by
Amanda M Koltz;
David Civitello;
Daniel J Becker;
Sharon L Deem;
Aimée T Classen;
Brandon Barton;
Maris Brenn-White;
Zoë E Johnson;
Susan Kutz;
Matthew Malishev;
Daniel L Preston;
J Trevor Vannatta;
Rachel M Penczykowski;
Vanessa O Ezenwa
Parasitic infections are common, but how they shape ecosystem-level processes is understudied. Using a mathematical model and meta-analysis, we explored the potential for helminth parasites to trigger trophic cascades through lethal and sublethal effects imposed on herbivorous ruminant hosts after infection. First, using the model, we linked negative effects of parasitic infection on host survival, fecundity, and feeding rate to host and producer biomass. Our model, parameterized with data from a well-documented producer–caribou–helminth system, reveals that even moderate impacts of parasites on host survival, fecundity, or feeding rate can have cascading effects on ruminant host and producer biomass. Second, using meta-analysis, we investigated the links between helminth infections and traits of free-living ruminant hosts in nature. We found that helminth infections tend to exert negative but sublethal effects on ruminant hosts. Specifically, infection significantly reduces host feeding rates, body mass, and body condition but has weak and highly variable effects on survival and fecundity. Together, these findings suggest that while helminth parasites can trigger trophic cascades through multiple mechanisms, overlooked sublethal effects on nonreproductive traits likely dominate their impacts on ecosystems. In particular, by reducing ruminant herbivory, pervasive helminth infections may contribute to a greener world.
by
David Civitello;
Teckla Angelo;
Karena H. Nguyen;
Rachel B. Hartman;
Naima C. Starkloff;
Moses P. Mahalila;
Jenitha Charles;
Andres Manrique;
Bryan K. Delius;
L. M. Bradley;
Roger M. Nisbet;
Safari Kinung hi;
Jason R. Rohr
Predicting and disrupting transmission of human parasites from wildlife hosts or vectors remains challenging because ecological interactions can influence their epidemiological traits. Human schistosomes, parasitic flatworms that cycle between freshwater snails and humans, typify this challenge. Human exposure risk, given water contact, is driven by the production of free-living cercariae by snail populations. Conventional epidemiological models and management focus on the density of infected snails under the assumption that all snails are equally infectious. However, individual-level experiments contradict this assumption, showing increased production of schistosome cercariae with greater access to food resources.
We built bioenergetics theory to predict how resource competition among snails drives the temporal dynamics of transmission potential to humans and tested these predictions with experimental epidemics and demonstrated consistency with field observations. This resource-explicit approach predicted an intense pulse of transmission potential when snail populations grow from low densities, i.e., when per capita access to resources is greatest, due to the resource-dependence of cercarial production. The experiment confirmed this prediction, identifying a strong effect of infected host size and the biomass of competitors on per capita cercarial production.
A field survey of 109 waterbodies also found that per capita cercarial production decreased as competitor biomass increased. Further quantification of snail densities, sizes, cercarial production, and resources in diverse transmission sites is needed to assess the epidemiological importance of resource competition and support snail-based disruption of schistosome transmission. More broadly, this work illustrates how resource competition can sever the correspondence between infectious host density and transmission potential.
Temperature constrains the transmission of many pathogens. Interventions that target temperature-sensitive life stages, such as vector controlmeasures that kill intermediate hosts, could shift the thermal optimum of transmission, thereby altering seasonal disease dynamics and rendering interventions less effective at certain times of the year and with global climate change. To test these hypotheses, we integrated an epidemiological model of schistosomiasis with empirically determined temperature-dependent traits of the human parasite Schistosoma mansoni and its intermediate snail host (Biomphalaria spp.). We show that transmission risk peaks at 21.7 °C (Topt), and simulated interventions targeting snails and free-living parasite larvae increased Toptby up to 1.3 °C because interventionrelated mortality overrode thermal constraints on transmission. This Toptshift suggests that snail control is more effective at lower temperatures, and global climate change will increase schistosomiasis risk in regions that move closer to Topt. Considering regional transmission phenologies and timing of interventions when local conditions approach Toptwill maximize human health outcomes.
by
Kathryn L. Schaber;
T. Alex Perkins;
Alun L. Lloyd;
Lance Waller;
Uriel Kitron;
Valerie A. Paz-Soldan;
John P. Elder;
Alan L. Rothman;
David Civitello;
William H. Elson;
Amy C. Morrison;
Thomas W. Scott;
Gonzalo M. Vazquez-Prokopec
Heterogeneous exposure to mosquitoes determines an individual’s contribution to vector-borne pathogen transmission. Particularly for dengue virus (DENV), there is a major difficulty in quantifying human-vector contacts due to the unknown coupled effect of key heterogeneities. To test the hypothesis that the reduction of human out-of-home mobility due to dengue illness will significantly influence population-level dynamics and the structure of DENV transmission chains, we extended an existing modeling framework to include social structure, disease-driven mobility reductions, and heterogeneous transmissibility from different infectious groups. Compared to a baseline model, naïve to human pre-symptomatic infectiousness and disease-driven mobility changes, a model including both parameters predicted an increase of 37% in the probability of a DENV outbreak occurring; a model including mobility change alone predicted a 15.5% increase compared to the baseline model.
At the individual level, models including mobility change led to a reduction of the importance of out-of-home onward transmission (R, the fraction of secondary cases predicted to be generated by an individual) by symptomatic individuals (up to -62%) at the expense of an increase in the relevance of their home (up to +40%). An individual’s positive contribution to R could be predicted by a GAM including a non-linear interaction between an individual’s biting suitability and the number of mosquitoes in their home (>10 mosquitoes and 0.6 individual attractiveness significantly increased R). We conclude that the complex fabric of social relationships and differential behavioral response to dengue illness cause the fraction of symptomatic DENV infections to concentrate transmission in specific locations, whereas asymptomatic carriers (including individuals in their pre-symptomatic period) move the virus throughout the landscape. Our findings point to the difficulty of focusing vector control interventions reactively on the home of symptomatic individuals, as this approach will fail to contain virus propagation by visitors to their house and asymptomatic carriers.
by
Neal T. Halstead;
Christopher M. Hoover;
Arathi Arakala;
David Civitello;
Giulio A. De Leo;
Manoj Gambhir;
Steve A. Johnson;
Nicolas Jouanard;
Kristin A. Loerns;
Taegan A. McMahon;
Raphael Ndione;
Karena Nguyen;
Thomas R. Raffel;
Justin V. Remais;
Gilles Riveau;
Susanne H. Sokolow;
Jason R. Rohr
Schistosomiasis is a snail-borne parasitic disease that ranks among the most important water-based diseases of humans in developing countries. Increased prevalence and spread of human schistosomiasis to non-endemic areas has been consistently linked with water resource management related to agricultural expansion. However, the role of agrochemical pollution in human schistosome transmission remains unexplored, despite strong evidence of agrochemicals increasing snail-borne diseases of wildlife and a projected 2- to 5-fold increase in global agrochemical use by 2050. Using a field mesocosm experiment, we show that environmentally relevant concentrations of fertilizer, a herbicide, and an insecticide, individually and as mixtures, increase densities of schistosome-infected snails by increasing the algae snails eat and decreasing densities of snail predators. Epidemiological models indicate that these agrochemical effects can increase transmission of schistosomes. Identifying agricultural practices or agrochemicals that minimize disease risk will be critical to meeting growing food demands while improving human wellbeing.
by
Vanessa O. Ezenwa;
David Civitello;
Brandon T. Barton;
Daniel J. Becker;
Maris Brenn-White;
Aimee T. Classen;
Sharon L. Deem;
Zoe E. Johnson;
Susan Kutz;
Matthew Malishev;
Rachel M. Penczykowski;
Daniel L. Preston;
J. Trevor Vannatta;
Amanda M. Koltz
Ruminant livestock are a significant contributor to global methane emissions. Infectious diseases have the potential to exacerbate these contributions by elevating methane outputs associated with animal production. With the increasing spread of many infectious diseases, the emergence of a vicious climate–livestock–disease cycle is a looming threat.
Wildlife vaccination is of urgent interest to reduce disease-induced extinction and zoonotic spillover events. However, several challenges complicate its application to wildlife. For example, vaccines rarely provide perfect immunity. While some protection may seem better than none, imperfect vaccination can present epidemiological, ecological, and evolutionary challenges. While anti-infection and antitransmission vaccines reduce parasite transmission, antidisease vaccines may undermine herd immunity, select for increased virulence, or promote spillover. These imperfections interact with ecological and logistical constraints that are magnified in wildlife, such as poor control and substantial trait variation within and among species. Ultimately, we recommend approaches such as trait-based vaccination, modeling tools, and methods to assess community- and ecosystem-level vaccine safety to address these concerns and bolster wildlife vaccination campaigns.
by
Christopher J. E. Haggerty;
Sidy Bakhoum;
David Civitello;
Giulio A. De Leo;
Nicolas Jouanard;
Raphael A. Ndione;
Justin Remais;
Gilles Riveau;
Simon Senghor;
Susanna H. Sokolow;
Souleymane Sow;
Caitlin Wolfe;
Chelsea l. Wood;
Isabel Jones;
Andrew J. Chamberlin;
Jason R. Rohr
Background
Schistosomiasis is responsible for the second highest burden of disease among neglected tropical diseases globally, with over 90 percent of cases occurring in African regions where drugs to treat the disease are only sporadically available. Additionally, human re-infection after treatment can be a problem where there are high numbers of infected snails in the environment. Recent experiments indicate that aquatic factors, including plants, nutrients, or predators, can influence snail abundance and parasite production within infected snails, both components of human risk. This study investigated how snail host abundance and release of cercariae (the free swimming stage infective to humans) varies at water access sites in an endemic region in Senegal, a setting where human schistosomiasis prevalence is among the highest globally.
Methods/Principal findings
We collected snail intermediate hosts at 15 random points stratified by three habitat types at 36 water access sites, and counted cercarial production by each snail after transfer to the laboratory on the same day. We found that aquatic vegetation was positively associated with per-capita cercarial release by snails, probably because macrophytes harbor periphyton resources that snails feed upon, and well-fed snails tend to produce more parasites. In contrast, the abundance of aquatic macroinvertebrate snail predators was negatively associated with per-capita cercarial release by snails, probably because of several potential sublethal effects on snails or snail infection, despite a positive association between snail predators and total snail numbers at a site, possibly due to shared habitat usage or prey tracking by the predators. Thus, complex bottom-up and top-down ecological effects in this region plausibly influence the snail shedding rate and thus, total local density of schistosome cercariae.
Conclusions/Significance
Our study suggests that aquatic macrophytes and snail predators can influence per-capita cercarial production and total abundance of snails. Thus, snail control efforts might benefit by targeting specific snail habitats where parasite production is greatest. In conclusion, a better understanding of top-down and bottom-up ecological factors that regulate densities of cercarial release by snails, rather than solely snail densities or snail infection prevalence, might facilitate improved schistosomiasis control.
by
Tierra Smiley Evans;
Zhengli Shi;
Michael Boots;
Wenjun Liu;
Kevin J. Olival;
Xiangming Xiao;
Sue Vandewoude;
Heidi Brown;
Ji-Long Chen;
David Civitello;
Luis Escobar;
Yrjo Grohn;
Hongying Li;
Karen Lips;
Qiyoung Liu;
Jiahai Lu;
Beatriz Martínez-López;
Jishu Shi;
Xiaolu Shi;
Biao Xu;
Lihong Yuan;
Guoqiang Zhu;
Wayne M. Getz
The risk of a zoonotic pandemic disease threatens hundreds of millions of people. Emerging infectious diseases also threaten livestock and wildlife populations around the world and can lead to devastating economic damages. China and the USA—due to their unparalleled resources, widespread engagement in activities driving emerging infectious diseases and national as well as geopolitical imperatives to contribute to global health security—play an essential role in our understanding of pandemic threats. Critical to efforts to mitigate risk is building upon existing investments in global capacity to develop training and research focused on the ecological factors driving infectious disease spillover from animals to humans.
International cooperation, particularly between China and the USA, is essential to fully engage the resources and scientific strengths necessary to add this ecological emphasis to the pandemic preparedness strategy. Here, we review the world’s current state of emerging infectious disease preparedness, the ecological and evolutionary knowledge needed to anticipate disease emergence, the roles that China and the USA currently play as sources and solutions to mitigating risk, and the next steps needed to better protect the global community from zoonotic disease.
by
Jason R. Rohr;
Christopher B. Barrett;
David Civitello;
Meggan E. Craft;
Bryan Delius;
Guilio A. DeLeo;
Peter J. Hudson;
Nicolas Jouanard;
Karena H. Nguyen;
Richard S. Ostfeld;
Justin Remais;
Gilles Riveau;
Susanne H. Sokolow;
David Tilman
Infectious diseases are emerging globally at an unprecedented rate while global food demand is projected to increase sharply by 2100. Here, we synthesize the pathways by which projected agricultural expansion and intensification will influence human infectious diseases and how human infectious diseases might likewise affect food production and distribution. Feeding 11 billion people will require substantial increases in crop and animal production that will expand agricultural use of antibiotics, water, pesticides and fertilizer, and contact rates between humans and both wild and domestic animals, all with consequences for the emergence and spread of infectious agents. Indeed, our synthesis of the literature suggests that, since 1940, agricultural drivers were associated with >25% of all — and >50% of zoonotic — infectious diseases that emerged in humans, proportions that will likely increase as agriculture expands and intensifies. We identify agricultural and disease management and policy actions, and additional research, needed to address the public health challenge posed by feeding 11 billion people.