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Papers by Susanne Sokolow

Research paper thumbnail of Infection with schistosome parasites in snails leads to increased predation by prawns: implications for human schistosomiasis control

Schistosomiasis – a parasitic disease that affects over 200 million people across the globe – is ... more Schistosomiasis – a parasitic disease that affects over 200 million people across the globe – is primarily transmitted between human definitive hosts and snail intermediate hosts. To reduce schistosomiasis transmission, some have advocated disrupting the schistosome life cycle through biological control of snails, achieved by boosting the abundance of snails' natural predators. But little is known about the effect of parasitic infection on predator–prey interactions, especially in the case of schistosomiasis. Here, we present the results of laboratory experiments performed on Bulinus truncatus and Biomphalaria glabrata snails to investigate: (i) rates of predation on schistosome-infected versus uninfected snails by a sympatric native river prawn, Macrobrachium vollenhovenii, and (ii) differences in snail behavior (including movement, refuge-seeking and anti-predator behavior) between infected and uninfected snails. In predation trials, prawns showed a preference for consuming snails infected with schistosome larvae. In behavioral trials, infected snails moved less quickly and less often than uninfected snails, and were less likely to avoid predation by exiting the water or hiding under substrate. Although the mechanism by which the parasite alters snail behavior remains unknown, these results provide insight into the effects of parasitic infection on predator–prey dynamics and suggest that boosting natural rates of predation on snails may be a useful strategy for reducing transmission in schistosomiasis hotspots.

Research paper thumbnail of A Theoretical Analysis of the Geography of Schistosomiasis in Burkina Faso Highlights the Roles of Human Mobility and Water Resources Development in Disease Transmission

PLOS Neglected Tropical Diseases, 2015

We study the geography of schistosomiasis across Burkina Faso by means of a spatially explicit mo... more We study the geography of schistosomiasis across Burkina Faso by means of a spatially explicit model of water-based disease dynamics. The model quantitatively addresses the geographic stratification of disease burden in a novel framework by explicitly accounting for drivers and controls of the disease, including spatial information on the distributions of population and infrastructure, jointly with a general description of human mobility and climatic/ecological drivers. Spatial patterns of disease are analysed by the extraction and the mapping of suitable eigenvectors of the Jacobian matrix subsuming the stability of the disease-free equilibrium. The relevance of the work lies in the novel mapping of disease burden, a byproduct of the parametrization induced by regional upscaling, by model-guided field validations and in the predictive scenarios allowed by exploiting the range of possible parameters and processes. Human mobility is found to be a primary control at regional scales both for pathogen invasion success and the overall distribution of disease burden. The effects of water resources development highlighted by systematic reviews are accounted for by the average distances of human settlements from water bodies that are habitats for the parasite's intermediate host. Our results confirm the empirical findings about the role of water resources development on disease spread into regions previously nearly disease-free also by inspection of empirical prevalence patterns. We conclude that while the model still needs refinements based on field and epidemiological evidence, the proposed framework provides a powerful tool for large-scale public health planning and schistosomiasis management.

Research paper thumbnail of Reduced transmission of human schistosomiasis after restoration of a native river prawn that preys on the snail intermediate host

Proceedings of the National Academy of Sciences of the United States of America, Jan 4, 2015

Eliminating human parasitic disease often requires interrupting complex transmission pathways. Ev... more Eliminating human parasitic disease often requires interrupting complex transmission pathways. Even when drugs to treat people are available, disease control can be difficult if the parasite can persist in nonhuman hosts. Here, we show that restoration of a natural predator of a parasite's intermediate hosts may enhance drug-based schistosomiasis control. Our study site was the Senegal River Basin, where villagers suffered a massive outbreak and persistent epidemic after the 1986 completion of the Diama Dam. The dam blocked the annual migration of native river prawns (Macrobrachium vollenhoveni) that are voracious predators of the snail intermediate hosts for schistosomiasis. We tested schistosomiasis control by reintroduced river prawns in a before-after-control-impact field experiment that tracked parasitism in snails and people at two matched villages after prawns were stocked at one village's river access point. The abundance of infected snails was 80% lower at that vill...

Research paper thumbnail of Restoring native crustacean predators offers transmission control for a neglected tropical disease, schistosomiasis, in Africa

Background/Question/Methods Among neglected tropical diseases (NTDs), human schistosomiasis is on... more Background/Question/Methods Among neglected tropical diseases (NTDs), human schistosomiasis is one of the most widespread and devastating. The disease is easy to treat, using the drug praziquantel, but remains hard to control. In endemic areas, treated people are rapidly re-infected when they wade or swim in waters that harbor parasite-infected snails. Thus, affordable tools to control transmission are lacking, drugs alone are an unsustainable remedy, and more than 220 million infected people on three continents are in need of a solution. Here, we present a proof-of-concept for a novel method to control transmission of this NTD by restoring native crustaceans that feed on snails. We propose that predatory freshwater prawns will lead to substantial disease reductions when restored to the rivers and streams where human-induced landscape changes (like dams and irrigation schemes) have decimated their populations and led to disease outbreaks. We present field evidence of transmission co...

Research paper thumbnail of Sapronosis: a distinctive type of infectious agent

Trends in Parasitology, 2014

Research paper thumbnail of The Prawn Macrobrachium vollenhovenii in the Senegal River Basin: Towards Sustainable Restocking of All-Male Populations for Biological Control of Schistosomiasis

PLoS Neglected Tropical Diseases, 2014

Early malacological literature suggests that the outbreak of schistosomiasis, a parasitic disease... more Early malacological literature suggests that the outbreak of schistosomiasis, a parasitic disease transmitted by aquatic snails, in the Senegal River basin occurred due to ecological changes resulting from the construction of the Diama dam. The common treatment, the drug praziquantel, does not protect from the high risk of re-infection due to human contact with infested water on a daily basis. The construction of the dam interfered with the life cycle of the prawn Macrobrachium vollenhovenii by blocking its access to breeding grounds in the estuary. These prawns were demonstrated to be potential biological control agents, being effective predators of Schistosoma-susceptible snails. Here, we propose a responsible restocking strategy using all-male prawn populations which could provide sustainable disease control. Male prawns reach a larger size and have a lower tendency to migrate than females. We, therefore, expect that periodic restocking of all-male juveniles will decrease the prevalence of schistosomiasis and increase villagers' welfare. In this interdisciplinary study, we examined current prawn abundance along the river basin, complemented with a retrospective questionnaire completed by local fishermen. We revealed the current absence of prawns upriver and thus demonstrated the need for restocking. Since male prawns are suggested to be preferable for bio-control, we laid the molecular foundation for production of all-male M. vollenhovenii through a complete sequencing of the insulin-like androgenic gland-encoding gene (IAG), which is responsible for sexual differentiation in crustaceans. We also conducted bioinformatics and immunohistochemistry analyses to demonstrate the similarity of this sequence to the IAG of another Macrobrachium species in which neo-females are produced and their progeny are 100% males. At least 100 million people at risk of schistosomiasis are residents of areas that experienced water management manipulations. Our suggested non-breeding sustainable model of control-if proven successful-could prevent re-infections and thus prove useful throughout the world.

Research paper thumbnail of Predictive Power of Air Travel and Socio-Economic Data for Early Pandemic Spread

PLoS ONE, 2010

Controlling the pandemic spread of newly emerging diseases requires rapid, targeted allocation of... more Controlling the pandemic spread of newly emerging diseases requires rapid, targeted allocation of limited resources among nations. Critical, early control steps would be greatly enhanced if the key risk factors can be identified that accurately predict early disease spread immediately after emergence. Here, we examine the role of travel, trade, and national healthcare resources in predicting the emergence and initial spread of 2009 A/H1N1 influenza. We find that incorporating national healthcare resource data into our analyses allowed a much greater capacity to predict the international spread of this virus. In countries with lower healthcare resources, the reporting of 2009 A/H1N1 cases was significantly delayed, likely reflecting a lower capacity for testing and reporting, as well as other socio-political issues. We also report substantial international trade in live swine and poultry in the decade preceding the pandemic which may have contributed to the emergence and mixed genotype of this pandemic strain. However, the lack of knowledge of recent evolution of each H1N1 viral gene segment precludes the use of this approach to determine viral origins. We conclude that strategies to prevent pandemic influenza virus emergence and spread in the future should include: 1) enhanced surveillance for strains resulting from reassortment in traded livestock; 2) rapid deployment of control measures in the initial spreading phase to countries where travel data predict the pathogen will reach and to countries where lower healthcare resources will likely cause delays in reporting. Our results highlight the benefits, for all parties, when higher income countries provide additional healthcare resources for lower income countries, particularly those that have high air traffic volumes. In particular, international authorities should prioritize aid to those poorest countries where both the risk of emerging infectious diseases and air traffic volume is highest. This strategy will result in earlier detection of pathogens and a reduction in the impact of future pandemics.

Research paper thumbnail of Editor's choice: Disease dynamics in marine metapopulations: modelling infectious diseases on coral reefs

Journal of Applied Ecology, 2009

Coral reefs are experiencing devastating mortality due, in part, to emerging disease. Despite thi... more Coral reefs are experiencing devastating mortality due, in part, to emerging disease. Despite this growing problem, the long-term consequences of infectious disease in marine ecosystems remain poorly understood, and the application of epidemiological models to marine disease systems represents a research priority for managing resources in the world's oceans. 2. Metapopulation models may provide a framework for modelling coral population dynamics at the regional scale, and we use this approach to investigate the effects of infectious disease. The model presented here incorporates a susceptible-infected or 'S-I' disease into a system of patchily distributed, dynamic coral hosts, and highlights some basic differences that set many marine disease systems apart from their terrestrial counterparts. 3. The model predicts several possible long-term outcomes of disease introduction, and suggests that the consequences of disease may vary considerably among different pathogens and regions. Due to the long time-scales for coral dynamics, epizootics are expected to be prolonged with recovery slow at the regional scale. 4. Our model results show how infectious disease can substantially alter host metapopulation dynamics, with some non-linear relationships which are likely to affect the response of these systems to management and environmental change. For example, higher rates of coral colonization can have variable consequences for host population occupancy (i.e. coral cover) when infectious disease is considered, and chronic diseases with long-lived pathogens pose the highest risks for regional coral extinction. 5. Synthesis and applications. We present a tractable epidemiological model within a metapopulation framework and compare the model output with empirical data for a white plague type II (WPII) outbreak among coral of the upper Florida Keys. We conclude that this model fits well with the spatial and temporal patterns of WPII over a decade. Despite terrestrial-marine differences, many patterns derived from our model are consistent with epidemiological principles. Thus, the careful application of these principles within the context of marine management may be a promising research frontier. Although we focus on coral disease, the methods and results may apply to other marine metapopulations.

Research paper thumbnail of Spatial Epidemiology of Caribbean Yellow Band Syndrome in Montastrea spp. Coral in the Eastern Yucatan, Mexico

Hydrobiologia, 2005

Caribbean yellow band syndrome (YBS) is a poorly understood, progressively fatal disease primaril... more Caribbean yellow band syndrome (YBS) is a poorly understood, progressively fatal disease primarily affecting Montastraea spp. coral. This disease has exhibited rapid spread throughout the entire Caribbean over the last few decades. In this study, geographical information systems (GIS) and spatial statistics were used to analyze the distribution of YBS in Akumal Bay, Mexico, and host and environmental risk factors for YBS were evaluated epidemiologically. In this Bay, there are hundreds of colonies of Montastraea annularis from 1 m depths inside the fringing reefs to reef crests and beyond. Of 63 corals that were evaluated, the overall prevalence of YBS in Akumal Bay was 28.6%, with 35.7% in large colonies, 23.8% in medium-sized colonies, and 23.8% in small colonies, where small colonies were <200 cm diameter, medium-sized were 200-500 cm, and large were >500 cm. Lesions covered 3.8% (±1.3 s.e.) of the surface of colonies assessed, compared with a mean percentage of dead colony cover of 54.4% (±4.2 s.e.). Analysis for spatial clustering documented that M. annularis colonies (well and sick) were highly spatially clustered, compared to expected complete spatial randomness. However, compared with all M. annularis corals, colonies with YBS tended to be less spatially clustered (i.e. within the overall clustered spatial distribution of M. annularis colonies, YBS-affected coloniesÕ distribution was more regular). These findings are consistent with several hypotheses for the etiology of YBS, including near-shore pathogens or toxins either directly inducing disease or indirectly leading to disease by increasing host susceptibility. Ongoing investigations into the management and cause of YBS can use this information to develop management strategies and more efficiently target future sampling.

Research paper thumbnail of Causal inference in disease ecology: investigating ecological drivers of disease emergence

Frontiers in Ecology and the Environment, 2008

Research paper thumbnail of Allometry and spatial scales of foraging in mammalian herbivores

Ecology Letters, 2010

Herbivores forage in spatially complex habitats. Due to allometry and scale-dependent foraging, h... more Herbivores forage in spatially complex habitats. Due to allometry and scale-dependent foraging, herbivores are hypothesized to perceive and respond to heterogeneity of resources at scales relative to their body sizes. This hypothesis has not been manipulatively tested for animals with only moderate differences in body size and similar food niches. We compared short-term spatial foraging behavior of two herbivores (sheep and cattle) with similar dietary niche but differing body size. Although intake rates scaled allometrically with body mass (mass 0.75 ), spatial foraging strategies substantially differed, with cattle exhibiting a coarser-grained use of the Ôfoodscape.Õ Selectivity by cattle (and not sheep) for their preferred food was more restricted when patches were smaller (< 10 m 2 ). We conclude that differences in spatial scales of selection offers a plausible mechanism by which species can coexist on shared resources that exhibit multiple scales of spatial heterogeneity.

Research paper thumbnail of Ecology of avian influenza viruses in a changing world

Annals of the New York Academy of Sciences, 2010

Influenza A virus infections result in ∼500,000 human deaths per year and many more sublethal inf... more Influenza A virus infections result in ∼500,000 human deaths per year and many more sublethal infections. Wild birds are recognized as the ancestral host of influenza A viruses, and avian viruses have contributed genetic material to most human viruses, including subtypes H5N1 and H1N1. Thus, influenza virus transmission in wild and domestic animals and humans is intimately connected. Here we review how anthropogenic change, including human population growth, land use, climate change, globalization of trade, agricultural intensification, and changes in vaccine technology may alter the evolution and transmission of influenza viruses. Evidence suggests that viral transmission in domestic poultry, spillover to other domestic animals, wild birds and humans, and the potential for subsequent pandemic spread, are all increasing. We highlight four areas in need of research: drivers of viral subtype dynamics; ecological and evolutionary determinants of transmissibility and virulence in birds and humans; the impact of changing land use and climate on hosts, viruses, and transmission; and the impact of influenza viruses on wild bird hosts, including their ability to migrate while shedding virus.

Research paper thumbnail of Epidemiologic evaluation of diarrhea in dogs in an animal shelter

American Journal of Veterinary Research, 2005

Research paper thumbnail of Regulation of laboratory populations of snails (Biomphalaria and Bulinus spp.) by river prawns, Macrobrachium spp. (Decapoda, Palaemonidae): Implications for control of schistosomiasis

Acta Tropica, 2014

Human schistosomiasis is a common parasitic disease endemic in many tropical and subtropical coun... more Human schistosomiasis is a common parasitic disease endemic in many tropical and subtropical countries. One barrier to achieving long-term control of this disease has been re-infection of treated patients when they swim, bathe, or wade in surface fresh water infested with snails that harbor and release larval parasites. Because some snail species are obligate intermediate hosts of schistosome parasites, removing snails may reduce parasitic larvae in the water, reducing re-infection risk. Here, we evaluate the potential for snail control by predatory freshwater prawns, Macrobrachium rosenbergii and M. vollenhovenii, native to Asia and Africa, respectively. Both prawn species are high value, protein-rich human food commodities, suggesting their cultivation may be beneficial in resource-poor settings where few other disease control options exist. In a series of predation trials in laboratory aquaria, we found both species to be voracious predators of schistosome-susceptible snails, hatchlings, and eggs, even in the presence of alternative food, with sustained average consumption rates of 12% of their body weight per day. Prawns showed a weak preference for Bulinus truncatus over Biomphalaria glabrata snails. Consumption rates were highly predictable based on the ratio of prawn: snail body mass, suggesting satiation-limited predation. Even the smallest prawns tested (0.5-2 g) caused snail recruitment failure, despite high snail fecundity. With the World Health Organization turning attention toward schistosomiasis elimination, native prawn cultivation may be a viable snail control strategy that offers a win-win for public health and economic development.

Research paper thumbnail of Nearly 400 million people are at higher risk of schistosomiasis because dams block the migration of snail-eating river prawns

Cite this article: Sokolow SH et al. 2017

Research paper thumbnail of Infection with schistosome parasites in snails leads to increased predation by prawns: implications for human schistosomiasis control

Schistosomiasis – a parasitic disease that affects over 200 million people across the globe – is ... more Schistosomiasis – a parasitic disease that affects over 200 million people across the globe – is primarily transmitted between human definitive hosts and snail intermediate hosts. To reduce schistosomiasis transmission, some have advocated disrupting the schistosome life cycle through biological control of snails, achieved by boosting the abundance of snails' natural predators. But little is known about the effect of parasitic infection on predator–prey interactions, especially in the case of schistosomiasis. Here, we present the results of laboratory experiments performed on Bulinus truncatus and Biomphalaria glabrata snails to investigate: (i) rates of predation on schistosome-infected versus uninfected snails by a sympatric native river prawn, Macrobrachium vollenhovenii, and (ii) differences in snail behavior (including movement, refuge-seeking and anti-predator behavior) between infected and uninfected snails. In predation trials, prawns showed a preference for consuming snails infected with schistosome larvae. In behavioral trials, infected snails moved less quickly and less often than uninfected snails, and were less likely to avoid predation by exiting the water or hiding under substrate. Although the mechanism by which the parasite alters snail behavior remains unknown, these results provide insight into the effects of parasitic infection on predator–prey dynamics and suggest that boosting natural rates of predation on snails may be a useful strategy for reducing transmission in schistosomiasis hotspots.

Research paper thumbnail of A Theoretical Analysis of the Geography of Schistosomiasis in Burkina Faso Highlights the Roles of Human Mobility and Water Resources Development in Disease Transmission

PLOS Neglected Tropical Diseases, 2015

We study the geography of schistosomiasis across Burkina Faso by means of a spatially explicit mo... more We study the geography of schistosomiasis across Burkina Faso by means of a spatially explicit model of water-based disease dynamics. The model quantitatively addresses the geographic stratification of disease burden in a novel framework by explicitly accounting for drivers and controls of the disease, including spatial information on the distributions of population and infrastructure, jointly with a general description of human mobility and climatic/ecological drivers. Spatial patterns of disease are analysed by the extraction and the mapping of suitable eigenvectors of the Jacobian matrix subsuming the stability of the disease-free equilibrium. The relevance of the work lies in the novel mapping of disease burden, a byproduct of the parametrization induced by regional upscaling, by model-guided field validations and in the predictive scenarios allowed by exploiting the range of possible parameters and processes. Human mobility is found to be a primary control at regional scales both for pathogen invasion success and the overall distribution of disease burden. The effects of water resources development highlighted by systematic reviews are accounted for by the average distances of human settlements from water bodies that are habitats for the parasite&amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;#39;s intermediate host. Our results confirm the empirical findings about the role of water resources development on disease spread into regions previously nearly disease-free also by inspection of empirical prevalence patterns. We conclude that while the model still needs refinements based on field and epidemiological evidence, the proposed framework provides a powerful tool for large-scale public health planning and schistosomiasis management.

Research paper thumbnail of Reduced transmission of human schistosomiasis after restoration of a native river prawn that preys on the snail intermediate host

Proceedings of the National Academy of Sciences of the United States of America, Jan 4, 2015

Eliminating human parasitic disease often requires interrupting complex transmission pathways. Ev... more Eliminating human parasitic disease often requires interrupting complex transmission pathways. Even when drugs to treat people are available, disease control can be difficult if the parasite can persist in nonhuman hosts. Here, we show that restoration of a natural predator of a parasite's intermediate hosts may enhance drug-based schistosomiasis control. Our study site was the Senegal River Basin, where villagers suffered a massive outbreak and persistent epidemic after the 1986 completion of the Diama Dam. The dam blocked the annual migration of native river prawns (Macrobrachium vollenhoveni) that are voracious predators of the snail intermediate hosts for schistosomiasis. We tested schistosomiasis control by reintroduced river prawns in a before-after-control-impact field experiment that tracked parasitism in snails and people at two matched villages after prawns were stocked at one village's river access point. The abundance of infected snails was 80% lower at that vill...

Research paper thumbnail of Restoring native crustacean predators offers transmission control for a neglected tropical disease, schistosomiasis, in Africa

Background/Question/Methods Among neglected tropical diseases (NTDs), human schistosomiasis is on... more Background/Question/Methods Among neglected tropical diseases (NTDs), human schistosomiasis is one of the most widespread and devastating. The disease is easy to treat, using the drug praziquantel, but remains hard to control. In endemic areas, treated people are rapidly re-infected when they wade or swim in waters that harbor parasite-infected snails. Thus, affordable tools to control transmission are lacking, drugs alone are an unsustainable remedy, and more than 220 million infected people on three continents are in need of a solution. Here, we present a proof-of-concept for a novel method to control transmission of this NTD by restoring native crustaceans that feed on snails. We propose that predatory freshwater prawns will lead to substantial disease reductions when restored to the rivers and streams where human-induced landscape changes (like dams and irrigation schemes) have decimated their populations and led to disease outbreaks. We present field evidence of transmission co...

Research paper thumbnail of Sapronosis: a distinctive type of infectious agent

Trends in Parasitology, 2014

Research paper thumbnail of The Prawn Macrobrachium vollenhovenii in the Senegal River Basin: Towards Sustainable Restocking of All-Male Populations for Biological Control of Schistosomiasis

PLoS Neglected Tropical Diseases, 2014

Early malacological literature suggests that the outbreak of schistosomiasis, a parasitic disease... more Early malacological literature suggests that the outbreak of schistosomiasis, a parasitic disease transmitted by aquatic snails, in the Senegal River basin occurred due to ecological changes resulting from the construction of the Diama dam. The common treatment, the drug praziquantel, does not protect from the high risk of re-infection due to human contact with infested water on a daily basis. The construction of the dam interfered with the life cycle of the prawn Macrobrachium vollenhovenii by blocking its access to breeding grounds in the estuary. These prawns were demonstrated to be potential biological control agents, being effective predators of Schistosoma-susceptible snails. Here, we propose a responsible restocking strategy using all-male prawn populations which could provide sustainable disease control. Male prawns reach a larger size and have a lower tendency to migrate than females. We, therefore, expect that periodic restocking of all-male juveniles will decrease the prevalence of schistosomiasis and increase villagers' welfare. In this interdisciplinary study, we examined current prawn abundance along the river basin, complemented with a retrospective questionnaire completed by local fishermen. We revealed the current absence of prawns upriver and thus demonstrated the need for restocking. Since male prawns are suggested to be preferable for bio-control, we laid the molecular foundation for production of all-male M. vollenhovenii through a complete sequencing of the insulin-like androgenic gland-encoding gene (IAG), which is responsible for sexual differentiation in crustaceans. We also conducted bioinformatics and immunohistochemistry analyses to demonstrate the similarity of this sequence to the IAG of another Macrobrachium species in which neo-females are produced and their progeny are 100% males. At least 100 million people at risk of schistosomiasis are residents of areas that experienced water management manipulations. Our suggested non-breeding sustainable model of control-if proven successful-could prevent re-infections and thus prove useful throughout the world.

Research paper thumbnail of Predictive Power of Air Travel and Socio-Economic Data for Early Pandemic Spread

PLoS ONE, 2010

Controlling the pandemic spread of newly emerging diseases requires rapid, targeted allocation of... more Controlling the pandemic spread of newly emerging diseases requires rapid, targeted allocation of limited resources among nations. Critical, early control steps would be greatly enhanced if the key risk factors can be identified that accurately predict early disease spread immediately after emergence. Here, we examine the role of travel, trade, and national healthcare resources in predicting the emergence and initial spread of 2009 A/H1N1 influenza. We find that incorporating national healthcare resource data into our analyses allowed a much greater capacity to predict the international spread of this virus. In countries with lower healthcare resources, the reporting of 2009 A/H1N1 cases was significantly delayed, likely reflecting a lower capacity for testing and reporting, as well as other socio-political issues. We also report substantial international trade in live swine and poultry in the decade preceding the pandemic which may have contributed to the emergence and mixed genotype of this pandemic strain. However, the lack of knowledge of recent evolution of each H1N1 viral gene segment precludes the use of this approach to determine viral origins. We conclude that strategies to prevent pandemic influenza virus emergence and spread in the future should include: 1) enhanced surveillance for strains resulting from reassortment in traded livestock; 2) rapid deployment of control measures in the initial spreading phase to countries where travel data predict the pathogen will reach and to countries where lower healthcare resources will likely cause delays in reporting. Our results highlight the benefits, for all parties, when higher income countries provide additional healthcare resources for lower income countries, particularly those that have high air traffic volumes. In particular, international authorities should prioritize aid to those poorest countries where both the risk of emerging infectious diseases and air traffic volume is highest. This strategy will result in earlier detection of pathogens and a reduction in the impact of future pandemics.

Research paper thumbnail of Editor's choice: Disease dynamics in marine metapopulations: modelling infectious diseases on coral reefs

Journal of Applied Ecology, 2009

Coral reefs are experiencing devastating mortality due, in part, to emerging disease. Despite thi... more Coral reefs are experiencing devastating mortality due, in part, to emerging disease. Despite this growing problem, the long-term consequences of infectious disease in marine ecosystems remain poorly understood, and the application of epidemiological models to marine disease systems represents a research priority for managing resources in the world's oceans. 2. Metapopulation models may provide a framework for modelling coral population dynamics at the regional scale, and we use this approach to investigate the effects of infectious disease. The model presented here incorporates a susceptible-infected or 'S-I' disease into a system of patchily distributed, dynamic coral hosts, and highlights some basic differences that set many marine disease systems apart from their terrestrial counterparts. 3. The model predicts several possible long-term outcomes of disease introduction, and suggests that the consequences of disease may vary considerably among different pathogens and regions. Due to the long time-scales for coral dynamics, epizootics are expected to be prolonged with recovery slow at the regional scale. 4. Our model results show how infectious disease can substantially alter host metapopulation dynamics, with some non-linear relationships which are likely to affect the response of these systems to management and environmental change. For example, higher rates of coral colonization can have variable consequences for host population occupancy (i.e. coral cover) when infectious disease is considered, and chronic diseases with long-lived pathogens pose the highest risks for regional coral extinction. 5. Synthesis and applications. We present a tractable epidemiological model within a metapopulation framework and compare the model output with empirical data for a white plague type II (WPII) outbreak among coral of the upper Florida Keys. We conclude that this model fits well with the spatial and temporal patterns of WPII over a decade. Despite terrestrial-marine differences, many patterns derived from our model are consistent with epidemiological principles. Thus, the careful application of these principles within the context of marine management may be a promising research frontier. Although we focus on coral disease, the methods and results may apply to other marine metapopulations.

Research paper thumbnail of Spatial Epidemiology of Caribbean Yellow Band Syndrome in Montastrea spp. Coral in the Eastern Yucatan, Mexico

Hydrobiologia, 2005

Caribbean yellow band syndrome (YBS) is a poorly understood, progressively fatal disease primaril... more Caribbean yellow band syndrome (YBS) is a poorly understood, progressively fatal disease primarily affecting Montastraea spp. coral. This disease has exhibited rapid spread throughout the entire Caribbean over the last few decades. In this study, geographical information systems (GIS) and spatial statistics were used to analyze the distribution of YBS in Akumal Bay, Mexico, and host and environmental risk factors for YBS were evaluated epidemiologically. In this Bay, there are hundreds of colonies of Montastraea annularis from 1 m depths inside the fringing reefs to reef crests and beyond. Of 63 corals that were evaluated, the overall prevalence of YBS in Akumal Bay was 28.6%, with 35.7% in large colonies, 23.8% in medium-sized colonies, and 23.8% in small colonies, where small colonies were <200 cm diameter, medium-sized were 200-500 cm, and large were >500 cm. Lesions covered 3.8% (±1.3 s.e.) of the surface of colonies assessed, compared with a mean percentage of dead colony cover of 54.4% (±4.2 s.e.). Analysis for spatial clustering documented that M. annularis colonies (well and sick) were highly spatially clustered, compared to expected complete spatial randomness. However, compared with all M. annularis corals, colonies with YBS tended to be less spatially clustered (i.e. within the overall clustered spatial distribution of M. annularis colonies, YBS-affected coloniesÕ distribution was more regular). These findings are consistent with several hypotheses for the etiology of YBS, including near-shore pathogens or toxins either directly inducing disease or indirectly leading to disease by increasing host susceptibility. Ongoing investigations into the management and cause of YBS can use this information to develop management strategies and more efficiently target future sampling.

Research paper thumbnail of Causal inference in disease ecology: investigating ecological drivers of disease emergence

Frontiers in Ecology and the Environment, 2008

Research paper thumbnail of Allometry and spatial scales of foraging in mammalian herbivores

Ecology Letters, 2010

Herbivores forage in spatially complex habitats. Due to allometry and scale-dependent foraging, h... more Herbivores forage in spatially complex habitats. Due to allometry and scale-dependent foraging, herbivores are hypothesized to perceive and respond to heterogeneity of resources at scales relative to their body sizes. This hypothesis has not been manipulatively tested for animals with only moderate differences in body size and similar food niches. We compared short-term spatial foraging behavior of two herbivores (sheep and cattle) with similar dietary niche but differing body size. Although intake rates scaled allometrically with body mass (mass 0.75 ), spatial foraging strategies substantially differed, with cattle exhibiting a coarser-grained use of the Ôfoodscape.Õ Selectivity by cattle (and not sheep) for their preferred food was more restricted when patches were smaller (< 10 m 2 ). We conclude that differences in spatial scales of selection offers a plausible mechanism by which species can coexist on shared resources that exhibit multiple scales of spatial heterogeneity.

Research paper thumbnail of Ecology of avian influenza viruses in a changing world

Annals of the New York Academy of Sciences, 2010

Influenza A virus infections result in ∼500,000 human deaths per year and many more sublethal inf... more Influenza A virus infections result in ∼500,000 human deaths per year and many more sublethal infections. Wild birds are recognized as the ancestral host of influenza A viruses, and avian viruses have contributed genetic material to most human viruses, including subtypes H5N1 and H1N1. Thus, influenza virus transmission in wild and domestic animals and humans is intimately connected. Here we review how anthropogenic change, including human population growth, land use, climate change, globalization of trade, agricultural intensification, and changes in vaccine technology may alter the evolution and transmission of influenza viruses. Evidence suggests that viral transmission in domestic poultry, spillover to other domestic animals, wild birds and humans, and the potential for subsequent pandemic spread, are all increasing. We highlight four areas in need of research: drivers of viral subtype dynamics; ecological and evolutionary determinants of transmissibility and virulence in birds and humans; the impact of changing land use and climate on hosts, viruses, and transmission; and the impact of influenza viruses on wild bird hosts, including their ability to migrate while shedding virus.

Research paper thumbnail of Epidemiologic evaluation of diarrhea in dogs in an animal shelter

American Journal of Veterinary Research, 2005

Research paper thumbnail of Regulation of laboratory populations of snails (Biomphalaria and Bulinus spp.) by river prawns, Macrobrachium spp. (Decapoda, Palaemonidae): Implications for control of schistosomiasis

Acta Tropica, 2014

Human schistosomiasis is a common parasitic disease endemic in many tropical and subtropical coun... more Human schistosomiasis is a common parasitic disease endemic in many tropical and subtropical countries. One barrier to achieving long-term control of this disease has been re-infection of treated patients when they swim, bathe, or wade in surface fresh water infested with snails that harbor and release larval parasites. Because some snail species are obligate intermediate hosts of schistosome parasites, removing snails may reduce parasitic larvae in the water, reducing re-infection risk. Here, we evaluate the potential for snail control by predatory freshwater prawns, Macrobrachium rosenbergii and M. vollenhovenii, native to Asia and Africa, respectively. Both prawn species are high value, protein-rich human food commodities, suggesting their cultivation may be beneficial in resource-poor settings where few other disease control options exist. In a series of predation trials in laboratory aquaria, we found both species to be voracious predators of schistosome-susceptible snails, hatchlings, and eggs, even in the presence of alternative food, with sustained average consumption rates of 12% of their body weight per day. Prawns showed a weak preference for Bulinus truncatus over Biomphalaria glabrata snails. Consumption rates were highly predictable based on the ratio of prawn: snail body mass, suggesting satiation-limited predation. Even the smallest prawns tested (0.5-2 g) caused snail recruitment failure, despite high snail fecundity. With the World Health Organization turning attention toward schistosomiasis elimination, native prawn cultivation may be a viable snail control strategy that offers a win-win for public health and economic development.

Research paper thumbnail of Nearly 400 million people are at higher risk of schistosomiasis because dams block the migration of snail-eating river prawns

Cite this article: Sokolow SH et al. 2017