Katherine F. Smith

Reducing the Risks of the Wildlife Trade

Importation of wildlife into the United States, most with scant identification, brings an increased threat of disease and introduction of invasive species. The magnitude of the international wildlife trade is immense, with estimates of billions of live animals and animal products traded globally each year (1, 2). This trade has facilitated the introduction of species to new regions, where they compete with native species for resources, alter ecosystems, damage infrastructure, and destroy crops (1, 3). It has also led to the introduction of pathogens that threaten public health, agricultural production, and biodiversity (1, 4).

Global rise in human infectious disease outbreaks

To characterize the change in frequency of infectious disease outbreaks over time worldwide, we encoded and analysed a novel 33-year dataset (1980–2013) of 12 102 outbreaks of 215 human infectious diseases, comprising more than 44 million cases occuring in 219 nations. We merged these records with ecological characteristics of the causal pathogens to examine global temporal trends in the total number of outbreaks, disease richness (number of unique diseases), disease diversity (richness and outbreak evenness) and per capita cases. Bacteria, viruses, zoonotic diseases (originating in animals) and those caused by pathogens transmitted by vector hosts were responsible for the majority of outbreaks in our dataset. After controlling for disease surveillance, communications, geography and host availability, we find the total number and diversity of outbreaks, and richness of causal diseases increased significantly since 1980 (p < 0.0001). When we incorporate Internet usage into the model to control for biased reporting of outbreaks (starting 1990), the overall number of outbreaks and disease richness still increase significantly with time (p < 0.0001), but per capita cases decrease significantly (p = 0.005). Temporal trends in outbreaks differ based on the causal pathogens taxonomy, host requirements and transmission mode. We discuss our preliminary findings in the context of global disease emergence and surveillance.

Globalization of human infectious disease.

Globalization has facilitated the spread of numerous infectious agents to all corners of the planet. Analysis of the Global Infectious Disease and Epidemiology Network (GIDEON) database quantitatively illustrates that the globalization of human infectious agents depends significantly on the range of hosts used. Infectious agents specific to humans are broadly and uniformly distributed, whereas zoonotic infectious agents are far more localized in their geographical distribution. Moreover, these patterns vary depending on transmission mode and infectious agent taxonomy. This dichotomy is unlikely to persist if certain aspects of globalization (for example, exotic species introductions) continue unabated. This raises a serious concern for public health and leaves nations with the task of determining the infectious agents that have the greatest potential to establish within their borders. At the advent of a century characterized by an apparent increase in emerging infectious diseases, these results have critical implications for public-health policy and future research pathways of infectious disease ecology.

Managed relocation: a nuanced evaluation is needed.

Managed relocation (aka ‘assisted colonization’ and ‘assisted migration’ [1,2]) aims to save species from the effects of climate change by purposefully transporting them to areas where they have not previously occurred, but where they are expected to survive as temperatures increase. In a recent Opinion article in TREE [3], Ricciardi and Simberloff suggest that ‘assisted colonization is tantamount to ecological roulette and should probably be rejected as a sound conservation strategy by the precautionary principle.’ We disagree for three primary reasons.

Community assembly of a euryhaline fish microbiome during salinity acclimation

Microbiomes play a critical role in promoting a range of host functions. Microbiome function, in turn, is dependent on its community composition. Yet, how microbiome taxa are assembled from their regional species pool remains unclear. Many possible drivers have been hypothesized, including deterministic processes of competition, stochastic processes of colonization and migration, and physiological ‘host‐effect’ habitat filters. The contribution of each to assembly in nascent or perturbed microbiomes is important for understanding host–microbe interactions and host health. In this study, we characterized the bacterial communities in a euryhaline fish and the surrounding tank water during salinity acclimation. To assess the relative influence of stochastic versus deterministic processes in fish microbiome assembly, we manipulated the bacterial species pool around each fish by changing the salinity of aquarium water. Our results show a complete and repeatable turnover of dominant bacterial taxa in the microbiomes from individuals of the same species after acclimation to the same salinity. We show that changes in fish microbiomes are not correlated with corresponding changes to abundant taxa in tank water communities and that the dominant taxa in fish microbiomes are rare in the aquatic surroundings, and vice versa. Our results suggest that bacterial taxa best able to compete within the unique host environment at a given salinity appropriate the most niche space, independent of their relative abundance in tank water communities. In this experiment, deterministic processes appear to drive fish microbiome assembly, with little evidence for stochastic colonization.

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.

Microbial Diversity and Potential Pathogens in Ornamental Fish Aquarium Water

Ornamental fishes are among the most popular and fastest growing categories of pets in the United States (U.S.). The global scope and scale of the ornamental fish trade and growing popularity of pet fish in the U.S. are strong indicators of the myriad economic and social benefits the pet industry provides. Relatively little is known about the microbial communities associated with these ornamental fishes or the aquarium water in which they are transported and housed. Using conventional molecular approaches and next generation high-throughput amplicon sequencing of 16S ribosomal RNA gene hypervariable regions, we characterized the bacterial community of aquarium water containing common goldfish (Carassius auratus) and Chinese algae eaters (Gyrinocheilus aymonieri) purchased from seven pet/aquarium shops in Rhode Island and identified the presence of potential pathogens. Our survey identified a total of 30 phyla, the most common being Proteobacteria (52%), Bacteroidetes (18%) and Planctomycetes (6%), with the top four phyla representing >80% of all sequences. Sequences from our water samples were most closely related to eleven bacterial species that have the potential to cause disease in fishes, humans and other species: Coxiella burnetii, Flavobacterium columnare, Legionella birminghamensis, L. pneumophila, Vibrio cholerae, V. mimicus. V. vulnificus, Aeromonas schubertii, A. veronii, A. hydrophila and Plesiomonas shigelloides. Our results, combined with evidence from the literature, suggest aquarium tank water harboring ornamental fish are an understudied source for novel microbial communities and pathogens that pose potential risks to the pet industry, fishes in trade, humans and other species.

The macroecology of infectious diseases: a new perspective on global-scale drivers of pathogen distributions and impacts

Identifying drivers of infectious disease patterns and impacts at the broadest scales of organisation is one of the most crucial challenges for modern science, yet answers to many fundamental questions remain elusive. These include what factors commonly facilitate transmission of pathogens to novel host species, what drives variation in immune investment among host species, and more generally what drives global patterns of parasite diversity and distribution? Here we consider how the perspectives and tools of macroecology, a field that investigates patterns and processes at broad spatial, temporal and taxonomic scales, are expanding scientific understanding of global infectious disease ecology. In particular, emerging approaches are providing new insights about scaling properties across all living taxa, and new strategies for mapping pathogen biodiversity and infection risk. Ultimately, macroecology is establishing a framework to more accurately predict global patterns of infectious disease distribution and emergence.

Merging Economics and Epidemiology to Improve the Prediction and Management of Infectious Disease

Mathematical epidemiology, one of the oldest and richest areas in mathematical biology, has significantly enhanced our understanding of how pathogens emerge, evolve, and spread. Classical epidemiological models, the standard for predicting and managing the spread of infectious disease, assume that contacts between susceptible and infectious individuals depend on their relative frequency in the population. The behavioral factors that underpin contact rates are not generally addressed. There is, however, an emerging a class of models that addresses the feedbacks between infectious disease dynamics and the behavioral decisions driving host contact. Referred to as “economic epidemiology” or “epidemiological economics,” the approach explores the determinants of decisions about the number and type of contacts made by individuals, using insights and methods from economics. We show how the approach has the potential both to improve predictions of the course of infectious disease, and to support development of novel approaches to infectious disease management.

Local Scale Effects of Disease on Biodiversity

To date, ecologists and conservation biologists have focused much of their attention on the population and ecosystem effects of disease at regional scales and the role that diseases play in global species extinction. Far less research has been dedicated to identifying the effects that diseases can have on local scale species assemblages. We examined the role of infectious disease in structuring local biodiversity. Our intention was to illustrate how variable outcomes can occur by focusing on three case studies: the influence of chestnut blight on forest communities dominated by chestnut trees, the influence of red-spot disease on urchin barrens and kelp forests, and the influence of sylvatic plague on grassland communities inhabited by prairie dogs. Our findings reveal that at local scales infectious disease seems to play an important, though unpredictable, role in structuring species diversity. Through our case studies, we have shown that diseases can cause drastic population declines or local extirpations in keystone species, ecosystem engineers, and otherwise abundant species. These changes in local diversity may be very important, particularly when considered alongside potentially corresponding changes in community structure and function, and we believe that future efforts to understand the importance of disease to species diversity should have an increased focus on these local scales.