Reframing wildlife disease management problems with decision analysis.

Contemporary wildlife disease management is complex because managers need to respond to a wide range of stakeholders, multiple uncertainties, and difficult trade-offs that characterize the interconnected challenges of today. Despite general acknowledgment of these complexities, managing wildlife disease tends to be framed as a scientific problem, in which the major challenge is lack of knowledge. The complex and multifactorial process of decision-making is collapsed into a scientific endeavor to reduce uncertainty. As a result, contemporary decision-making may be oversimplified, rely on simple heuristics, and fail to account for the broader legal, social, and economic context in which the decisions are made. Concurrently, scientific research on wildlife disease may be distant from this decision context, resulting in information that may not be directly relevant to the pertinent management questions. We propose reframing wildlife disease management challenges as decision problems and addressing them with decision analytical tools to divide the complex problems into more cognitively manageable elements. In particular, structured decision-making has the potential to improve the quality, rigor, and transparency of decisions about wildlife disease in a variety of systems. Examples of management of severe acute respiratory syndrome coronavirus 2, white-nose syndrome, avian influenza, and chytridiomycosis illustrate the most common impediments to decision-making, including competing objectives, risks, prediction uncertainty, and limited resources.

Replanteamiento del manejo de problemas por enfermedades de fauna mediante el análisis de decisiones Resumen El manejo actual de las enfermedades de la fauna es complejo debido a que los gestores necesitan responder a una amplia gama de actores, varias incertidumbres y compensaciones difíciles que caracterizan los retos interconectados del día de hoy. A pesar de que en general se reconocen estas complejidades, el manejo de las enfermedades tiende a plantearse como un problema científico en el que el principal obstáculo es la falta de conocimiento. El proceso complejo y multifactorial de la toma decisiones está colapsado dentro de un esfuerzo científico para reducir la incertidumbre. Como resultado de esto, las decisiones contemporáneas pueden estar simplificadas en exceso, depender de métodos heurísticos simples y no considerar el contexto legal, social y económico más amplio en el que se toman las decisiones. De manera paralela, las investigaciones científicas sobre las enfermedades de la fauna pueden estar lejos de este contexto de decisiones, lo que deriva en información que puede no ser directamente relevante para las preguntas pertinentes de manejo. Proponemos replantear los obstáculos para el manejo de enfermedades de fauna como problemas de decisión y abordarlos con herramientas analíticas de decisión para dividir los problemas complejos en elementos más manejables de manera cognitiva. En particular, las decisiones estructuradas tienen el potencial de mejorar la calidad, el rigor y la transparencia de las decisiones sobre las enfermedades de la fauna en una variedad de sistemas. Ejemplos como el manejo del coronavirus del síndrome de respiración agudo tipo 2, el síndrome de nariz blanca, la influenza aviar y la quitridiomicosis ilustran los impedimentos más comunes para la toma de decisiones, incluyendo los objetivos en competencia, riesgos, incertidumbre en las predicciones y recursos limitados.

Habitat Specialization by Wildlife Reduces Pathogen Spread in Urbanizing Landscapes.

AbstractUrban areas are expanding globally with far-reaching ecological consequences, including for wildlife-pathogen interactions. Wildlife show tremendous variation in their responses to urbanization; even within a single population, some individuals can specialize on urban or natural habitat types. This specialization could alter pathogen impacts on host populations via changes to wildlife movement and aggregation. Here, we build a mechanistic model to explore how habitat specialization in urban landscapes affects interactions between a mobile host population and a density-dependent specialist pathogen that confers no immunity. We model movement on a network of resource-stable urban sites and resource-fluctuating natural sites, where hosts are urban specialists, natural specialists, or generalists that use both patch types. We find that for generalists, natural and partially urban landscapes produce the highest infection prevalence and mortality, driven by high movement rates at natural sites and high densities at urban sites. However, habitat specialization protects hosts from these negative effects of partially urban landscapes by limiting movement between patch types. These findings suggest that habitat specialization can benefit populations by reducing infectious disease transmission, but by reducing movement between habitat types it could also carry the cost of reducing other movement-related ecosystem functions, such as seed dispersal and pollination.

Avian influenza antibody prevalence increases with mercury contamination in wild waterfowl.

Environmental contamination is widespread and can negatively impact wildlife health. Some contaminants, including heavy metals, have immunosuppressive effects, but prior studies have rarely measured contamination and disease simultaneously, which limits our understanding of how contaminants and pathogens interact to influence wildlife health. Here, we measured mercury concentrations, influenza infection, influenza antibodies and body condition in 749 individuals from 11 species of wild ducks overwintering in California. We found that the odds of prior influenza infection increased more than fivefold across the observed range of blood mercury concentrations, while accounting for species, age, sex and date. Influenza infection prevalence was also higher in species with higher average mercury concentrations. We detected no relationship between influenza infection and body fat content. This positive relationship between influenza prevalence and mercury concentrations in migratory waterfowl suggests that immunotoxic effects of mercury contamination could promote the spread of avian influenza along migratory flyways, especially if influenza has minimal effects on bird health and mobility. More generally, these results show that the effects of environmental contamination could extend beyond the geographical area of contamination itself by altering the prevalence of infectious diseases in highly mobile hosts.

Movement rules determine nomadic species' responses to resource supplementation and degradation.

In environments that vary unpredictably, many animals are nomadic, moving in an irregular pattern that differs from year to year. Exploring the mechanisms of nomadic movement is needed to understand how animals survive in highly variable environments, and to predict behavioural and population responses to environmental change. We developed a network model to identify plausible mechanisms of nomadic animal movement by comparing the performance of multiple movement rules along a continuum from nomadism to residency. Using simulations and analytical results, we explored how different types of habitat modifications (that augment or decrease resource availability) might affect the abundance and movement rates of animals following each of these rules. Movement rules for which departure from patches depended on resource availability and/or competition performed almost equally well and better than residency or uninformed movement under most conditions, even though animals using each rule moved at substantially different rates. Habitat modifications that stabilized resources, either by resource supplementation or degradation, eroded the benefits of informed nomadic movements, particularly for movements based on resource availability alone. These results suggest that simple movement rules can explain nomadic animal movements and determine species' responses to environmental change. In particular, landscape stabilization and supplementation might be useful strategies for promoting populations of resident animals, but would be less beneficial for managing highly mobile species, many of which are threatened by habitat disruption and changes in climate.

On the relationship between body condition and parasite infection in wildlife: a review and meta-analysis.

Body condition metrics are widely used to infer animal health and to assess costs of parasite infection. Since parasites harm their hosts, ecologists might expect negative relationships between infection and condition in wildlife, but this assumption is challenged by studies showing positive or null condition-infection relationships. Here, we outline common condition metrics used by ecologists in studies of parasitism, and consider mechanisms that cause negative, positive, and null condition-infection relationships in wildlife systems. We then perform a meta-analysis of 553 condition-infection relationships from 187 peer-reviewed studies of animal hosts, analysing observational and experimental records separately, and noting whether authors measured binary infection status or intensity. Our analysis finds substantial heterogeneity in the strength and direction of condition-infection relationships, a small, negative average effect size that is stronger in experimental studies, and evidence for publication bias towards negative relationships. The strongest predictors of variation in study outcomes are host thermoregulation and the methods used to evaluate body condition. We recommend that studies aiming to assess parasite impacts on body condition should consider host-parasite biology, choose condition measures that can change during the course of infection, and employ longitudinal surveys or manipulate infection status when feasible.

Migratory behaviour predicts greater parasite diversity in ungulates.

Long-distance animal movements can increase exposure to diverse parasites, but can also reduce infection risk through escape from contaminated habitats or culling of infected individuals. These mechanisms have been demonstrated within and between populations in single-host/single-parasite interactions, but how long-distance movement behaviours shape parasite diversity and prevalence across host taxa is largely unknown. Using a comparative approach, we analyse the parasite communities of 93 migratory, nomadic and resident ungulate species. We find that migrants have higher parasite species richness than residents or nomads, even after considering other factors known to influence parasite diversity, such as body size and host geographical range area. Further analyses support a novel 'environmental tracking' hypothesis, whereby migration allows parasites to experience environments favourable to transmission year-round. In addition, the social aggregation and large group sizes that facilitate migration might increase infection risk for migrants. By contrast, we find little support for previously proposed hypotheses, including migratory escape and culling, in explaining the relationship between host movement and parasitism in mammals at this cross-species scale. Our findings, which support mechanistic links between long-distance movement and increased parasite richness at the species level, could help predict the effects of future environmental change on parasitism in migratory animals.

How far to go? Determinants of migration distance in land mammals.

Animal migration is a global phenomenon, but few studies have examined the substantial within- and between-species variation in migration distances. We built a global database of 94 land migrations of large mammalian herbivore populations ranging from 10 to 1638 km. We examined how resource availability, spatial scale of resource variability and body size affect migration distance among populations. Resource availability measured as normalised difference vegetation index had a strong negative effect, predicting a tenfold difference in migration distances between low- and high-resource areas and explaining 23% of the variation in migration distances. We found a weak, positive effect of the spatial scale of resource variability but no effect of body size. Resource-poor environments are known to increase the size of mammalian home ranges and territories. Here, we demonstrate that for migratory populations as well, animals living in resource-poor environments travel farther to fulfil their resource needs.

North American wintering mallards infected with highly pathogenic avian influenza show few signs of altered local or migratory movements.

Avian influenza viruses pose a threat to wildlife and livestock health. The emergence of highly pathogenic avian influenza (HPAI) in wild birds and poultry in North America in late 2021 was the first such outbreak since 2015 and the largest outbreak in North America to date. Despite its prominence and economic impacts, we know relatively little about how HPAI spreads in wild bird populations. In January 2022, we captured 43 mallards (Anas platyrhynchos) in Tennessee, USA, 11 of which were actively infected with HPAI. These were the first confirmed detections of HPAI H5N1 clade 2.3.4.4b in the Mississippi Flyway. We compared movement patterns of infected and uninfected birds and found no clear differences; infected birds moved just as much during winter, migrated slightly earlier, and migrated similar distances as uninfected birds. Infected mallards also contacted and shared space with uninfected birds while on their wintering grounds, suggesting ongoing transmission of the virus. We found no differences in body condition or survival rates between infected and uninfected birds. Together, these results show that HPAI H5N1 clade 2.3.4.4b infection was unrelated to body condition or movement behavior in mallards infected at this location during winter; if these results are confirmed in other seasons and as HPAI H5N1 continues to evolve, they suggest that these birds could contribute to the maintenance and dispersal of HPAI in North America. Further research on more species across larger geographic areas and multiple seasons would help clarify potential impacts of HPAI on waterfowl and how this emerging disease spreads at continental scales, across species, and potentially between wildlife and domestic animals.

Ontogenetic shifts from social to experiential learning drive avian migration timing.

Migrating animals may benefit from social or experiential learning, yet whether and how these learning processes interact or change over time to produce observed migration patterns remains unexplored. Using 16 years of satellite-tracking data from 105 reintroduced whooping cranes, we reveal an interplay between social and experiential learning in migration timing. Both processes dramatically improved individuals' abilities to dynamically adjust their timing to track environmental conditions along the migration path. However, results revealed an ontogenetic shift in the dominant learning process, whereby subadult birds relied on social information, while mature birds primarily relied on experiential information. These results indicate that the adjustment of migration phenology in response to the environment is a learned skill that depends on both social context and individual age. Assessing how animals successfully learn to time migrations as environmental conditions change is critical for understanding intraspecific differences in migration patterns and for anticipating responses to global change.

Urban specialization reduces habitat connectivity by a highly mobile wading bird.

BACKGROUND: Mobile animals transport nutrients and propagules across habitats, and are crucial for the functioning of food webs and for ecosystem services. Human activities such as urbanization can alter animal movement behavior, including site fidelity and resource use. Because many urban areas are adjacent to natural sites, mobile animals might connect natural and urban habitats. More generally, understanding animal movement patterns in urban areas can help predict how urban expansion will affect the roles of highly mobile animals in ecological processes. METHODS: Here, we examined movements by a seasonally nomadic wading bird, the American white ibis (Eudocimus albus), in South Florida, USA. White ibis are colonial wading birds that forage on aquatic prey; in recent years, some ibis have shifted their behavior to forage in urban parks, where they are fed by people. We used a spatial network approach to investigate how individual movement patterns influence connectivity between urban and non-urban sites. We built a network of habitat connectivity using GPS tracking data from ibis during their non-breeding season and compared this network to simulated networks that assumed individuals moved indiscriminately with respect to habitat type. RESULTS: We found that the observed network was less connected than the simulated networks, that urban-urban and natural-natural connections were strong, and that individuals using urban sites had the least-variable habitat use. Importantly, the few ibis that used both urban and natural habitats contributed the most to connectivity. CONCLUSIONS: Habitat specialization in urban-acclimated wildlife could reduce the exchange of propagules and nutrients between urban and natural areas, which has consequences both for beneficial effects of connectivity such as gene flow and for detrimental effects such as the spread of contaminants or pathogens.

Beyond Migration: Causes and Consequences of Nomadic Animal Movements.

Recent advances in animal tracking reveal that many species display irregular movements that do not fall into classical categories of movement patterns such as range residency or migration. Here, we develop a unifying framework that distinguishes these nomadic movements based on their patterns, drivers, and mechanisms. Though they occur in diverse taxa and geographic regions, nomadic movements are united by both their underlying environmental drivers, mainly environmental stochasticity, and the resulting irregular, far-ranging movement patterns. The framework further classifies types of nomadic movements, including full, seasonal, phase, irruptive, and partial nomadism. Nomadic movements can have unique effects on populations, communities, and ecosystems, most notably providing intermittent disturbances and novel introductions of propagules.

Multiscale model of regional population decline in little brown bats due to white-nose syndrome.

The introduced fungal pathogen Pseudogymnoascus destructans is causing decline of several species of bats in North America, with some even at risk of extinction or extirpation. The severity of the epidemic of white-nose syndrome caused by P. destructans has prompted investigation of the transmission and virulence of infection at multiple scales, but linking these scales is necessary to quantify the mechanisms of transmission and assess population-scale declines.We built a model connecting within-hibernaculum disease dynamics of little brown bats to regional-scale dispersal, reproduction, and disease spread, including multiple plausible mechanisms of transmission.We parameterized the model using the approach of plausible parameter sets, by comparing stochastic simulation results to statistical probes from empirical data on within-hibernaculum prevalence and survival, as well as among-hibernacula spread across a region.Our results are consistent with frequency-dependent transmission between bats, support an important role of environmental transmission, and show very little effect of dispersal among colonies on metapopulation survival.The results help identify the influential parameters and largest sources of uncertainty. The model also offers a generalizable method to assess hypotheses about hibernaculum-to-hibernaculum transmission and to identify gaps in knowledge about key processes, and could be expanded to include additional mechanisms or bat species.

Assessing the contributions of intraspecific and environmental sources of infection in urban wildlife: Salmonella enterica and white ibis as a case study.

Conversion of natural habitats into urban landscapes can expose wildlife to novel pathogens and alter pathogen transmission pathways. Because transmission is difficult to quantify for many wildlife pathogens, mathematical models paired with field observations can help select among competing transmission pathways that might operate in urban landscapes. Here we develop a mathematical model for the enteric bacteria Salmonella enterica in urban-foraging white ibis ( Eudocimus albus) in south Florida as a case study to determine (i) the relative importance of contact-based versus environmental transmission among ibis and (ii) whether transmission can be supported by ibis alone or requires external sources of infection. We use biannual field prevalence data to restrict model outputs generated from a Latin hypercube sample of parameter space and select among competing transmission scenarios. We find the most support for transmission from environmental uptake rather than between-host contact and that ibis-ibis transmission alone could maintain low infection prevalence. Our analysis provides the first parameter estimates for Salmonella shedding and uptake in a wild bird and provides a key starting point for predicting how ibis response to urbanization alters their exposure to a multi-host zoonotic enteric pathogen. More broadly, our study provides an analytical roadmap to assess transmission pathways of multi-host wildlife pathogens in the face of scarce infection data.

Experience drives innovation of new migration patterns of whooping cranes in response to global change.

Anthropogenic changes in climate and land use are driving changes in migration patterns of birds worldwide. Spatial changes in migration have been related to long-term temperature trends, but the intrinsic mechanisms by which migratory species adapt to environmental change remain largely unexplored. We show that, for a long-lived social species, older birds with more experience are critical for innovating new migration behaviours. Groups containing older, more experienced individuals establish new overwintering sites closer to the breeding grounds, leading to a rapid population-level shift in migration patterns. Furthermore, these new overwintering sites are in areas where changes in climate have increased temperatures and where food availability from agriculture is high, creating favourable conditions for overwintering. Our results reveal that the age structure of populations is critical for the behavioural mechanisms that allow species to adapt to global change, particularly for long-lived animals, where changes in behaviour can occur faster than evolution.