Using a Bayesian network to clarify areas requiring research in a host–pathogen system

Bayesian network analyses can be used to interactively change the strength of effect of variables in a model to explore complex relationships in new ways. In doing so, they allow one to identify influential nodes that are not well studied empirically so that future research can be prioritized. We identified relationships in host and pathogen biology to examine disease‐driven declines of amphibians associated with amphibian chytrid fungus (Batrachochytrium dendrobatidis). We constructed a Bayesian network consisting of behavioral, genetic, physiological, and environmental variables that influence disease and used them to predict host population trends. We varied the impacts of specific variables in the model to reveal factors with the most influence on host population trend. The behavior of the nodes (the way in which the variables probabilistically responded to changes in states of the parents, which are the nodes or variables that directly influenced them in the graphical model) was consistent with published results. The frog population had a 49% probability of decline when all states were set at their original values, and this probability increased when body temperatures were cold, the immune system was not suppressing infection, and the ambient environment was conducive to growth of B. dendrobatidis. These findings suggest the construction of our model reflected the complex relationships characteristic of host–pathogen interactions. Changes to climatic variables alone did not strongly influence the probability of population decline, which suggests that climate interacts with other factors such as the capacity of the frog immune system to suppress disease. Changes to the adaptive immune system and disease reservoirs had a large effect on the population trend, but there was little empirical information available for model construction. Our model inputs can be used as a base to examine other systems, and our results show that such analyses are useful tools for reviewing existing literature, identifying links poorly supported by evidence, and understanding complexities in emerging infectious‐disease systems.     

Effects of Invasive Parasites on Bumble Bee Declines

Abstract: Bumble bees are a group of pollinators that are both ecologically and economically important and declining worldwide. Numerous mechanisms could be behind this decline, and the spread of parasites from commercial colonies into wild populations has been implicated recently in North America. Commercial breeding may lead to declines because commercial colonies may have high parasite loads, which can lead to colonization of native bumble bee populations; commercial rearing may allow higher parasite virulence to evolve; and global movement of commercial colonies may disrupt spatial patterns in local adaptation between hosts and parasites. We assessed parasite virulence, transmission mode, and infectivity. Microparasites and so‐called honey bee viruses may pose the greatest threat to native bumble bee populations because certain risk factors are present; for example, the probability of horizontal transmission of the trypanosome parasite Crithidia bombi is high. The microsporidian parasite Nosema bombi may play a role in declines of bumble bees in the United States. Preliminary indications that C. bombi and the neogregarine Apicystis bombi may not be native in parts of South America. We suggest that the development of molecular screening protocols, thorough sanitation efforts, and cooperation among nongovernmental organizations, governments, and commercial breeders might immediately mitigate these threats.     

Golden Eagle fatalities and the continental‐scale consequences of local wind‐energy generation

Renewable energy production is expanding rapidly despite mostly unknown environmental effects on wildlife and habitats. We used genetic and stable isotope data collected from Golden Eagles (Aquila chrysaetos) killed at the Altamont Pass Wind Resource Area (APWRA) in California in demographic models to test hypotheses about the geographic extent and demographic consequences of fatalities caused by renewable energy facilities. Geospatial analyses of δ²H values obtained from feathers showed that ≥25% of these APWRA‐killed eagles were recent immigrants to the population, most from long distances away (>100 km). Data from nuclear genes indicated this subset of immigrant eagles was genetically similar to birds identified as locals from the δ²H data. Demographic models implied that in the face of this mortality, the apparent stability of the local Golden Eagle population was maintained by continental‐scale immigration. These analyses demonstrate that ecosystem management decisions concerning the effects of local‐scale renewable energy can have continental‐scale consequences.     

Examining the uncertain origin and management role of martens on Prince of Wales Island,Alaska

Conservation biologists are generally united in efforts to curtail the spread of non‐native species globally. However, the colonization history of a species is not always certain, and whether a species is considered non‐native or native depends on the conservation benchmark. Such ambiguities have led to inconsistent management. Within the Tongass National Forest of Alaska, the status of American marten (Martes americana) on the largest, most biologically diverse and deforested island, Prince of Wales (POW), is unclear. Ten martens were released to POW in the early 1930s, and it was generally believed to be the founding event, although this has been questioned. The uncertainty surrounding when and how martens colonized POW complicates management, especially because martens were selected as a design species for the Tongass. To explore the history of martens of POW we reviewed other plausible routes of colonization; genetically and isotopically analyzed putative marten fossils deposited in the late Pleistocene and early Holocene to verify marten occupancy of POW; and used contemporary genetic data from martens on POW and the mainland in coalescent simulations to identify the probable source of the present‐day marten population on POW. We found evidence for multiple routes of colonization by forest‐associated mammals beginning in the Holocene, which were likely used by American martens to naturally colonize POW. Although we cannot rule out human‐assisted movement of martens by Alaskan Natives or fur trappers, we suggest that martens be managed for persistence on POW. More generally, our findings illustrate the difficulty of labeling species as non‐native or native, even when genetic and paleo‐ecological data are available, and support the notion that community resilience or species invasiveness should be prioritized when making management decisions rather than more subjective and less certain conservation benchmarks.     

Butterfly community shifts over two centuries

Environmental changes strongly impact the distribution of species and subsequently the composition of species assemblages. Although most community ecology studies represent temporal snap shots, long‐term observations are rather rare. However, only such time series allow the identification of species composition shifts over several decades or even centuries. We analyzed changes in the species composition of a southeastern German butterfly and burnet moth community over nearly 2 centuries (1840–2013). We classified all species observed over this period according to their ecological tolerance, thereby assessing their degree of habitat specialisation. This classification was based on traits of the butterfly and burnet moth species and on their larval host plants. We collected data on temperature and precipitation for our study area over the same period. The number of species declined substantially from 1840 (117 species) to 2013 (71 species). The proportion of habitat specialists decreased, and most of these are currently endangered. In contrast, the proportion of habitat generalists increased. Species with restricted dispersal behavior and species in need of areas poor in soil nutrients had severe losses. Furthermore, our data indicated a decrease in species composition similarity between different decades over time. These data on species composition changes and the general trends of modifications may reflect effects from climate change and atmospheric nitrogen loads, as indicated by the ecological characteristics of host plant species and local changes in habitat configuration with increasing fragmentation. Our observation of major declines over time of currently threatened and protected species shows the importance of efficient conservation strategies.     

Variation with Land Use of Immune Function and Prevalence of Avian Pox in Galapagos Finches

Introduced disease has been implicated in recent wildlife extinctions and population declines worldwide. Both anthropogenic‐induced change and natural environmental features can affect pathogen spread. Furthermore, environmental disturbance can result in changes in stress physiology, nutrition, and social structure, which in turn can suppress immune system function. However, it remains unknown whether landscape variation results in heterogeneity in host resistance to pathogens. Avian pox virus, a pathogen implicated in avian declines and extinctions in Hawaii, was introduced to the Galapagos in the 1890s, and prevalence (total number of current infections) has increased recently in finches. We tested whether prevalence and recovery trends in 7 species of Galapagos finches varied by elevation or human land use. To do so, we used infection data obtained from 545 wild‐caught birds. In addition, we determined whether annual changes in 4 aspects of innate immune function (complement protein activity, natural antibody activity, concentration of PIT54 protein, and heterophil:lymphocyte ratio) varied by elevation or land use. Prevalence and recovery rates did not vary by elevation from 2008 to 2009. Avian pox prevalence and proportion of recovered individuals in undeveloped and urban areas did not change from 2008 to 2009. In agricultural areas, avian pox prevalence increased 8‐fold (from 2% to 17% of 234 individuals sampled) and proportion of recovered individuals increased (11% to 19%) from 2008 to 2009. These results suggest high disease‐related mortality. Variation in immune function across human land‐use types correlated with variation in both increased prevalence and susceptibility, which indicates changes in innate immune function may underlie changes in disease susceptibility. Our results suggest anthropogenic disturbance, in particular agricultural practices, may underlie immunological changes in host species that themselves contribute to pathogen emergence. Variación con el Uso de Suelo de la Función Inmune y la Prevalencia de la Varicela Aviar en Pinzones de las Galápagos     

A case study of bats and white‐nose syndrome demonstrating how to model population viability with evolutionary effects

Ecological factors generally affect population viability on rapid time scales. Traditional population viability analyses (PVA) therefore focus on alleviating ecological pressures, discounting potential evolutionary impacts on individual phenotypes. Recent studies of evolutionary rescue (ER) focus on cases in which severe, environmentally induced population bottlenecks trigger a rapid evolutionary response that can potentially reverse demographic threats. ER models have focused on shifting genetics and resulting population recovery, but no one has explored how to incorporate those findings into PVA. We integrated ER into PVA to identify the critical decision interval for evolutionary rescue (DIER) under which targeted conservation action should be applied to buffer populations undergoing ER against extinction from stochastic events and to determine the most appropriate vital rate to target to promote population recovery. We applied this model to little brown bats (Myotis lucifugus) affected by white‐nose syndrome (WNS), a fungal disease causing massive declines in several North American bat populations. Under the ER scenario, the model predicted that the DIER period for little brown bats was within 11 years of initial WNS emergence, after which they stabilized at a positive growth rate (λ = 1.05). By comparing our model results with population trajectories of multiple infected hibernacula across the WNS range, we concluded that ER is a potential explanation of observed little brown bat population trajectories across multiple hibernacula within the affected range. Our approach provides a tool that can be used by all managers to provide testable hypotheses regarding the occurrence of ER in declining populations, suggest empirical studies to better parameterize the population genetics and conservation‐relevant vital rates, and identify the DIER period during which management strategies will be most effective for species conservation.     

Anthropogenic threats to evolutionary heritage of angiosperms in the Netherlands through an increase in high-competition environments

Present biodiversity comprises the evolutionary heritage of Earth's epochs. Lineages from particular epochs are often found in particular habitats, but whether current habitat decline threatens the heritage from particular epochs is unknown. We hypothesized that within a given region, humans threaten specifically habitats that harbor lineages from a particular geological epoch. We expect so because humans threaten environments that dominated and lineages that diversified during these epochs. We devised a new approach to quantify, per habitat type, diversification of lineages from different epochs. For Netherlands, one of the floristically and ecologically best-studied regions, we quantified the decline of habitat types and species in the past century. We defined habitat types based on vegetation classification and used existing ranking of decline of vegetation classes and species. Currently, most declining habitat types and the group of red-listed species are characterized by increased diversification of lineages dating back to Paleogene, specifically to Paleocene-Eocene and Oligocene. Among vulnerable habitat types with large representation of lineages from these epochs were sublittoral and eulittoral zones of temperate seas and 2 types of nutrient-poor, open habitats. These losses of evolutionary heritage would go unnoticed with classical measures of evolutionary diversity. Loss of heritage from Paleocene-Eocene became unrelated to decline once low competition, shade tolerance, and low proportion of non-Apiaceae were accounted for, suggesting that these variables explain the loss of heritage from Paleocene-Eocene. Losses of heritage from Oligocene were partly explained by decline of habitat types occupied by weak competitors and shade-tolerant species. Our results suggest a so-far unappreciated human threat to evolutionary heritage: habitat decline threatens descendants from particular epochs. If the trends persist into the future uncontrolled, there may be no habitats within the region for many descendants of evolutionary ancient epochs, such as Paleogene.     

The Threat of Disease Increases as Species Move Toward Extinction

At local scales, infectious disease is a common driver of population declines, but globally it is an infrequent contributor to species extinction and endangerment. For species at risk of extinction from disease important questions remain unanswered, including when does disease become a threat to species and does it co‐occur, predictably, with other threats? Using newly compiled data from the International Union for Conservation of Nature (IUCN) Red List, we examined the relative role and co‐occurrence of threats associated with amphibians, birds, and mammals at 6 levels of extinction risk (i.e., Red List status categories: least concern, near threatened, vulnerable, endangered, critically endangered, and extinct in the wild/extinct). We tested the null hypothesis that the proportion of species threatened by disease is the same in all 6 Red List status categories. Our approach revealed a new method for determining when disease most frequently threatens species at risk of extinction. The proportion of species threatened by disease varied significantly between IUCN status categories and linearly increased for amphibians, birds, and all species combined as these taxa move from move from least concern to critically endangered. Disease was infrequently the single contributing threat. However, when a species was negatively affected by a major threat other than disease (e.g., invasive species, land‐use change) that species was more likely to be simultaneously threatened by disease than species that had no other threats. Potential drivers of these trends include ecological factors, clustering of phylogenetically related species in Red List status categories, discovery bias among species at greater risk of extinction, and availability of data. We echo earlier calls for baseline data on the presence of parasites and pathogens in species when they show the first signs of extinction risk and arguably before. La Amenaza de Enfermedades Incrementa a Medida que las Especies se Aproximan a la Extinción