Linking microbiome temporal dynamics to host ecology in the wild.

Ignoring the dynamic nature of microbial communities risks underestimating the power of microbes to impact the health of their hosts. Microbiomes are thought to be important for host fitness, yet the coarse temporal scale and population-level focus of many studies precludes the ability to investigate the importance of among-individual variation in stability and identify the ecological contexts in which this variation matters. Here we briefly summarise current knowledge of temporal dynamics in wild host-associated microbial communities. We then discuss the implications of among-individual variation in microbiota stability and suggest analytical approaches for understanding these patterns. One major requirement is for future studies to conduct individual-level longitudinal analyses, with some systems already well set up for answering these questions.

Human habitat modification, not apex scavenger decline, drives isotopic niche variation in a carnivore community.

Top carnivores can influence the structure of ecological communities, primarily through competition and predation; however, communities are also influenced by bottom-up forces such as anthropogenic habitat disturbance. Top carnivore declines will likely alter competitive dynamics within and amongst sympatric carnivore species. Increasing intraspecific competition is generally predicted to drive niche expansion and/or individual specialisation, while interspecific competition tends to constrain niches. Using stable isotope analysis of whiskers, we studied the effects of Tasmanian devil Sarcophilus harrisii declines upon the population- and individual-level isotopic niches of Tasmanian devils and sympatric spotted-tailed quolls Dasyurus maculatus subsp. maculatus. We investigated whether time since the onset of devil decline (a proxy for severity of decline) and landscape characteristics affected the isotopic niche breadth and overlap of devil and quoll populations. We quantified individual isotopic niche breadth for a subset of Tasmanian devils and spotted-tailed quolls and assessed whether between-site population niche variation was driven by individual-level specialisation. Tasmanian devils and spotted-tailed quolls demonstrated smaller population-level isotopic niche breadths with increasing human-modified habitat, while time since the onset of devil decline had no effect on population-level niche breadth or interspecific niche overlap. Individual isotopic niche breadths of Tasmanian devils and spotted-tailed quolls were narrower in human-modified landscapes, likely driving population isotopic niche contraction, however, the degree of individuals' specialisation relative to one another remained constant. Our results suggest that across varied landscapes, mammalian carnivore niches can be more sensitive to the bottom-up forces of anthropogenic habitat disturbance than to the top-down effects of top carnivore decline.

Individuals departing non-breeding areas early achieve earlier breeding and higher breeding success.

Conditions experienced by an individual during migration have the potential to shape migratory tactic and in turn fitness. For large birds, environmental conditions encountered during migration have been linked with survival and subsequent reproductive output, but this is less known for smaller birds, hindering our understanding of mechanisms driving population change. By combining breeding and tracking data from 62 pied flycatchers (Ficedula hypoleuca) representing two breeding populations collected over 2016-2020, we determine how variation in migration phenology and tactic among individuals affects subsequent breeding. Departure date from West African non-breeding areas to European breeding grounds was highly variable among individuals and had a strong influence on migration tactic. Early departing individuals had longer spring migrations which included longer staging duration yet arrived at breeding sites and initiated breeding earlier than later departing individuals. Individuals with longer duration spring migrations and early arrival at breeding sites had larger clutches, and for males higher fledging success. We suggest that for pied flycatchers, individual carry-over effects may act through departure phenology from West Africa, and the associated spring migration duration, to influence reproduction. While our results confirm that departure date from non-breeding areas can be associated with breeding success in migratory passerines, we identify spring staging duration as a key component of this process.

The influence of diet on gut microbiome and body mass dynamics in a capital-breeding migratory bird.

Gut-associated microbial communities are known to play a vital role in the health and fitness of their hosts. Though studies investigating the factors associated with among-individual variation in microbiome structure in wild animal species are increasing, knowledge of this variation at the individual level is scarce, despite the clear link between microbiome and nutritional status uncovered in humans and model organisms. Here, we combine detailed observational data on life history and foraging preference with 16S rRNA profiling of the faecal microbiome to investigate the relationship between diet, microbiome stability and rates of body mass gain in a migratory capital-breeding bird, the light-bellied Brent goose (Branta bernicla hrota). Our findings suggest that generalist feeders have microbiomes that are intermediate in diversity and composition between two foraging specialisms, and also show higher within-individual plasticity. We also suggest a link between foraging phenotype and the rates of mass gain during the spring staging of a capital breeder. This study offers rare insight into individual-level temporal dynamics of the gut microbiome of a wild host. Further work is needed to uncover the functional link between individual dietary choices, gut microbiome structure and stability, and the implications this has for the reproductive success of this capital breeder.

Differing drivers of decline within a migratory metapopulation has implications for future conservation.

Researchers generally ascribe demographic drivers in a single sub-population and presume they are representative. With this information, practitioners implement blanket conservation measures across metapopulations to reverse declines. However, such approaches may not be appropriate in circumstances where sub-populations are spatiotemporally segregated and exposed to different environmental variation. The Greenland White-fronted Goose, Anser albifrons flavirostris, is an Arctic-nesting migrant that largely comprises two sub-populations (delineated by northerly and southerly breeding areas in west Greenland). The metapopulation has declined since 1999 but this trend is only mirrored in one sub-population and the causes of this disparity are unclear. Here we compare the drivers and trends of productivity in both sub-populations using population- and individual-level analysis. We examined how temperature and precipitation influenced population-level reproductive success over 37 years and whether there was a change in the relationship when metapopulation decline commenced. In addition, we used biologging devices to remotely classify incubation events for 86 bird-years and modelled how phenology and environmental conditions influenced individual-level nest survival. Correlations between reproductive success and temperature/precipitation on the breeding grounds have weakened for both sub-populations. This has resulted in lower reproductive success for the northerly, but not southerly breeding sub-population, which at the individual-level appears to be driven by lower nest survival. Earlier breeding ground arrival and less precipitation during incubation increased nest survival in the northerly breeding population, while no factors examined were important for the southerly breeding sub-population. This suggests reproductive success is driven by different factor(s) in the two sub-populations. Demographic rates and their environmental drivers differ between the sub-populations examined here and consequently we encourage further decomposition of demography within metapopulations. This is important for conservation practitioners to consider as bespoke conservation strategies, targeting different limiting factors, may be required for different sub-populations.

Demographic rates reveal the benefits of protected areas in a long-lived migratory bird.

Recent studies have suggested that protected areas often fail to conserve target species. However, the efficacy of terrestrial protected areas is difficult to measure, especially for highly vagile species like migratory birds that may move between protected and unprotected areas throughout their lives. Here, we use a 30-y dataset of detailed demographic data from a migratory waterbird, the Whooper swan (Cygnus cygnus), to assess the value of nature reserves (NRs). We assess how demographic rates vary at sites with varying levels of protection and how they are influenced by movements between sites. Swans had a lower breeding probability when wintering inside NRs than outside but better survival for all age classes, generating a 30-fold higher annual growth rate within NRs. There was also a net movement of individuals from NRs to non-NRs. By combining these demographic rates and estimates of movement (into and out of NRs) into population projection models, we show that the NRs should help to double the population of swans wintering in the United Kingdom by 2030. These results highlight the major effect that spatial management can have on species conservation, even when the areas protected are relatively small and only used during short periods of the life cycle.

Geolocator-tracking seabird migration and moult reveal large-scale, temperature-driven isoscapes in the NE Atlantic.

RATIONALE: By combining precision satellite-tracking with blood sampling, seabirds can be used to validate marine carbon and nitrogen isoscapes, but it is unclear whether a comparable approach using low-precision light-level geolocators (GLS) and feather sampling can be similarly effective. METHODS: Here we used GLS to identify wintering areas of northern gannets (Morus bassanus) and sampled winter grown feathers (confirmed from image analysis of non-breeding birds) to test for spatial gradients in δ13 C and δ15 N in the NE Atlantic. RESULTS: By matching winter-grown feathers with the non-breeding location of tracked birds we found latitudinal gradients in δ13 C and δ15 N in neritic waters. Moreover, isotopic patterns were best explained by sea surface temperature. Similar isotope gradients were found in fish muscle sampled at local ports. CONCLUSIONS: Our study reveals the potential of using seabird GLS and feathers to reconstruct large-scale isotopic patterns.

Time-varying effects of local weather on behavior and probability of breeding deferral in two Arctic-nesting goose populations.

Arctic-nesting geese face energetic challenges during spring migration, including ecological barriers and weather conditions (e.g., precipitation and temperature), which in long-lived species can lead to a trade-off to defer reproduction in favor of greater survival. We used GPS location and acceleration data collected from 35 greater white-fronted geese of the North American midcontinent and Greenland populations at spring migration stopovers, and novel applications of Bayesian dynamic linear models to test daily effects of minimum temperature and precipitation on energy expenditure (i.e., overall dynamic body acceleration, ODBA) and proportion of time spent feeding (PTF), then examined the daily and additive importance of ODBA and PTF on probability of breeding deferral using stochastic antecedent models. We expected distinct responses in behavior and probability of breeding deferral between and within populations due to differences in stopover area availability. Time-varying coefficients of weather conditions were variable between ODBA and PTF, and often did not show consistent patterns among birds, indicating plasticity in how individuals respond to conditions. An increase in antecedent ODBA was associated with a slightly increased probability of deferral in midcontinent geese but not Greenland geese. Probability of deferral decreased with increased PTF in both populations. We did not detect any differentially important time periods. These results suggest either that movements and behavior throughout spring migration do not explain breeding deferral or that ecological linkages between bird decisions during spring and subsequent breeding deferral were different between populations and across migration but occurred at different time scales than those we examined.

What has biotelemetry ever done for avian translocations?

Species translocation is a popular approach in contemporary ecological restoration and rewilding. Improving the efficacy of conservation translocation programmes requires a combination of robust data from comparable populations, population viability modelling and post-release monitoring. Biotelemetry is becoming an ever more accessible means to collect some of the high-resolution information on the ecology and behaviour of founding populations that such evaluations require. Here, we review 81 published case studies to consider how this capability could increase the success of avian translocations. We found that 67 translocations favoured traditional radio telemetry, with surveillance focussing mostly on immediate post-release dispersal, survival and breeding attempts. Just 28 projects tracked founder individuals for longer than 1 year and no studies referenced pre-release sampling or planning using biotelemetry. While our review shows that tracking devices have been deployed extensively in translocation projects, its application has been mostly limited to short-term spatial and demographic monitoring. We conclude that biotelemetry is a powerful tool for harnessing a multitude of lifetime eco-behavioural data which can be used to build valuable predictive models and surveillance programmes, but this capability has yet to be fully realised by researchers in avian translocations.

Variation in movement strategies: Capital versus income migration.

Animal migrations represent the regular movements of trillions of individuals. The scale of these movements has inspired human intrigue for millennia and has been intensively studied by biologists. This research has highlighted the diversity of migratory strategies seen across and within migratory taxa: while some migrants temporarily express phenotypes dedicated to travel, others show little or no phenotypic flexibility in association with migration. However, a vocabulary for describing these contrasting solutions to the performance trade-offs inherent to the highly dynamic lifestyle of migrants (and strategies intermediate between these two extremes) is currently missing. We propose a taxon-independent organising framework based on energetics, distinguishing between migrants that forage as they travel (income migrants) and those that fuel migration using energy acquired before departure (capital migrants). Not only does our capital:income continuum of migratory energetics account for the variable extent of phenotypic flexibility within and across migrant populations, but it also aligns with theoreticians' treatment of migration and clarifies how migration impacts other phases of the life cycle. As such, it provides a unifying scale and common vacabulary for comparing the migratory strategies of divergent taxa.

Associations between abundances of free-roaming gamebirds and common buzzards Buteo buteo are not driven by consumption of gamebirds in the buzzard breeding season.

Releasing gamebirds in large numbers for sport shooting may directly or indirectly influence the abundance, distribution and population dynamics of native wildlife. The abundances of generalist predators have been positively associated with the abundance of gamebirds. These relationships have implications for prey populations, with the potential for indirect impacts of gamebird releases on wider biodiversity. To understand the basis of these associations, we investigated variation in territory size, prey provisioning to chicks, and breeding success of common buzzards Buteo buteo, and associations with variation in the abundances of free-roaming gamebirds, primarily pheasants Phasianus colchicus, and of rabbits Oryctolagus cuniculus and field voles Microtus agrestis, as important prey for buzzards. The relative abundance of gamebirds, but not those of rabbits or voles, was weakly but positively correlated with our index of buzzard territory size. Gamebirds were rarely brought to the nest. Rabbits and voles, and not gamebirds, were provisioned to chicks in proportion to their relative abundance. The number of buzzard chicks increased with provisioning rates of rabbits, in terms of both provisioning frequency and biomass, but not with provisioning rates for gamebirds or voles. Associations between the abundances of buzzards and gamebirds may not be a consequence of the greater availability of gamebirds as prey during the buzzard breeding season. Instead, the association may arise either from habitat or predator management leading to higher densities of alternative prey (in this instance, rabbits), or from greater availability of gamebirds as prey or carrion during the autumn and winter shooting season. The interactions between gamebird releases and associated practices of predator control and shooting itself require better understanding to more effectively intervene in any one aspect of this complex social-ecological system.

Spatial and sex differences in mercury contamination of skuas in the Southern Ocean.

Antarctic marine ecosystems are often considered to be pristine environments, yet wildlife in the polar regions may still be exposed to high levels of environmental contaminants. Here, we measured total mercury (THg) concentrations in blood samples from adult brown skuas Stercorarius antarcticus lonnbergi (n = 82) from three breeding colonies south of the Antarctic Polar Front in the Southern Ocean (southwest Atlantic region): (i) Bahía Esperanza/Hope Bay, Antarctic Peninsula; (ii) Signy Island, South Orkney Islands; and, (iii) Bird Island, South Georgia. Blood THg concentrations increased from the Antarctic Peninsula towards the Antarctic Polar Front, such that Hg contamination was lowest at Bahía Esperanza/Hope Bay (mean ± SD, 0.95 ± 0.45 µg g-1 dw), intermediate at Signy Island (3.42 ± 2.29 µg g-1 dw) and highest at Bird Island (4.47 ± 1.10 µg g-1 dw). Blood THg concentrations also showed a weak positive correlation with δ15N values, likely reflecting the biomagnification process. Males had higher Hg burdens than females, which may reflect deposition of Hg into eggs by females or potentially differences in their trophic ecology. These data provide important insights into intraspecific variation in contamination and the geographic transfer of Hg to seabirds in the Southern Ocean.

GPS tracking reveals landfill closures induce higher foraging effort and habitat switching in gulls.

BACKGROUND: Landfills are a major subsidy for some animals, with implications for their life history and demography. Gulls feed extensively on food from landfills and closures are expected to have ecological consequences, but how this influences movement ecology is virtually unknown. METHODS: We used GPS-tracking to quantify foraging behaviour and habitat choice of lesser black-backed gulls (Larus fuscus) breeding at two colonies before and after closure of two nearby landfills. RESULTS: Following closure, gulls from both colonies travelled further and for longer to forage. Gulls also changed habitat selection, although this differed by colony - birds from one colony shifted to agricultural habitats, while at the other, increased their use of urban areas. These behavioural responses had no effect on adult body condition but hint at potential direct effects of higher foraging costs and indirect impacts by shifting to new habitats. CONCLUSIONS: Our results demonstrate how landfill availability influences gull foraging movements and habitat selection. We also emphasize the value of biologging to detect rapid behavioural responses in contrast to more conventional demographic approaches, which is especially important for animals that spend the majority of their lives away from direct observation.

Trophic relationships between the crab Libinia ferreirae and its symbionts.

Symbioses are ubiquitous in the animal kingdom. However, in most cases, the role of each member is relatively fixed, and it is rare for the same species to exhibit different symbiotic behaviours throughout its ontogeny. Here, we use stable isotope analyses of food resources to identify the relationships between the spider crab Libinia ferreirae as a symbiont of its jellyfish host during juvenile life stages and as a host for sea anemone epibionts on its carapace as an adult. We ask the following questions: How do the food sources used by the crab change between its juvenile and adult phase? How does the symbiotic relationship change when the crab develops from a juvenile into an adult? We were particularly interested in the extent to which L. ferreirae juveniles feed on jellyfish hosts versus planktonic prey during the juvenile symbiont phase and how adults feed on their epibionts during the free-living phase. δ13C of L. ferreirae differed between juvenile (associated with the jellyfish) and adult stages (free-living), unsurprisingly suggesting that there is little isotopic niche overlap between these life phases. SIMMr models using δ13C and δ15N of the crab and its potential food sources indicated that the juvenile crab symbionts did not derive any significant nutrition from medusae and relied predominantly on zooplankton prey. Since juvenile crabs do not have structures to capture zooplankton for feeding, we suggest that they may be kleptoparasites, stealing zooplankton food from their host, though further work is needed to identify the form that such a symbiosis might take. The nutrition of free-living crabs was predominantly derived from benthic algae and shrimps rather than from epibionts. These epibionts appear to use similar food resources as the host, suggesting a symbiotic relationship more akin to mutualism. Thus, the crabs move from a symbiosis in which they may act as parasites to one where they act as hosts. Such flexible approaches to symbioses may be more common than currently described, particularly in species with different functional roles during individual life stages.

Isotopic niche variation in Tasmanian devils Sarcophilus harrisii with progression of devil facial tumor disease.

Devil facial tumor disease (DFTD) is a transmissible cancer affecting Tasmanian devils Sarcophilus harrisii. The disease has caused severe population declines and is associated with demographic and behavioral changes, including earlier breeding, younger age structures, and reduced dispersal and social interactions. Devils are generally solitary, but social encounters are commonplace when feeding upon large carcasses. DFTD tumors can disfigure the jaw and mouth and so diseased individuals might alter their diets to enable ingestion of alternative foods, to avoid conspecific interactions, or to reduce competition. Using stable isotope analysis (δ13C and δ15N) of whiskers, we tested whether DFTD progression, measured as tumor volume, affected the isotope ratios and isotopic niches of 94 infected Tasmanian devils from six sites in Tasmania, comprising four eucalypt plantations, an area of smallholdings and a national park. Then, using tissue from 10 devils sampled before and after detection of tumors and 8 devils where no tumors were detected, we examined whether mean and standard deviation of δ13C and δ15N of the same individuals changed between healthy and diseased states. δ13C and δ15N values were generally not related to tumor volume in infected devils, though at one site, Freycinet National Park, δ15N values increased significantly as tumor volume increased. Infection with DFTD was not associated with significant changes in the mean or standard deviation of δ13C and δ15N values in individual devils sampled before and after detection of tumors. Our analysis suggests that devils tend to maintain their isotopic niche in the face of DFTD infection and progression, except where ecological conditions facilitate a shift in diets and feeding behaviors, demonstrating that ecological context, alongside disease severity, can modulate the behavioral responses of Tasmanian devils to DFTD.

A deepening understanding of animal culture suggests lessons for conservation.

A key goal of conservation is to protect biodiversity by supporting the long-term persistence of viable, natural populations of wild species. Conservation practice has long been guided by genetic, ecological and demographic indicators of risk. Emerging evidence of animal culture across diverse taxa and its role as a driver of evolutionary diversification, population structure and demographic processes may be essential for augmenting these conventional conservation approaches and decision-making. Animal culture was the focus of a ground-breaking resolution under the Convention on the Conservation of Migratory Species of Wild Animals (CMS), an international treaty operating under the UN Environment Programme. Here, we synthesize existing evidence to demonstrate how social learning and animal culture interact with processes important to conservation management. Specifically, we explore how social learning might influence population viability and be an important resource in response to anthropogenic change, and provide examples of how it can result in phenotypically distinct units with different, socially learnt behavioural strategies. While identifying culture and social learning can be challenging, indirect identification and parsimonious inferences may be informative. Finally, we identify relevant methodologies and provide a framework for viewing behavioural data through a cultural lens which might provide new insights for conservation management.

Mercury exposure in an endangered seabird: long-term changes and relationships with trophic ecology and breeding success.

Mercury (Hg) is an environmental contaminant which, at high concentrations, can negatively influence avian physiology and demography. Albatrosses (Diomedeidae) have higher Hg burdens than all other avian families. Here, we measure total Hg (THg) concentrations of body feathers from adult grey-headed albatrosses (Thalassarche chrysostoma) at South Georgia. Specifically, we (i) analyse temporal trends at South Georgia (1989-2013) and make comparisons with other breeding populations; (ii) identify factors driving variation in THg concentrations and (iii) examine relationships with breeding success. Mean ± s.d. feather THg concentrations were 13.0 ± 8.0 µg g-1 dw, which represents a threefold increase over the past 25 years at South Georgia and is the highest recorded in the Thalassarche genus. Foraging habitat, inferred from stable isotope ratios of carbon (δ13C), significantly influenced THg concentrations-feathers moulted in Antarctic waters had far lower THg concentrations than those moulted in subantarctic or subtropical waters. THg concentrations also increased with trophic level (δ15N), reflecting the biomagnification process. There was limited support for the influence of sex, age and previous breeding outcome on feather THg concentrations. However, in males, Hg exposure was correlated with breeding outcome-failed birds had significantly higher feather THg concentrations than successful birds. These results provide key insights into the drivers and consequences of Hg exposure in this globally important albatross population.

Migrant birds and mammals live faster than residents.

Billions of vertebrates migrate to and from their breeding grounds annually, exhibiting astonishing feats of endurance. Many such movements are energetically costly yet there is little consensus on whether or how such costs might influence schedules of survival and reproduction in migratory animals. Here we provide a global analysis of associations between migratory behaviour and vertebrate life histories. After controlling for latitudinal and evolutionary patterns, we find that migratory birds and mammals have faster paces of life than their non-migratory relatives. Among swimming and walking species, migrants tend to have larger body size, while among flying species, migrants are smaller. We discuss whether pace of life is a determinant, consequence, or adaptive outcome, of migration. Our findings have important implications for the understanding of the migratory phenomenon and will help predict the responses of bird and mammal species to environmental change.

Age-related variation in the trophic characteristics of a marsupial carnivore, the Tasmanian devil Sarcophilus harrisii.

Age-related changes in diet have implications for competitive interactions and for predator-prey dynamics, affecting individuals and groups at different life stages. To quantify patterns of variation and ontogenetic change in the diets of Tasmanian devils Sarcophilus harrisii, a threatened marsupial carnivore, we analyzed variation in the stable isotope composition of whisker tissue samples taken from 91 individual devils from Wilmot, Tasmania from December 2014 to February 2017. Both δ13C and δ15N decreased with increasing age in weaned Tasmanian devils, indicating that as they age devils rely less on small mammals and birds, and more on large herbivores. Devils <12 months old had broader group isotopic niches, as estimated by Bayesian standard ellipses (SEAB mode = 1.042) than devils from 12 to 23 months old (mode = 0.541) and devils ≥24 months old (mode = 0.532). Devils <24 months old had broader individual isotopic niches (SEAB mode range 0.492-1.083) than devils ≥24 months old (mode range 0.092-0.240). A decrease in δ15N from the older whisker sections to the more recently grown sections in devils <24 months old likely reflects the period of weaning in this species, as this pattern was not observed in devils ≥24 months old. Our data reveal changes in the isotopic composition of devil whiskers with increasing age, accompanied by a reduction in isotopic variation both among population age classes and within individuals, reflecting the effect of weaning in early life, and a likely shift from an initially diverse diet of small mammals, birds, and invertebrates towards increasing consumption of larger herbivores in adulthood.