Temperature impacts on an insect-parasite interaction

For insects, environmental temperature can influence their physiology, survival, activity patterns, and large-scale distribution. Shifts in temperature will have pervasive effects, not just on individual insect species, but also on their interactions with other organisms, notably, their parasites. Given that insects are important pollinators and vectors of disease, it is vital that we explore how temperature impacts insect-parasite interactions. Monarch butterflies are parasitized by a protozoan parasite, Ophryocystis elektroscirrha (OE), that can have negative effects on the insect’s survival, reproduction, and flight ability. Their iconic migration exposes the butterflies to a range of environmental temperatures over the course of several generations, making the monarch-OE system quite suitable for investigating how temperature impacts host susceptibility and parasite virulence. This project, aimed at quantifying elements of host and parasite fitness at different temperatures, will include controlled lab experiments and the development of a mathematical model of infection. The student will participate in experimental data collection/analysis, model design, and model parameterization. This project is suitable for students with interests in infectious disease ecology and conservation hoping to integrate experimental and modeling techniques.

Host laboratory: Sonia Altizer & Richard Hall; co-mentored by Isabella Ragonese (PhD student)
Type of project: A combination of Quantitative (computer-based) and Empirical (lab-based)

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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A protozoan parasite weakens the stress reaction of monarch butterflies

Jovani Raya, a student from Abaraham Baldwin Agricultural College, worked with Dr. Sonia Altizer and Dr. Andy Davis to study the effect of infection on the stress reaction of monarch butterflies.

Abstract:  The protozoan parasite Ophryocystis elektroscirrha (OE) affects the adult mortality, longevity, body size, and flight ability of monarch butterflies (Danaus plexippus). However, very little research on how the parasite influences the stress response in monarchs has been conducted. We examined the effects of parasite infection and larval rearing densities on the monarch stress response. Monarch larvae were inoculated with parasite spores and reared in low (2 larva) or high (10 larva) densities. When the monarch larvae reached pupation, we assessed their stress reactions. To produce the stress response in the pupae, physical disturbance was applied for 20 seconds. After the disturbance, the pupa was placed on a device that detects movement within animal tissue and can record the movements of the heartbeat. This recording allowed us to count the number of beats per minute. The result showed that infection was a significant predictor of the magnitude and duration of pupa HR; infected monarchs had lower reactions. Lower reactions would negatively affect how well infected monarchs could cope with daily stressors, especially during the arduous fall migration.

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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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Effects of temperature on larval immunity

2013 student Kaela Caballero worked with Professor Sonia Altizer and graduate student Alexa Fritzsche to investigate the effect of temperature on immunity to parasites in monarch butterfly larvae.

 

Abstract

Recent studies indicate that environmental factors, particularly temperature, can affect the outcome of host-parasite interactions, with implications for predicting pathogen responses and parasite development to future climate change. In this study, we experimentally tested how ambient temperature affects both immunity and parasite infection focusing on monarch butterflies (Danaus plexippus) and a common protozoan parasite, Ophryocystis elektroscirrha (OE). Monarchs become infected as larvae when they eat milkweed plants covered in OE. Each year, populations of monarchs in eastern North America migrate from as far north as Canada to overwintering colonies in Mexico. Monarchs encounter a wide range of temperatures over the course of migration. For this reason, monarchs are an exemplary system for identifying relationships between temperature and immune defense. In this experiment, we explore the response of two measures of innate immune defense – phenoloxidase (PO) activity and the concentration of haemocytes in monarch larvae reared across a gradient of four temperatures: 23o C, 26oC, 29oC, 32oC. These temperatures represent a range normally experienced by monarchs during the summer months. Both PO activity and haemocytes are relevant indicators of immune competence and pathogen defense in a number of insect species. At the second instar stage, we placed 25 larvae into each of the four temperature treatments. At the fifth instar stage, we weighed and bled larvae for immune assays. We also measured the outcome of parasite infection for monarch larvae experimentally inoculated with OE and reared under the same temperature treatments. Warmer temperatures are known to accelerate growth and development in a linear fashion for a variety of insect species, but previous studies have indicated that rising temperatures are not positively correlated with improved immune competence. We hypothesized that both haemocyte concentrations and PO activity would be highest at intermediate temperatures, and would decrease with both cool and very warm temperatures, as has been shown for some other insect species. We also predicted that the severity of OE infections would be lowest at intermediate temperatures, corresponding to greater resistance of the monarchs. Our initial results reveal that haemocytes were greatest at 29oC, but decrease at both warmer and cooler temperatures implicating that some components of immunity perform best at intermediate temperatures.

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