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.

Urban living can rescue Darwin's finches from the lethal effects of invasive vampire flies.

Human activity changes multiple factors in the environment, which can have positive or negative synergistic effects on organisms. However, few studies have explored the causal effects of multiple anthropogenic factors, such as urbanization and invasive species, on animals and the mechanisms that mediate these interactions. This study examines the influence of urbanization on the detrimental effect of invasive avian vampire flies (Philornis downsi) on endemic Darwin's finches in the Galápagos Islands. We experimentally manipulated nest fly abundance in urban and non-urban locations and then characterized nestling health, fledging success, diet, and gene expression patterns related to host defense. Fledging success of non-parasitized nestlings from urban (79%) and non-urban (75%) nests did not differ significantly. However, parasitized, non-urban nestlings lost more blood, and fewer nestlings survived (8%) compared to urban nestlings (50%). Stable isotopic values (δ15 N) from urban nestling feces were higher than those from non-urban nestlings, suggesting that urban nestlings are consuming more protein. δ15 N values correlated negatively with parasite abundance, which suggests that diet might influence host defenses (e.g., tolerance and resistance). Parasitized, urban nestlings differentially expressed genes within pathways associated with red blood cell production (tolerance) and pro-inflammatory response (innate immunological resistance), compared to parasitized, non-urban nestlings. In contrast, parasitized non-urban nestlings differentially expressed genes within pathways associated with immunoglobulin production (adaptive immunological resistance). Our results suggest that urban nestlings are investing more in pro-inflammatory responses to resist parasites but also recovering more blood cells to tolerate blood loss. Although non-urban nestlings are mounting an adaptive immune response, it is likely a last effort by the immune system rather than an effective defense against avian vampire flies since few nestlings survived.

Effect of urbanization and parasitism on the gut microbiota of Darwin's finch nestlings.

Host-associated microbiota can be affected by factors related to environmental change, such as urbanization and invasive species. For example, urban areas often affect food availability for animals, which can change their gut microbiota. Invasive parasites can also influence microbiota through competition or indirectly through a change in the host immune response. These interacting factors can have complex effects on host fitness, but few studies have disentangled the relationship between urbanization and parasitism on an organism's gut microbiota. To address this gap in knowledge, we investigated the effects of urbanization and parasitism by the invasive avian vampire fly (Philornis downsi) on the gut microbiota of nestling small ground finches (Geospiza fuliginosa) on San Cristóbal Island, Galápagos. We conducted a factorial study in which we experimentally manipulated parasite presence in an urban and nonurban area. Faeces were then collected from nestlings to characterize the gut microbiota (i.e. bacterial diversity and community composition). Although we did not find an interactive effect of urbanization and parasitism on the microbiota, we did find main effects of each variable. We found that urban nestlings had lower bacterial diversity and different relative abundances of taxa compared to nonurban nestlings, which could be mediated by introduction of the microbiota of the food items or changes in host physiology. Additionally, parasitized nestlings had lower bacterial richness than nonparasitized nestlings, which could be mediated by a change in the immune system. Overall, this study advances our understanding of the complex effects of anthropogenic stressors on the gut microbiota of birds.

Urban living influences the nesting success of Darwin's finches in the Galápagos Islands.

Urbanization is expanding worldwide with major consequences for organisms. Anthropogenic factors can reduce the fitness of animals but may have benefits, such as consistent human food availability. Understanding anthropogenic trade-offs is critical in environments with variable levels of natural food availability, such as the Galápagos Islands, an area of rapid urbanization. For example, during dry years, the reproductive success of bird species, such as Darwin's finches, is low because reduced precipitation impacts food availability. Urban areas provide supplemental human food to finches, which could improve their reproductive success during years with low natural food availability. However, urban finches might face trade-offs, such as the incorporation of anthropogenic debris (e.g., string, plastic) into their nests, which may increase mortality. In our study, we determined the effect of urbanization on the nesting success of small ground finches (Geospiza fuliginosa; a species of Darwin's finch) during a dry year on San Cristóbal Island. We quantified nest building, egg laying and hatching, and fledging in an urban and nonurban area and characterized the anthropogenic debris in nests. We also documented mortalities including nest trash-related deaths and whether anthropogenic materials directly led to entanglement- or ingestion-related nest mortalities. Overall, urban finches built more nests, laid more eggs, and produced more fledglings than nonurban finches. However, every nest in the urban area contained anthropogenic material, which resulted in 18% nestling mortality while nonurban nests had no anthropogenic debris. Our study showed that urban living has trade-offs: urban birds have overall higher nesting success during a dry year than nonurban birds, but urban birds can suffer mortality from anthropogenic-related nest-materials. These results suggest that despite potential costs, finches benefit overall from urban living and urbanization may buffer the effects of limited resource availability in the Galápagos Islands.

Phylogenetic structure of Holbrookia lacerata (Cope 1880) (Squamata: Phrynosomatidae): one species or two?

Species delimitation attempts to match species-level taxonomy with actual evolutionary lineages. Such taxonomic conclusions are typically, but not always, based on patterns of congruence across multiple data sources and methods of analyses. Here, we use this pluralistic approach to species delimitation to help resolve uncertainty in species boundaries of phrynosomatid sand lizards of the genus Holbrookia. Specifically, the Spot-tailed Earless Lizard (H. lacerata) was historically divided into a northern (H. l. lacerata) and southern (H. l. subcaudalis) subspecies based on differences in morphology and allopatry, but no research has been conducted evaluating genetic differences between these taxa. In this study, patterns in sequence data derived from two genes, one nuclear and one mitochondrial, for 66 individuals sampled across 18 counties in Texas revealed three strongly supported, reciprocally monophyletic lineages, each comprised of individuals from a single geographic region. Distinct genetic variation evident across two of these regions corresponds with differences in morphology, differences in environmental niche, and lines up with the presumed geographic barrier, the Balcones Escarpment, which is the historical subspecies boundary. The combined evidence from genetics, morphology and environmental niche is sufficient to consider these subspecies as distinct species with the lizards north of the Balcones Escarpment retaining the name Holbrookia lacerata, and those south of the Balcones Escarpment being designated as Holbrookia subcaudalis.

Host associations and climate influence avian haemosporidian distributions in Benin.

A majority of avian haemosporidian diversity likely remains undiscovered, and each new recovery helps to further elucidate distributional patterns of diversification. We conducted the first known sampling of avian haemosporidians, Haemoproteus, Leucocytozoon, and Plasmodium from Benin located in tropical West Africa. We sampled 222 birds of 77 species and across distinct ecoregions with varied habitats. Haemosporidians were detected in 113 of 222 individuals, resulting in a 50.9% infection rate. By molecular analysis, we recovered a high number of novel lineages, 52.9%, and characterized the multivariate variables which influence the distributions of haemosporidian genetic lineages, including host associations and bioclimatic variables. We introduced a novel visualization method to better capture the multivariate environment of haemosporidians, and this approach resulted in the recovery of intra-generic distribution patterns of diversity, although no patterns were recovered at the genus level. Our results remain descriptive in nature, but show the promise of predictive strength with an increase in sampling localities with future work. Assessing host and bioclimatic variables at a larger geographic scale and across multiple ecoregions will help to elucidate processes regulating the distribution of haemosporidian diversity.

Avian haemosporidian detection across source materials: prevalence and genetic diversity.

Avian haemosporidians make up one of the most widely distributed and diverse vector borne parasite systems, found nearly worldwide in tropical and temperate areas. Despite the clear relationship between avian host fitness measures and infection, few studies have addressed the importance of source material selection when assessing these relationships. We show that source material, here blood and pectoral muscle, do not yield equivalent results when assessing prevalence and genetic diversity of haemosporidian genera. We find higher prevalence and genetic diversity are recovered from blood versus pectoral muscle for Haemoproteus. Contrastingly, we find that a higher prevalence of Plasmodium is detected from pectoral muscle, while higher genetic diversity is recovered from blood. Our results indicate that source material may bias parasite detection and be an important factor in study design, which is not only related to parasite infection, but by extension to the ecology and fitness of avian hosts.

Diversity and distribution of avian haemosporidians in sub-Saharan Africa: an inter-regional biogeographic overview.

The diversity of avian malaria parasites is much greater than 20th century morphologists realized and virtually every study in this field in the last 15 years has uncovered previously undocumented diversity at multiple levels within the taxonomic hierarchy. Despite this explosion of knowledge, there remain vast sampling gaps, both geographically and host-taxonomically, which makes characterizing patterns of diversity extremely challenging. Here, we summarize the current state of knowledge of sub-Saharan African avian malaria parasite diversity, focusing on avian hosts endemic to Africa. The relative proportions of the parasite genera included here, Plasmodium, Haemoproteus (including Parahaemoproteus) and Leucocytozoon, varied between regions, in part due to habitat preferences of the insect vectors of these genera, and in part we believe due to sampling bias. Biogeographic regions of sub-Saharan Africa harbour about the same proportion of endemic to shared parasite lineages, but there appears to be no phylogenetic structuring across regions. Our results highlight the sampling problem that must be addressed if we are to have a detailed understanding of parasite diversity in Africa. Without broad sampling within and across regions and hosts, using both molecular tools and microscopy, conclusions about parasite diversity, host-parasite interactions or even transmission dynamics remain extremely limited.

Does the niche breadth or trade-off hypothesis explain the abundance-occupancy relationship in avian Haemosporidia?

Two hypotheses have been proposed to explain the abundance-occupancy relationship (AOR) in parasites. The niche breadth hypothesis suggests that host generalists are more abundant and efficient at colonizing different host communities than specialists. The trade-off hypothesis argues that host specialists achieve high density across their hosts' ranges, whereas generalists incur the high cost of adaptation to diverse immuno-defence systems. We tested these hypotheses using 386 haemosporidian cytochrome-b lineages (1894 sequences) recovered from 2318 birds of 103 species sampled in NW Africa, NW Iberia, W Greater Caucasus and Transcaucasia. The number of regions occupied by lineages was associated with their frequency suggesting the presence of AOR in avian Haemosporidia. However, neither hypothesis provided a better explanation for the AOR. Although the host generalist Plasmodium SGS1 was over three times more abundant than other widespread lineages, both host specialists and generalists were successful in colonizing all study regions and achieved high overall prevalence.