Deforestation alters spillover risk of multi-host pathogens

Annalise Cramer, a student at Westfield State University, worked in the lab of Dr. Richard Hall

Abstract Deforestation alters landscape configuration resulting in novel contacts between host species, which can promote pathogen spillover from wildlife to domesticated animals and humans. Given heightened awareness of zoonotic spillover, studies are urgently needed to understand how the rate of deforestation interacts with host abundance and distribution to shape pathogen transmission across habitats and human exposure risk. In this study, we derive a mathematical model coupling land use change with pathogen transmission between hosts in forested and deforested habitats. We explore how deforestation rate and host relative abundance across habitats influence the dynamics, peak and cumulative number of infected hosts in deforested habitats as a proxy for human spillover risk. We find that the number of infected hosts in deforested habitats peaks sooner under faster deforestation rates. When the deforested hosts are less abundant, most transmission occurs in mixtures of forested and deforested habitats where large habitat boundaries maximize contacts with the more abundant forest hosts. This results in a hump-shaped relationship between deforestation rate and short- and long-term spillover risk. These results suggest that surveillance and interventions at habitat boundaries are crucial to reduce the risk of zoonotic spillover.


Extreme heat reduces fitness of monarchs and their parasites

Maya Sarkar, a student at the University of Minnesota, worked with Isabella Ragonese, Dr. Sonia Altizer and Dr. Richard Hall.

Abstract: It is important to understand the consequences of a warming climate, especially in organisms that are more sensitive to temperature changes and where the outcome of warming may not be intuitive. This project used the Monarch-OE system to study how temperature may affect host-parasite interactions. The monarch butterfly (Danaus plexippus) is an iconic North American migratory species and the specialist protozoan parasite OE (Ophryocystis elektroscirrha) is present in all monarch populations. It has been shown that monarch development proceeds faster with increasing temperatures and that increased temperature exposure lowers OE spore infectivity over time. However, the effect of temperature on the host and parasite during active infection is not known. This project examined how temperature affects the monarch-OE system, focusing on the interaction between monarch immune function and parasite replication. Monarchs were inoculated with strains of OE parasite and placed in different temperature treatments. Three lineages (B,F, and D) of migratory monarch were used to test genetic effects, while 2 spore lines (E3 and E10) were used to study virulence effects within 5 different temperature treatments (18, 22, 26, 30, and 34°C). The results of this study provide novel insight to how extreme temperatures affect the fitness of a host and its parasite.


Behavioral and environmental determinants of parasite transmission in a butterfly host

Chastity Ward, a senior from Fayetteville State University, worked on a project with Dr. Sonia Altizer, Dr. Richard Hall and Dr. Paola Barriga to examine how parasites of the Monarch butterfly are transmitted.

Abstract:  Many pathogens can be transmitted when infectious stages shed into the environment are later encountered by susceptible hosts. Environmental transmission is common among insect parasites, and also occurs for human diseases such as cholera and polio. Understanding how host behavior and environmental variables affect the shedding of infectious stages is crucial for predicting patterns of infection risk. Monarch butterflies Danaus plexippus are commonly infected by the protozoan Ophryocystis elektroscirrha (OE); this parasite is transmitted environmentally when infected adults deposit spores onto host plants (milkweed) that are consumed by monarch larvae. To quantify host contact with milkweeds as an estimate of parasite transmission, we set up outdoor flight cages with adult monarchs and milkweed plants. Cages varied in the number of adult monarchs and milkweed plants, and were assigned to one of two milkweed species. We used captive-raised monarchs from several genetic lineages, and marked the monarchs with unique number and color codes to track activity. We observed cages for replicate intervals over a week-long period, during which we noted observed monarch contacts with plants, and recorded monarch and plant identity, activity type, temperature, weather, and time of day. Our results showed strong heterogeneity in plant visitation rates among monarchs that was best explained by monarch sex (females had 4.7 times higher visitation rates than males, owing to frequent oviposition on milkweeds).  We also found wide variation among individual plants in the number of visits by monarchs. Milkweed species, plant flowering status and plant leaf number did not affect visitation rates, but plants in cages with a higher number of monarchs were visited more frequently. In sum, our findings provided evidence for individual monarch’s serving as superspreaders of infection, and for some milkweed plants serving as hotspots of infection. This study provides a starting point for estimating environmental parasite transmission in wild milkweed patches, and suggests that individual-level heterogeneity might be more important than environmental variation in driving parasite transmission in this system.


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Diet, Dispersal, and Disease: How Food Supplemented Habitat Alters Metapopulation Disease Spread

Celine Snedden, a Mathematics major at the University of California Berkeley, worked with Drs. Richard Hall and Sonia Altizer to look at how supplemental feeding of wildlife can affect disease spread.

Abstract: Recreational and unintentional feeding of wildlife occurs frequently but can have negative consequences, such as increasing pathogen transmission within provisioned sites. However, it is unclear how resource supplementation influences the spatial spread of pathogens. Provisioning could increase pathogen spread if the corresponding sites produce more offspring with higher dispersal success; alternatively, supplementation might reduce pathogen spread if provisioned sites promote site fidelity. Infection may also affect spatial dynamics by reducing wildlife mobility. In this project, we extend the Levins metapopulation model to account for heterogeneity in colonization rates caused by provisioning-induced changes to patch attractiveness, animal site fidelity, and infection-induced costs to movement. We derive two key parameters, the net effect of provisioning on movement (ρ) and the pathogen basic reproductive number (R0) that are crucial determinants of host occupancy and pathogen prevalence. We also explore how increasing the number of provisioned patches across the landscape influences host occupancy and pathogen prevalence under different supplementation scenarios. We find that provisioning should be avoided when infection has only small effects on animal mobility and when supplementation increases net movement of hosts between patches. However, provisioning can be beneficial to hosts when (i) infected patches produce fewer dispersers or when (ii) highly transmissible pathogens are present and supplemental feeding promotes site fidelity. To improve the effects of supplemental feeding on wildlife and decrease the risk of pathogen spillover, future work should aim to obtain empirical estimates of the effects of infection and resource provisioning on animal movement.


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Behavioral determinants of parasite transmission in a monarch (Danaus plexippus) population

Anna Schneider, a student from the University of Wisconsin-Stevens Point, worked with mentors Dr. Sonia Altizer, Dr. Richard Hall, and Ania Majewska to look at how butterfly behavior affects parasite transmission.

Abstract: Altered behavior of an infected host can have important consequences for pathogen transmission. Pathogens can cause the host to increase foraging behavior and decrease activity levels due to increased energetic demands, which can significantly change the spread of the pathogen. Monarchs can suffer from a debilitating protozoan parasite, Ophryocystis elektroscirrha (OE), which is transmitted when infected adults inadvertently shed spores on milkweed (Asclepias spp.) leaves that are subsequently consumed by the caterpillars.  While infected adults are known to experience reduced flight ability and survival, less is known about how infection influences milkweed visitation behavior and, therefore, spore deposition.  Here, we investigated whether infection status altered activity budgets of wild adult Monarchs, particularly visitation rates to milkweed for foraging or oviposition.  Behavioral observations and milkweed visitation rates of adult Monarchs, both infected and uninfected, were collected in the butterfly gardens at the Wormsloe Historic Site in Savannah, GA.  Our results concluded that sex, not infection status, showed significance in variation of behavior.  Milkweed visitation rates were higher than previously thought and these are critical for parasite persistence.  These data provide the first field estimates of parasite spore deposition rates in monarchs.  We modified an existing differential equation model of monarch-OE dynamics to include adults contaminated with OE spores through mating and milkweed visitation.  According to this model, late-season OE prevalence varied between 16.5 and 78.6%.  This is consistent with the wide range of OE prevalence recorded in US monarchs (6-20% in the Midwest, up to 100% in tropical milkweed patches in the Southeast).

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Spore persistence in the environment drives infection dynamics of a butterfly pathogen

Mary-Kate Williams, from the University of Arkansas at Little Rock, examined parasites of Monarch butterflies with Dr. Sonia Altizer, Dr. Richard Hall and graduate student Dara Satterfield.

Mary-Kate Williams1, Sonia Altizer2, Richard Hall2, Dara Satterfield2

1University of Arkansas at Little Rock, 2Odum School of Ecology, University of Georgia

Environmentally transmitted parasites commonly infect humans and wildlife. Environmental transmission is particularly important for insect pathogens, yet the factors affecting the persistence of infectious stages in the environment are poorly understood. Monarch butterflies are commonly infected by Ophryocystis elektroschirrha (OE); recent years have seen an increase in pathogen prevalence at the same time monarch populations in eastern North America have declined. OE is transmitted both vertically (from infected females to their progeny) and environmentally (when infected adults scatter spores onto milkweed leaves that are consumed by unrelated larvae). By using a combination of a mathematical modeling and an experimental study, we examined (1) how environmental conditions affect persistence of a free-living stage pathogen and (2) how pathogen shedding rate and environmental persistence time affect pathogen prevalence and host population size during the summer breeding season. We found that increased time spent fully exposed to environmental conditions (sun, rain, heat) reduced average infection severity induced by parasites, but did not reduce the fraction of monarchs infected by spores; therefore, parasites were able to remain viable after 15 days outdoors. Consistent with the experimental results, modeling findings showed that, parasite spores must persist for at least 20 days, in combination with a high shedding rate onto host plant leaves, for predicted prevalence to match the minimum prevalence observed in prior field studies.

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