vision uses image features, such as color, shape, and texture to infer image content. 3.I provide a brief primer on ecological computer vision to outline its goals, tools and applications to animal ecology. 4.I reviewed 187 existing applications of computer vision and divided articles into ecological description, counting, and identity tasks. 5.I discuss recommendations for enhancing the collaboration between ecologists and computer scientists and highlight areas for future growth of automated image analysis. This article is protected by copyright. All rights reserved.

Revisiting concepts of thermal physiology: Predicting responses of mammals to climate change.

Abstract: The accuracy of predictive models (also known as mechanistic or causal models) of animal responses to climate change depends on properly incorporating the principles of heat transfer and thermoregulation into those models. Regrettably, proper incorporation of these principles is not always evident. We have revisited the relevant principles of thermal physiology and analysed how they have been applied in predictive models of large mammals, which are particularly vulnerable, to climate change. We considered dry heat exchange, evaporative heat transfer, the thermoneutral zone and homeothermy, and we examined the roles of size and shape in the thermal physiology of large mammals. We report on the following misconceptions in influential predictive models: underestimation of the role of radiant heat transfer, misassignment of the role and misunderstanding of the sustainability of evaporative cooling, misinterpretation of the thermoneutral zone as a zone of thermal tolerance or as a zone of sustainable energetics, confusion of upper critical temperature and critical thermal maximum, overestimation of the metabolic energy cost of evaporative cooling, failure to appreciate that the current advantages of size and shape will become disadvantageous as climate change advances, misassumptions about skin temperature and, lastly, misconceptions about the relationship between body core temperature and its variability with body mass in large mammals. Not all misconceptions invalidate the models, but we believe that preventing inappropriate assumptions from propagating will improve model accuracy, especially as models progress beyond their current typically static format to include genetic and epigenetic adaptation that can result in phenotypic plasticity.

A practical guide for inferring reliable dominance hierarchies and estimating their uncertainty

Abstract: Many animal social structures are organized hierarchically, with some individuals monopolizing resources. Dominance hierarchies have received great attention from behavioural and evolutionary ecologists. There are many methods for inferring hierarchies from social interactions. Yet, there are no clear guidelines about how many observed dominance interactions (i.e. sampling effort) are necessary for inferring reliable dominance hierarchies, nor are there any established tools for quantifying their uncertainty. We simulate interactions (winners and losers) in scenarios of varying steepness (the probability that a dominant defeats a subordinate based on their difference in rank). Using these data, we (1) quantify how the number of interactions recorded and the steepness of the hierarchy affect the performance of five methods for inferring hierarchies, (2) propose an amendment that improves the performance of a popular method, and (3) suggest two easy procedures to measure uncertainty and steepness in the inferred hierarchy. We find that the ratio of interactions to individuals required to infer reliable hierarchies is surprisingly low, but depends on the steepness of the hierarchy and the method used. We show that David's score and our novel randomized Elo-rating are the best methods when hierarchies are not extremely steep, where the original Elo-rating, the I&SI and the recently described ADAGIO perform less well. In addition, we show that two simple methods can be used to estimate uncertainty at the individual and group level, and that the randomized Elo-rating repeatability provides researchers with a standardized measure valid for comparing the steepness of different hierarchies. We provide several worked examples to guide researchers interested in studying dominance hierarchies. Methods for inferring dominance hierarchies are relatively robust. We recommend that a ratio of observed interactions to individuals of at least 10 (for steep hierarchies), and ideally 20 serves as a good benchmark. Our simple procedures for estimating uncertainty in the observed data will facilitate evaluating whether sufficient data have been collected, while plotting the shape of the hierarchy will provide new insights into the social structure of the study organism.

Nowhere to hide: Effects of linear features on predator–prey dynamics in a large mammal system

Abstract: Rapid landscape alteration associated with human activity is currently challenging the evolved dynamical stability of many predator-prey systems by forcing species to behaviourally respond to novel environmental stimuli. In many forested systems, linear features (LFs) such as roads, pipelines and resource exploration lines (i.e. seismic lines) are a ubiquitous form of landscape alteration that have been implicated in altering predator-prey dynamics. One hypothesized effect is that LFs facilitate predator movement into and within prey refugia, thereby increasing predator-prey spatial overlap. We evaluated this hypothesis in a large mammal system, focusing on the interactions between boreal woodland caribou (Rangifer tarandus caribou) and their two main predators, wolves (Canis lupus) and black bears (Ursus americanus), during the calving season of caribou. In this system, LFs extend into and occur within peatlands (i.e. bogs and nutrient-poor fens), a habitat type highly used by caribou due to its refugia effects. Using resource selection analyses, we found that LFs increased predator selection of peatlands. Female caribou appeared to respond by avoiding LFs and areas with high LF density. However, in our study area, most caribou cannot completely avoid exposure to LFs and variation in female response had demographic effects. In particular, increasing proportional use of LFs by females negatively impacted survival of their neonate calves. Collectively, these results demonstrate how LFs can reduce the efficacy of prey refugia. Mitigating such effects will require limiting or restoring LFs within prey refugia, although the effectiveness of mitigation efforts will depend upon spatial scale, which in turn will be influenced by the life-history traits of predator and prey.

Invasive earthworms erode soil biodiversity: A meta-analysis

Abstract: Biological invasions pose a serious threat to biodiversity and ecosystem functioning across ecosystems. Invasions by ecosystem engineers, in particular, have been shown to have dramatic effects in recipient ecosystems. For instance, invasion by earthworms, a below-ground invertebrate ecosystem engineer, in previously earthworm-free ecosystems alters the physico-chemical characteristics of the soil. Studies have shown that such alterations in the soil can have far-reaching impacts on soil organisms, which form a major portion of terrestrial biodiversity. Here, we present the first quantitative synthesis of earthworm invasion effects on soil micro-organisms and soil invertebrates based on 430 observations from 30 independent studies. Our meta-analysis shows a significant decline of the diversity and density of soil invertebrates in response to earthworm invasion with anecic and endogeic earthworms causing the strongest effects. Earthworm invasion effects on soil micro-organisms were context-dependent, such as depending on functional group richness of invasive earthworms and soil depth. Microbial biomass and diversity increased in mineral soil layers, with a weak negative effect in organic soil layers, indicating that the mixing of soil layers by earthworms (bioturbation) may homogenize microbial communities across soil layers. Our meta-analysis provides a compelling evidence for negative effects of a common invasive below-ground ecosystem engineer on below-ground biodiversity of recipient ecosystems, which could potentially alter the ecosystem functions and services linked to soil biota.

Ants are the major agents of resource removal from tropical rainforests.

Abstract: Ants are diverse and abundant, especially in tropical ecosystems. They are often cited as the agents of key ecological processes, but their precise contributions compared with other organisms have rarely been quantified. Through the removal of food resources from the forest floor and subsequent transport to nests, ants play an important role in the redistribution of nutrients in rainforests. This is an essential ecosystem process and a key energetic link between higher trophic levels, decomposers and primary producers. We used the removal of carbohydrate, protein and seed baits as a proxy to quantify the contribution that ants, other invertebrates and vertebrates make to the redistribution of nutrients around the forest floor, and determined to what extent there is functional redundancy across ants, other invertebrate and vertebrate groups. Using a large-scale, field-based manipulation experiment, we suppressed ants from c. 1 ha plots in a lowland tropical rainforest in Sabah, Malaysia. Using a combination of treatment and control plots, and cages to exclude vertebrates, we made food resources available to: (i) the whole foraging community, (ii) only invertebrates and (iii) only non-ant invertebrates. This allowed us to partition bait removal into that taken by vertebrates, non-ant invertebrates and ants. Additionally, we examined how the non-ant invertebrate community responded to ant exclusion. When the whole foraging community had access to food resources, we found that ants were responsible for 52% of total bait removal whilst vertebrates and non-ant invertebrates removed the remaining 48%. Where vertebrates were excluded, ants carried out 61% of invertebrate-mediated bait removal, with all other invertebrates removing the remaining 39%. Vertebrates were responsible for just 24% of bait removal and invertebrates (including ants) collectively removed the remaining 76%. There was no compensation in bait removal rate when ants and vertebrates were excluded, indicating low functional redundancy between these groups. This study is the first to quantify the contribution of ants to the removal of food resources from rainforest floors and thus nutrient redistribution. We demonstrate that ants are functionally unique in this role because no other organisms compensated to maintain bait removal rate in their absence. As such, we strengthen a growing body of evidence establishing ants as ecosystem engineers, and provide new insights into the role of ants in maintaining key ecosystem processes. In this way, we further our basic understanding of the functioning of tropical rainforest ecosystems.

Effects of host species and environment on the skin microbiome of Plethodontid salamanders

Abstract: Summary 1.The amphibian skin microbiome is recognized for its role in defense against pathogens, including the deadly fungal pathogen Batrachochytrium dendrobatidis (Bd). Yet, we have little understanding of evolutionary and ecological processes that structure these communities, especially for salamanders and closely related species. We investigated patterns in the distribution of bacterial communities on Plethodon salamander skin across host species and environments. 2.Quantifying salamander skin microbiome structure contributes to our understanding of how host-associated bacteria are distributed across the landscape, among host species, and their putative relationship with disease. 3.We characterized skin microbiome structure (alpha-diversity, beta-diversity and bacterial operational taxonomic unit [OTU] abundances) using 16S rRNA gene sequencing for co-occurring Plethodon salamander species (35 P. cinereus, 17 P. glutinosus, 10 P. cylindraceus) at three localities to differentiate the effects of host species from environmental factors on the microbiome. We sampled the microbiome of P. cinereus along an elevational gradient (n = 50, 700 – 1000 masl) at one locality to determine whether elevation predicts microbiome structure. Finally, we quantified prevalence and abundance of putatively anti-Bd bacteria to determine if Bd-inhibitory bacteria are dominant microbiome members. 4.Co-occurring salamanders had similar microbiome structure, but among sites salamanders had dissimilar microbiome structure for beta-diversity and abundance of 28 bacterial OTUs. We found that alpha-diversity increased with elevation, beta-diversity and the abundance of 17 bacterial OTUs changed with elevation (16 OTUs decreasing, 1 OTU increasing). We detected 11 putatively anti-Bd bacterial OTUs that were present on 90% of salamanders and made up an average relative abundance of 83% (SD ± 8.5) per salamander. All salamanders tested negative for Bd. 5.We conclude that environment is more influential in shaping skin microbiome structure than host differences for these congeneric species, and suggest that environmental characteristics that co-vary with elevation influence microbiome structure. High prevalence and abundance of anti-Bd bacteria may contribute to low Bd levels in these populations of Plethodon salamanders. This article is protected by copyright. All rights reserved.

Disease implications of animal social network structure: A synthesis across social systems

Abstract: The disease costs of sociality have largely been understood through the link between group size and transmission. However, infectious disease spread is driven primarily by the social organization of interactions in a group and not its size. We used statistical models to review the social network organization of 47 species, including mammals, birds, reptiles, fish and insects by categorizing each species into one of three social systems, relatively solitary, gregarious and socially hierarchical. Additionally, using computational experiments of infection spread, we determined the disease costs of each social system. We find that relatively solitary species have large variation in number of social partners, that socially hierarchical species are the least clustered in their interactions, and that social networks of gregarious species tend to be the most fragmented. However, these structural differences are primarily driven by weak connections, which suggest that different social systems have evolved unique strategies to organize weak ties. Our synthetic disease experiments reveal that social network organization can mitigate the disease costs of group living for socially hierarchical species when the pathogen is highly transmissible. In contrast, highly transmissible pathogens cause frequent and prolonged epidemic outbreaks in gregarious species. We evaluate the implications of network organization across social systems despite methodological challenges, and our findings offer new perspective on the debate about the disease costs of group living. Additionally, our study demonstrates the potential of meta-analytic methods in social network analysis to test ecological and evolutionary hypotheses on cooperation, group living, communication and resilience to extrinsic pressures.

Ecological determinants of avian malaria infections: An integrative analysis at landscape, mosquito and vertebrate community levels

Abstract: Vector and host communities, as well as habitat characteristics, may have important but different impacts on the prevalence, richness and evenness of vector-borne parasites. We investigated the relative importance of (1) the mosquito community composition, (2) the vertebrate community composition and (3) landscape characteristics on the prevalence, richness and evenness of avian Plasmodium. We hypothesized that parasite prevalence will be more affected by vector-related parameters, while host parameters should be also important to explain Plasmodium richness and evenness. We sampled 2,588 wild house sparrows (Passer domesticus) and 340,829 mosquitoes, and we performed vertebrate censuses at 45 localities in the Southwest of Spain. These localities included urban, rural and natural landscapes that were characterized by several habitat variables. Twelve Plasmodium lineages were identified in house sparrows corresponding to three major clades. Variation partitioning showed that landscape characteristics explained the highest fraction of variation in all response variables (21.0%-44.8%). Plasmodium prevalence was in addition explained by vector-related variables (5.4%) and its interaction with landscape (10.2%). Parasite richness and evenness were mostly explained by vertebrate community-related variables. The structuring role of landscape characteristics in vector and host communities was a key factor in determining parasite prevalence, richness and evenness, although the role of each factor differed according to the parasite parameters studied. These results show that the biotic and abiotic contexts are important to explain the transmission dynamics of mosquito-borne pathogens in the wild.

Decreases in beetle body size linked to climate change and warming temperatures.

Abstract: Body size is a fundamental ecological trait and is correlated with population dynamics, community structure and function, and ecosystem fluxes. Laboratory data from broad taxonomic groups suggest that a widespread response to a warming world may be an overall decrease in organism body size. However, given the myriad of biotic and abiotic factors that can also influence organism body size in the wild, it is unclear whether results from these laboratory assays hold in nature. Here we use datasets spanning 30 to 100 years to examine whether the body size of wild-caught beetles has changed over time, whether body size changes are correlated with increased temperatures, and we frame these results using predictions derived from a quantitative review of laboratory responses of 22 beetle species to temperature. We found that 95% of laboratory-reared beetles decreased in size with increased rearing temperature, with larger-bodied species shrinking disproportionately more than smaller-bodied beetles. In addition, the museum datasets revealed that larger-bodied beetle species have decreased in size over time, that mean beetle body size explains much of the interspecific variation in beetle responses to temperature, and that long-term beetle size changes are explained by increases in autumn temperature and decreases in spring temperature in this region. Our data demonstrate that the relationship between body size and temperature of wild-caught beetles matches relatively well with results from laboratory studies, and that variation in this relationship is largely explained by interspecific variation in mean beetle body size. This long-term beetle dataset is one of the most comprehensive arthropod body size datasets compiled to date, it improves predictions regarding the shrinking of organisms with global climate change, and together with the meta-analysis data, call for new hypotheses to explain why larger-bodied organisms may be more sensitive to temperature.

When to choose dynamic vs. static social network analysis.

Abstract: There is increasing interest in using dynamic social networks in the study of animal sociality and its consequences. However, there is a general lack of guidance on the when and how such an approach will be valuable. The aim of this paper is to provide a guide on when to choose dynamic vs. static social network analysis, and how to choose the appropriate temporal scale for the dynamic network. I first discuss the motivations for using dynamic animal social networks. I then provide guidance on how to choose between dynamic networks and the "standard" approach of using static networks. I discuss this in the context of the temporal scale of changes observed, of their predictability and of the data availability. Dynamic networks are important in a number of scenarios. First, if the network data are being compared to independent processes, such as the spread of information or disease or environmental changes, then dynamic networks will provide more accurate estimates of spreading rates. Second, if the network has predictable patterns of change, for example diel cycles or seasonal changes, then dynamic networks should be used to capture the impact of these changes. Third, dynamic networks are important for studies of spread through networks when the relationship between edge weight and transmission probability is nonlinear. Finally, dynamic social networks are also useful in situations where interactions among individuals are dense, such as in studies of captive groups. The use of static vs. dynamic network requires careful consideration, both from a research question perspective and from a data perspective, and this paper provides a guide on how to evaluate the relative importance of these.

A global database and “state of the field” review of research into ecosystem engineering by land animals

Abstract: Ecosystem engineers have been widely studied for terrestrial systems, but global trends in research encompassing the range of taxa and functions have not previously been synthesised. We reviewed contemporary understanding of engineer fauna in terrestrial habitats and assessed the methods used to document patterns and processes, asking: (a) which species act as ecosystem engineers and with whom do they interact? (b) What are the impacts of ecosystem engineers in terrestrial habitats and how are they distributed? (c) What are the primary methods used to examine engineer effects and how have these developed over time? We considered the strengths, weaknesses and gaps in knowledge related to each of these questions and suggested a conceptual framework to delineate "significant impacts" of engineering interactions for all terrestrial animals. We collected peer-reviewed publications examining ecosystem engineer impacts and created a database of engineer species to assess experimental approaches and any additional covariates that influenced the magnitude of engineer impacts. One hundred and twenty-two species from 28 orders were identified as ecosystem engineers, performing five ecological functions. Burrowing mammals were the most researched group (27%). Half of all studies occurred in dry/arid habitats. Mensurative studies comparing sites with and without engineers (80%) were more common than manipulative studies (20%). These provided a broad framework for predicting engineer impacts upon abundance and species diversity. However, the roles of confounding factors, processes driving these patterns and the consequences of experimentally adjusting variables, such as engineer density, have been neglected. True spatial and temporal replication has also been limited, particularly for emerging studies of engineer reintroductions. Climate change and habitat modification will challenge the roles that engineers play in regulating ecosystems, and these will become important avenues for future research. We recommend future studies include simulation of engineer effects and experimental manipulation of engineer densities to determine the potential for ecological cascades through trophic and engineering pathways due to functional decline. We also recommend improving knowledge of long-term engineering effects and replication of engineer reintroductions across landscapes to better understand how large-scale ecological gradients alter the magnitude of engineering impacts.

An evolutionary framework outlining the integration of individual social and spatial ecology.

Abstract: Behaviour is the interface between an organism and its environment, and behavioural plasticity is important for organisms to cope with environmental change. Social behaviour is particularly important because sociality is a dynamic process, where environmental variation influences group dynamics and social plasticity can mediate resource acquisition. Heterogeneity in the ecological environment can therefore influence the social environment. The combination of the ecological and social environments may be interpreted collectively as the "socioecological environment," which could explain variation in fitness. Our objective was to outline a framework through which individual social and spatial phenotypes can be integrated and interpreted as phenotypes that covary as a function of changes in the socioecological environment. We propose the socioecological environment is composed of individual behavioural traits, including sociality and habitat selection, both of which are repeatable, potentially heritable and may reflect animal personality traits. We also highlight how ecological and social niche theory can be applied to the socioecological environment framework, where individuals occupy different socioecological niches. Individual sociality and habitat selection are also density-dependent, and theory predicts that density-dependent traits should affect reproduction, survival, and therefore fitness and population dynamics. We then illustrate the proximate links between sociality, habitat selection and fitness as well as the ultimate, and possibly adaptive, consequences associated with changes in population density. The ecological, evolutionary and applied implications of our proposed socioecological environment framework are broad and changes in density could influence individual fitness and population dynamics. For instance, human-induced environmental changes can influence population density, which can affect the distribution of social and spatial phenotypes within a population. In summary, we outline a conceptual framework that incorporates individual social and spatial behavioural traits with fitness and we highlight a range of ecological and evolutionary processes that are likely associated with the socioecological environment.

Using experimentation to understand the 10‐year snowshoe hare cycle in the boreal forest of North America

Abstract: Summary Population cycles have long fascinated ecologists from the time of Charles Elton in the 1920s. The discovery of large population fluctuations in undisturbed ecosystems challenged the idea that pristine nature was in a state of balance. The 10-year cycle of snowshoe hares (Lepus americanus Erxleben) across the boreal forests of Canada and Alaska is a classic cycle, recognized by fur traders for more than 300 years. Since the 1930s ecologists have investigated the mechanisms that might cause these cycles. Proposed causal mechanisms have varied from sunspots to food supplies, parasites, diseases, predation, and social behaviour. Both the birth rate and the death rate change dramatically over the cycle. Social behaviour was eliminated as a possible cause because snowshoe hares are not territorial and do not commit infanticide. Since the 1960s large-scale manipulative experiments have been used to discover the major limiting factors. Food supply and predation quickly became recognized as potential key factors causing the cycle. Experiments adding food and restricting predator access to field populations have been decisive in pinpointing predation as the key mechanism causing these fluctuations. The immediate cause of death of most snowshoe hares is predation by a variety of predators, including the Canada lynx (Lynx canadensis Kerr). The collapse in the reproductive rate is not due to food shortage as was originally thought, but is a result of chronic stress from predator chases. Five major issues remain unresolved. First, what is the nature of the predator-induced memory that results in the prolonged low phase of the cycle? Second, why do hare cycles form a travelling wave, starting in the centre of the boreal forest in Saskatchewan and travelling across western Canada and Alaska? Third, why does the amplitude of the cycle vary greatly from one cycle to the next in the same area? Fourth, do the same mechanisms of population limitation apply to snowshoe hares in eastern North American or in similar ecosystems across Siberia? Finally, what effect will climatic warming have on all the above issues? The answers to these questions remain for future generations of biologists to determine. This article is protected by copyright. All rights reserved.

Desynchronizations in bee-plant interactions cause severe fitness losses in solitary bees.

Abstract: 1.Global warming can disrupt mutualistic interactions between solitary bees and plants when increasing temperature differentially changes the timing of interacting partners. One possible scenario is for insect phenology to advance more rapidly than plant phenology. 2.However, empirical evidence for fitness consequences due to temporal mismatches is lacking for pollinators and it remains unknown if bees have developed strategies to mitigate fitness losses following temporal mismatches. 3.We tested the effect of temporal mismatches on the fitness of three spring-emerging solitary bee species, including one pollen specialist. Using flight cages, we simulated (i) a perfect synchronization (from a bee perspective): bees and flowers occur simultaneously, (ii) a mismatch of three days and (iii) a mismatch of six days, with bees occurring earlier than flowers in the latter two cases. 4.A mismatch of six days caused severe fitness losses in all three bee species, as few bees survived without flowers. Females showed strongly reduced activity and reproductive output compared to synchronized bees. Fitness consequences of a three day mismatch were species-specific. Both the early-spring species Osmia cornuta and the mid-spring species Osmia bicornis produced the same number of brood cells after a mismatch of three days as under perfect synchronization. However, O. cornuta decreased the number of female offspring, whereas O. bicornis spread the brood cells over fewer nests, which may increase offspring mortality e.g. due to parasitoids. The late-spring specialist Osmia brevicornis produced fewer brood cells even after a mismatch of three days. Additionally, our results suggest that fitness losses after temporal mismatches are higher during warm than cold springs, as the naturally occurring temperature variability revealed that warm temperatures during starvation decreased the survival rate of O. bicornis. 5.We conclude that short temporal mismatches can cause clear fitness losses in solitary bees. Although our results suggest that bees have evolved species-specific strategies to mitigate fitness losses after temporal mismatches, the bees were not able to completely compensate for impacts on their fitness after temporal mismatches with their food resources. This article is protected by copyright. All rights reserved.

Gut microbial communities of American pikas (Ochotona princeps): Evidence for phylosymbiosis and adaptations to novel diets.

Abstract: Gut microbial communities provide many physiological functions to their hosts, especially in herbivorous animals. We still lack an understanding of how these microbial communities are structured across hosts in nature, especially within a given host species. Studies on laboratory mice have demonstrated that host genetics can influence microbial community structure, but that diet can overwhelm these genetic effects. We aimed to test these ideas in a natural system, the American pika (Ochotona princeps). First, pikas are high-elevation specialists with significant population structure across various mountain ranges in the USA, allowing us to investigate whether similarities in microbial communities match host genetic differences. Additionally, pikas are herbivorous, with some populations exhibiting remarkable dietary plasticity and consuming high levels of moss, which is exceptionally high in fibre and low in protein. This allows us to investigate adaptations to an herbivorous diet, as well as to the especially challenging diet of moss. Here, we inventoried the microbial communities of pika caecal pellets from various populations using 16S rRNA sequencing to investigate structuring of microbial communities across various populations with different natural diets. Microbial communities varied significantly across populations, and differences in microbial community structure were congruent with genetic differences in host population structure, a pattern known as "phylosymbiosis." Several microbial members (Ruminococcus, Prevotella, Oxalobacter and Coprococcus) were detected across all samples, and thus likely represent a "core microbiome." These genera are known to perform a number of services for herbivorous hosts such as fibre fermentation and the degradation of plant defensive compounds, and thus are likely important for herbivory in pikas. Moreover, pikas that feed on moss harboured microbial communities highly enriched in Melainabacteria. This uncultivable candidate phylum has been proposed to ferment fibre for herbivores, and thus may contribute to the ability of some pika populations to consume high amounts of moss. These findings demonstrate that both host genetics and diet can influence the microbial communities of the American pika. These animals may be novel sources of fibre-degrading microbes. Last, we discuss the implications of population-specific microbial communities for conservation efforts in this species.

Spatio-temporal variation in lifelong telomere dynamics in a long-term ecological study

Abstract: Understanding individual-level variation in response to the environment is fundamental to understanding life-history evolution and population dynamics. Telomeres, the protective caps at the ends of chromosomes, shorten in response to oxidative stress, and telomere shortening is correlated with reduced survival and life span. Investigating telomere dynamics may help us quantify individual variation in the costs experienced from social and ecological factors, and enhance our understanding of the dynamics of natural populations. Here, we study spatio-temporal variation in lifelong telomere dynamics in the Seychelles warbler, Acrocephalus sechellensis. We combine long-term life history and ecological data with a large longitudinal dataset of mean telomere lengths, consisting of 1,808 samples from 22 cohorts born between 1993 and 2014. We provide a detailed analysis of how telomere dynamics vary over individual life spans and cohorts, and with spatio-temporal variation in the social and ecological environment. We found that telomere length decreases with cross-sectional and longitudinal measures of age, and most rapidly very early in life. However, both cross-sectional and longitudinal data suggested that against this overall pattern of shortening, bouts of telomere length increase occur in some individuals. Using a large number of repeated measurements we show statistically that these increases are unlikely to be explained solely by qPCR measurement error. Telomere length varied markedly among cohorts. Telomere length was positively associated with temporal variation in island-wide insect abundance-a key resource for the insectivorous Seychelles warbler-suggesting that the costs associated with living in harsher environments can be studied by investigating telomere dynamics. We also found evidence for sex-specific relationships between telomeres and tarsus length, potentially reflecting differential costs of growth. Our long-term data show that in a natural population, telomere dynamics vary in a complex manner over individual life spans, and across space and time. Variance in telomere dynamics among individuals is the product of a wide array of genetic, parental and environmental factors. Explaining this variation more fully will require the integration of comprehensive long-term ecological and genetic data from multiple populations and species.

On the development of a predictive functional trait approach for studying terrestrial arthropods.

Abstract: The characterization of ecological communities with functional traits allows to consider simultaneously the ability of a species to survive and reproduce in an environment, its interactions with other species and its effects on the ecosystem. Functional traits have been studied mainly by plant ecologists, but are increasingly common in the study of other taxa including arthropods. Arthropods represent a group for which a functional trait approach could be highly profitable because of their high diversity, abundance, ubiquity and role in many important ecological processes. This review synthesizes two decades of functional trait research on terrestrial arthropods. We show that while the approach has gained popularity, particularly in the last decade, the absence of clearly postulated hypotheses is a recurrent problem limiting generalization. Furthermore, studied traits are often poorly related to studied functions. To address these problems, we propose a step-by-step protocol to postulate clear hypotheses prior to trait selection and emphasize the need for a common set of more generalizable traits in future studies. Extending the functional trait approach to arthropods opens the door to improving our understanding of interspecific interactions and potential links between response and effect traits. We present the concept of trait-matching with several examples of arthropod traits known to be effective predictors of consumer-resource interactions. The development of a successful functional trait approach for terrestrial arthropods will necessitate an understanding of relevant traits, standardized measurement protocols and open access databases to share this information. Such progress will provide ecologists with a new set of tools to answer broad questions in several fields including the study of community assembly, ecological networks and multitrophic functionality.

Moving from frugivory to seed dispersal: Incorporating the functional outcomes of interactions in plant–frugivore networks

Abstract: There is growing interest in understanding the functional outcomes of species interactions in ecological networks. For many mutualistic networks, including pollination and seed dispersal networks, interactions are generally sampled by recording animal foraging visits to plants. However, these visits may not reflect actual pollination or seed dispersal events, despite these typically being the ecological processes of interest. Frugivorous animals can act as seed dispersers, by swallowing entire fruits and dispersing their seeds, or as pulp peckers or seed predators, by pecking fruits to consume pieces of pulp or seeds. These processes have opposing consequences for plant reproductive success. Therefore, equating visitation with seed dispersal could lead to biased inferences about the ecology, evolution and conservation of seed dispersal mutualisms. Here, we use natural history information on the functional outcomes of pairwise bird-plant interactions to examine changes in the structure of seven European plant-frugivore visitation networks after non-mutualistic interactions (pulp pecking and seed predation) have been removed. Following existing knowledge of the contrasting structures of mutualistic and antagonistic networks, we hypothesized a number of changes following interaction removal, such as increased nestedness and lower specialization. Non-mutualistic interactions with pulp peckers and seed predators occurred in all seven networks, accounting for 21%-48% of all interactions and 6%-24% of total interaction frequency. When non-mutualistic interactions were removed, there were significant increases in network-level metrics such as connectance and nestedness, while robustness decreased. These changes were generally small, homogenous and driven by decreases in network size. Conversely, changes in species-level metrics were more variable and sometimes large, with significant decreases in plant degree, interaction frequency, specialization and resilience to animal extinctions and significant increases in frugivore species strength. Visitation data can overestimate the actual frequency of seed dispersal services in plant-frugivore networks. We show here that incorporating natural history information on the functions of species interactions can bring us closer to understanding the processes and functions operating in ecological communities. Our categorical approach lays the foundation for future work quantifying functional interaction outcomes along a mutualism-antagonism continuum, as documented in other frugivore faunas.

Parasite–microbiota interactions potentially affect intestinal communities in wild mammals

Abstract: Detecting interaction between species is notoriously difficult, and disentangling species associations in host-related gut communities is especially challenging. Nevertheless, due to contemporary methods, including metabarcoding and 16S sequencing, collecting observational data on community composition has become easier and much more common. We studied the previously collected datasets of intestinal bacterial microbiota and parasite compositions within longitudinally followed mouse lemurs by analysing the potential interactions with diversity metrics and novel joint species distribution modelling. Both methods showed statistical association between certain parasite species and bacterial microbiota composition. Unicellular Eimeria sp. had an effect on diversity of gut microbiota. The cestode Hymenolepis diminuta had negative associations with several bacterial orders, whereas closely related species Hymenolepis nana had positive associations with several bacterial orders. Our results reveal potential interactions between some, but not all, intestinal parasites and gut bacterial microbiota. Host variables contributed over half of the total variation explained with the model, and sex was the most important single host variable; especially with microbiota, there were sex-related differences in the community composition. This study shows how joint species distribution modelling can incorporate both within-host dynamics of several taxa and host characteristics to model potential interactions in intestinal community. These results provide new hypothesis for interactions between and among parasites and bacterial microbiota to be tested further with experimental studies.

Immune priming specificity within and across generations reveals the range of pathogens affecting evolution of immunity in an insect

Abstract: Many organisms can improve their immune response as a function of their immunological experience or that of their parents. This phenomenon, called immune priming, has likely evolved from repetitive challenges by the same pathogens during the host lifetime or across generation. All pathogens may not expose host to the same probability of re-infection, and immune priming is expected to evolve from pathogens exposing the host to the greatest probability of re-infection. Under this hypothesis, the priming response to these pathogens should be specifically more efficient and less costly than to others. We examined the specificity of immune priming within and across generations in the mealworm beetle, Tenebrio molitor, by comparing survival of individuals to infection with bacteria according to their own immunological experience or that of their mother with these bacteria. We found that insects primed with Gram-positive bacteria became highly protected against both Gram-positive and Gram-negative bacterial infections, mainly due to an induced persistent antibacterial response, which did not exist in insects primed with Gram-negative bacteria. Insects primed with Gram-positive bacteria also exhibited enhanced concentration of haemocytes, but their implication in acquired resistance was not conclusive because of the persistent antibacterial activity in the haemolymph. Offspring maternally primed with Gram-positive and Gram-negative bacteria exhibited similarly improved immunity, whatever the bacteria used for the infection. Such maternal protection was costly in the larval development of offspring, but this cost was lower for offspring maternally primed with Gram-positive bacteria. While T. molitor can develop some levels of primed response to Gram-negative bacteria, the priming response to Gram-positive bacteria was more efficient and less costly. We concluded that Gram-positive bacterial pathogens were of paramount importance in the evolution of immune priming in this insect species.

Active migration is associated with specific and consistent changes to gut microbiota in Calidris shorebirds.

Abstract: Gut microbes are increasingly recognised for their role in regulating an animal's metabolism and immunity. However, identifying repeatable associations between host physiological processes and their gut microbiota has proved challenging, in part because microbial communities often respond stochastically to host physiological stress (e.g. fasting, forced exercise or infection). Migratory birds provide a valuable system in which to test host-microbe interactions under physiological extremes because these hosts are adapted to predictable metabolic and immunological challenges as they undergo seasonal migrations, including temporary gut atrophy during long-distance flights. These physiological challenges may either temporarily disrupt gut microbial ecosystems, or, alternatively, promote predictable host-microbe associations during migration. To determine the relationship between migration and gut microbiota, we compared gut microbiota composition between migrating and non-migrating ("resident") conspecific shorebirds sharing a flock. We performed this across two sandpiper species, Calidris ferruginea and Calidris ruficollis, in north-western Australia, and an additional C. ruficollis population 3,000 km away in southern Australia. We found that migrants consistently had higher abundances of the bacterial genus Corynebacterium (average 28% abundance) compared to conspecific residents (average <1% abundance), with this effect holding across both species and sites. However, other than this specific association, community structure and diversity was almost identical between migrants and residents, with migration status accounting for only 1% of gut community variation when excluding Corynebacterium. Our findings suggest a consistent relationship between Corynebacterium and Calidris shorebirds during migration, with further research required to identify causal mechanisms behind the association, and to elucidate functionality to the host. However, outside this specific association, migrating shorebirds broadly maintained gut community structure, which may allow them to quickly recover gut function after a migratory flight. This study provides a rare example of a repeatable and specific response of the gut microbiota to a major physiological challenge across two species and two distant populations.

Review: Allee effects in social species

Abstract: Allee effects have important implications for many aspects of basic and applied ecology. The benefits of aggregation of conspecific individuals are central to Allee effects, which have led to the widely held assumption that social species are more prone to Allee effects. Robust evidence for this assumption, however, remains rare. Furthermore, previous research on Allee effects has failed to adequately address the consequences of the different levels of organisation within social species' populations. Here, we review available evidence of Allee effects and model the role of demographic and behavioural factors that may combine to dampen or strengthen Allee effects in social species. We use examples across various species with contrasting social structure, including carnivores, bats, primates and eusocial insects. Building on this, we provide a conceptual framework that allows for the integration of different Allee effects in social species. Social species are characterised by nested levels of organisation. The benefits of cooperation, measured by mean individual fitness, can be observed at both the population and group levels, giving rise to "population level" and "group level" Allee effects respectively. We also speculate on the possibility of a third level, reporting per capita benefits for different individuals within a group (e.g. castes in social insects). We show that group size heterogeneity and intergroup interactions affect the strength of population-level demographic Allee effects. Populations with higher group size heterogeneity and in which individual social groups cooperate demonstrate the weakest Allee effects and may thus provide an explanation for why extinctions due to Allee effects are rare in social species. More adequately accounting for Allee effects in social species will improve our understanding of the ecological and evolutionary implications of cooperation in social species.

Dynamic, spatial models of parasite transmission in wildlife: Their structure, applications and remaining challenges

Abstract: Individual differences in contact rate can arise from host, group and landscape heterogeneity and can result in different patterns of spatial spread for diseases in wildlife populations with concomitant implications for disease control in wildlife of conservation concern, livestock and humans While dynamic disease models can provide a better understanding of the drivers of spatial spread, the effects of landscape heterogeneity have only been modelled in a few well-studied wildlife systems such as rabies and bovine tuberculosis Such spatial models tend to be either purely theoretical with intrinsic limiting assumptions or individual-based models that are often highly species- and system-specific, limiting the breadth of their utility Our goal was to review studies that have utilized dynamic, spatial models to answer questions about pathogen transmission in wildlife and identify key gaps in the literature We begin by providing an overview of the main types of dynamic, spatial models (eg, metapopulation, network, lattice, cellular automata, individual-based and continuous-space) and their relation to each other We investigate different types of ecological questions that these models have been used to explore: pathogen invasion dynamics and range expansion, spatial heterogeneity and pathogen persistence, the implications of management and intervention strategies and the role of evolution in host-pathogen dynamics We reviewed 168 studies that consider pathogen transmission in free-ranging wildlife and classify them by the model type employed, the focal host-pathogen system, and their overall research themes and motivation We observed a significant focus on mammalian hosts, a few well-studied or purely theoretical pathogen systems, and a lack of studies occurring at the wildlife-public health or wildlife-livestock interfaces Finally, we discuss challenges and future directions in the context of unprecedented human-mediated environmental change Spatial models may provide new insights into understanding, for example, how global warming and habitat disturbance contribute to disease maintenance and emergence Moving forward, better integration of dynamic, spatial disease models with approaches from movement ecology, landscape genetics/genomics and ecoimmunology may provide new avenues for investigation and aid in the control of zoonotic and emerging infectious diseases

Hunger mediates apex predator's risk avoidance response in wildland-urban interface

Abstract: Conflicts between large mammalian predators and humans present a challenge to conservation efforts, as these events drive human attitudes and policies concerning predator species. Unfortunately, generalities portrayed in many empirical carnivore landscape selection studies do not provide an explanation for a predator's occasional use of residential development preceding a carnivore-human conflict event. In some cases, predators may perceive residential development as a risk-reward trade-off. We examine whether state-dependent mortality risk-sensitive foraging can explain an apex carnivore's (Puma concolor) occasional utilization of residential areas. We assess whether puma balance the risk and rewards in a system characterized by a gradient of housing densities ranging from wildland to suburban. Puma GPS location data, characterized as hunting and feeding locations, were used to assess landscape variables governing hunting success and hunting site selection. Hunting site selection behaviour was then analysed conditional on indicators of hunger state. Residential development provided a high energetic reward to puma based on increases in prey availability and hunting success rates associated with increased housing density. Despite a higher energetic reward, hunting site selection analysis indicated that pumas generally avoided residential development, a landscape type attributed with higher puma mortality risk. However, when a puma experienced periods of extended hunger, risk avoidance behaviour towards housing waned. This study demonstrates that an apex carnivore faces a trade-off between acquiring energetic rewards and avoiding risks associated with human housing. Periods of hunger can help explain an apex predator's occasional use of developed landscapes and thus the rare conflicts in the wildland-urban interface. Apex carnivore movement behaviours in relation to human conflicts are best understood as a three-player community-level interaction incorporating wild prey distribution.

Social behaviour and gut microbiota in red-bellied lemurs (Eulemur rubriventer): In search of the role of immunity in the evolution of sociality

Abstract: Vertebrate gut microbiota form a key component of immunity and a dynamic link between an individual and the ecosystem. Microbiota might play a role in social systems as well, because microbes are transmitted during social contact and can affect host behaviour. Combining methods from behavioural and molecular research, we describe the relationship between social dynamics and gut microbiota of a group-living cooperative species of primate, the red-bellied lemur (Eulemur rubriventer). Specifically, we ask whether patterns of social contact (group membership, group size, position in social network, individual sociality) are associated with patterns of gut microbial composition (diversity and similarity) between individuals and across time. Red-bellied lemurs were found to have gut microbiota with slight temporal fluctuations and strong social group-specific composition. Contrary to expectations, individual sociality was negatively associated with gut microbial diversity. However, position within the social network predicted gut microbial composition. These results emphasize the role of the social environment in determining the microbiota of adult animals. Since social transmission of gut microbiota has the potential to enhance immunity, microbiota might have played an escalating role in the evolution of sociality.

Personalities influence spatial responses to environmental fluctuations in wild fish.

Abstract: Although growing evidence supports the idea that animal personality can explain plasticity in response to changes in the social environment, it remains to be tested whether it can explain spatial responses of individuals in the face of natural environmental fluctuations. This is a major challenge in ecology and evolution as spatial dynamics link individual- and population-level processes. In this study, we investigated the potential of individual personalities to predict differences in fish behaviour in the wild. Specifically, our goal was to answer if individual differences in plasticity of space use to sea surface temperature could be explained by differences in personality along the reactive-proactive axis. To address this question, we first conducted repeated standard laboratory assays (i.e., open-field test, novel object test and mirror stimulation test) to assess the personality type of 76 wild-caught Atlantic cod (Gadus morhua). Next, we released the fish back into the sea and monitored their spatial behaviour over large temporal (16 months) and spatial (a whole fjord) scales, using high-resolution acoustic tracking. We demonstrate that (a) cod personality traits are structured into a proactive-reactive syndrome (proactive fish being more bold, exploratory and aggressive), (b) mean depth use of individuals is mainly driven by sea temperature and (c) personality is a significant predictor of home range changes in the wild, where reactive, but not proactive, individuals reduced their home range as sea temperature increased. These findings expand our understanding of the ecological consequences of animal personality and the mechanisms shaping spatial dynamics of animals in nature.

Strategies for managing rival bacterial communities: Lessons from burying beetles.

Abstract: 1.The role of bacteria in animal development, ecology and evolution is increasingly well-understood, yet little is known of how animal behaviour affects bacterial communities. Animals that benefit from defending a key resource from microbial competitors are likely to evolve behaviours to control or manipulate the animal's associated external microbiota. 2.We describe four possible mechanisms by which animals could gain a competitive edge by disrupting a rival bacterial community: ‘weeding’, ‘seeding’, ‘replanting’ and ‘preserving’. By combining detailed behavioural observations with molecular and bioinformatic analyses, we then test which of these mechanisms best explains how burying beetles, Nicrophorus vespilloides, manipulate the bacterial communities on their carcass breeding resource. 3.Burying beetles are a suitable species to study how animals manage external microbiota because reproduction revolves around a small vertebrate carcass. Parents shave a carcass and apply antimicrobial exudates on its surface, shaping it into an edible nest for their offspring. We compared bacterial communities in mice carcasses that were either fresh, prepared by beetles or unprepared but buried underground for the same length of time. We also analysed bacterial communities in the burying beetle's gut, during and after breeding, to understand whether beetles could be ‘seeding’ the carcass with particular microbes. 4.We show that burying beetles do not ‘preserve’ the carcass by reducing bacterial load, as is commonly supposed. Instead, our results suggest they ‘seed’ the carcass with bacterial groups which are part of the Nicrophorus core microbiome. They may also ‘replant’ other bacteria from the carcass gut onto the surface of their carrion nest. Both these processes may lead to the observed increase in bacterial load on the carcass surface in the presence of beetles. Beetles may also ‘weed’ the bacterial community by eliminating some groups of bacteria on the carcass, perhaps through the production of antimicrobials themselves. 5.Whether these alterations to the bacterial community are adaptive from the beetle's perspective, or are simply a by-product of the way in which the beetles prepare the carcass for reproduction, remains to be determined in future work. In general, our work suggests that animals might use more sophisticated techniques for attacking and disrupting rival microbial communities than is currently appreciated. This article is protected by copyright. All rights reserved.

Generalisation and specialisation in hoverfly (Syrphidae) grassland pollen transport networks revealed by DNA metabarcoding.

Abstract: Pollination by insects is a key ecosystem service and important to wider ecosystem function. Most species-level pollination networks studied have a generalised structure, with plants having several potential pollinators, and pollinators in turn visiting a number of different plant species. This is in apparent contrast to a plant's need for efficient conspecific pollen transfer. The aim of this study was to investigate the structure of pollen transport networks at three levels of biological hierarchy: community, species and individual. We did this using hoverflies in the genus Eristalis, a key group of non-Hymenopteran pollinators. We constructed pollen transport networks using DNA metabarcoding to identify pollen. We captured hoverflies in conservation grasslands in west Wales, UK, removed external pollen loads, sequenced the pollen DNA on the Illumina MiSeq platform using the standard plant barcode rbcL, and matched sequences using a pre-existing plant DNA barcode reference library. We found that Eristalis hoverflies transport pollen from 65 plant taxa, more than previously appreciated. Networks were generalised at the site and species level, suggesting some degree of functional redundancy, and were more generalised in late summer compared to early summer. In contrast, pollen transport at the individual level showed some degree of specialisation. Hoverflies defined as "single-plant visitors" varied from 40% of those captured in early summer to 24% in late summer. Individual hoverflies became more generalised in late summer, possibly in response to an increase in floral resources. Rubus fruticosus agg. and Succisa pratensis were key plant species for hoverflies at our sites Our results contribute to resolving the apparent paradox of how generalised pollinator networks can provide efficient pollination to plant species. Generalised hoverfly pollen transport networks may result from a varied range of short-term specialised feeding bouts by individual insects. The generalisation and functional redundancy of Eristalis pollen transport networks may increase the stability of the pollination service they deliver.

Wildlife disease ecology from the individual to the population: Insights from a long-term study of a naturally infected European badger population

Abstract: Long-term individual-based datasets on host-pathogen systems are a rare and valuable resource for understanding the infectious disease dynamics in wildlife. A study of European badgers (Meles meles) naturally infected with bovine tuberculosis (bTB) at Woodchester Park in Gloucestershire (UK) has produced a unique dataset, facilitating investigation of a diverse range of epidemiological and ecological questions with implications for disease management. Since the 1970s, this badger population has been monitored with a systematic mark-recapture regime yielding a dataset of >15,000 captures of >3,000 individuals, providing detailed individual life-history, morphometric, genetic, reproductive and disease data. The annual prevalence of bTB in the Woodchester Park badger population exhibits no straightforward relationship with population density, and both the incidence and prevalence of Mycobacterium bovis show marked variation in space. The study has revealed phenotypic traits that are critical for understanding the social structure of badger populations along with mechanisms vital for understanding disease spread at different spatial resolutions. Woodchester-based studies have provided key insights into how host ecology can influence infection at different spatial and temporal scales. Specifically, it has revealed heterogeneity in epidemiological parameters; intrinsic and extrinsic factors affecting population dynamics; provided insights into senescence and individual life histories; and revealed consistent individual variation in foraging patterns, refuge use and social interactions. An improved understanding of ecological and epidemiological processes is imperative for effective disease management. Woodchester Park research has provided information of direct relevance to bTB management, and a better appreciation of the role of individual heterogeneity in disease transmission can contribute further in this regard. The Woodchester Park study system now offers a rare opportunity to seek a dynamic understanding of how individual-, group- and population-level processes interact. The wealth of existing data makes it possible to take a more integrative approach to examining how the consequences of individual heterogeneity scale to determine population-level pathogen dynamics and help advance our understanding of the ecological drivers of host-pathogen systems.