Exploring Effects of Abiotic and Biotic Environmental Factors in the Human Malaria System

Mosquitoes are the deadliest organism in the world, taking out approximately 725,000 people annually due to the infectious organisms they transmit to humans. The principle pathogen that contributes the most human mortality is the human malaria parasite. The transmission of malaria parasites is linked inextricably to the biology of the mosquito vector and occurs in environments where mosquitoes and parasites are exposed to a suite of biotic and abiotic factors that vary considerably over time and space. In order to better understand the net outcome of the mosquito-parasite interaction in the field, and better predict the likely performance of mosquito control tools, it is necessary to begin to consider environmental context. For example, it could be that environmental factors play a small role, simply adding ‘noise’ to the system. Alternatively, environmental factors might massively shape the outcome of vector-parasite interactions and dominate the effectiveness of novel control tools. We are interested in an REU student that is willing to combine both empirical work in the lab with computational approaches to assess the relative influence of key environmental factors (e.g. temperature, relative humidity, mosquito microbiota) on mosquito life history traits and parasite traits relevant for predicting transmission. Example projects that could be developed include the effect of microbiota and relative humidity on mosquito life history traits and transmission or the role of transgenerational imprinting of environmental cues on these traits. This work will occur in the Indian malaria mosquito (Anopheles stephensi) and human malaria (Plasmodium falciparum) system. This student will be mentored by Drs. Ash Pathak (Infectious Diseases) and Courtney Murdock (Infectious Diseases & Odum School of Ecology).

Host Laboratory: Courtney Murdock, mentored by Ash Pathak
Type of Project: Combination of Empirical/Laboratory-based and Quantitative/Computer-based


Exploring links between mosquitoes, the environment, and disease transmission

The Asian tiger mosquito, Aedes albopictus is one of the most highly invasive mosquito species seen to date.  The physiological and ecological plasticity of Ae. albopictus has led to its rapid global expansion.  Additionally, its ability to vector a wide-range of recently emerging arboviruses, such as dengue and Chikungunya, make it a significant public health threat.  The transmission of many mosquito-borne pathogens is strongly influenced by environmental temperature due to effects on the physiology of the insect vector and the pathogen.  Therefore, changes in local environmental conditions could significantly impact the distributions and dynamics of a range of mosquito-borne diseases.  Predicting the extent of possible changes in disease dynamics will require a detailed understanding of how a suite of mosquito-pathogen traits respond to variation in environmental temperature and other biotic factors. Projects can explore the following potential questions: 1) what are the microclimate conditions mosquitoes experience in the larval environment and relevant transmission settings?, 2) how does thermal variation influence mosquito life history traits relevant for transmission (e.g. larval development rates, larval survival, adult longevity)?, 3) can we use remotely sensed data to predict relevant mosquito microclimate?, or 4) what factors contribute to Ae. albopictus oviposition behavior and density-dependence in the larval environment. We are looking for two REU students that are interested in combining field work with computational approaches to carry out projects in the Athen’s system this summer mentored by Drs. Courtney Murdock (Infectious Diseases & Odum School of Ecology) and Craig Osenberg (Odum School of Ecology).

Host Laboratories: Courtney Murdock and Craig Osenberg
Type of Project: Combination of Empirical/Field-based, and Computational/Computer-based

What’s the buzz? An investigation on how urbanization impacts mosquito species distribution

Lilith South, a junior from the University of Georgia, worked with Mike Newberry in the lab of Dr. Courtney Murdock to study the relationship between urbanization and distribution of mosquito species.

Abstract:   Impervious surfaces, mainly paved roads and buildings, significantly impact microclimate by making an area hotter and less humid. For this reason, urban areas are warmer than less developed rural areas. Heat associated with high impervious surface coverage impacts mosquito development and decreases larval survival in Aedes albopictus. Although many species of mosquitoes are present in Athens, Georgia, the most prominent species and most important species for human health, Ae. albopictus, is one of few species that dominate the area. Ae. albopictus has shown potential vectoral capacity for diseases such as Zika, Dengue, and Chikungunya. Fortunately, it does not yet transmit these diseases in the south eastern United States, but with changing climate and urbanization these diseases have potential to spread. The impact that impervious surface coverage has on mosquito community composition was not previously known. To investigate this effect, sites were classified and selected by their impervious surface coverage. Rural sites had impervious surface coverage ranging from 0-5%, suburban had 5-55%, and urban had 55-100% coverage.  Larval samples from each site were identified to species and the proportion of occupied habitats for each species in each site was noted. Overall, species richness decreased in suburban and urban areas with higher impervious surface coverage. Diversity was highest and there was a more even spread of species in rural areas. Contrary to what was expected, the percentage of Ae. albopictus occupied habitats did not significantly change with impervious surface coverage. Although previous studies suggest that Ae. albopictus is sensitive to hotter urban areas, this species may be more resilient than other mosquito species to the effects of urbanization. Knowing how urbanization impacts mosquito community composition can help researchers better understand disease transmittance and develop solutions for potential viral outbreaks.

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How does the proportion of sugar fed Aedes albopictus mosquitoes vary across land use?

Alyssa Slicko, a junior from the University of Arkansas Little Rock, worked with Nikki Solano in the lab of Dr. Courtney Murdock to look at sugar-feeding and its relationship to land use in an invasive mosquito.

Abstract:  The Asian tiger mosquito, Aedes albopictus, is a non-native species to North America and is known to be highly invasive with an ability to vector up to 27 different arboviruses. Since female mosquitoes feed on both sugar and blood to survive, understanding the tendencies for sugar feeding could explain the differences in the abundance of invasive mosquito populations. Past studies have shown that temperature plays an important role in the distribution of vector borne diseases, but it has not been discovered whether other environmental factors such as sugar availability is a limiting resource for mosquito populations. Some species have evolutionarily adapted to low sugar resources, meaning they primarily feed on blood. However, little is known about the sugar feeding habits of Aedes albopictus. We collected A. albopictus from nine field sites classified as suburban, urban and rural based on percentage of impervious surface. A backpack aspirator was used to collect mosquitoes that were then frozen and identified by sex and species. A total of 90 female A. albopictus mosquitoes were collected, 30 from each land use type. Using homogenized solution of each individual mosquito, colorimetric sugar assays were performed with serial dilutions to determine relative sugar content per mosquito. The absorbance values of these solution were read through a spectrophotometer. At the 1:4 dilution values, urban sites have the greatest overall amount of sugar followed by rural and suburban land uses. There is evidence that mosquitoes in Aedes albopictus females do sugar-feed and that there are differences between sugar contents across land use types. However, a negative relationship was found between absorbance and concentration values across sites. This could be due to a potential chemical inhibitor formed with highly concentrated mosquito dilutions not allowing complete reading of absorbance values and determination of sugar content.

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How does overall population density and temperature affect the fecundity of female Aedes aegypti mosquitoes?

Lindsey Jones, a student from Albany State University, worked with Michelle Evans in the lab of Dr. Courtney Murdock to look at fecundity of a mosquito vector species.

Abstract:  Dynamics of mosquito-borne diseases such as Zika, yellow fever, chikungunya, and dengue depend on the ecology of both the disease and vector. Past studies have shown that both abiotic and biotic factors, such as temperature and population density, influence mosquito population dynamics, but the relationship of their interaction is unknown. Here, we explore how abiotic and biotic factors interact to influence life history traits of the Aedes aegypti mosquito. Specifically, we explored how intra- and inter-specific population densities and environmental temperature affect the fecundity of female Ae. aegypti mosquitoes. We used a factorial design of twelve density and four temperature treatments, for a total of 48 treatments in this experiment. We reared 1st instar Ae. aegypti and An. stephensi larvae to adulthood in 250 mL RO water with 0.1 g Tetramin fish food in mason jars in Percival incubators. Following emergence, adult female Ae. aegypti mosquitoes were collected, blood fed, and individually placed into centrifuge tubes at 28oC. We collected and recorded the number of eggs laid for each individual emerging per day to estimate the mosquito per capita growth rate. We found that Ae. aegypti fecundity increases with decreasing temperatures. We also found that fecundity decreases as the overall population density increases, along with the density of the competitor. As an interaction, temperature, overall density, and density of the competitor, affected fecundity, suggesting the effects of biotic factors could quantitatively and qualitatively vary across different thermal environments. We found that the population growth rate of Ae. aegypti decreased with increasing density and decreasing temperatures. These results highlight the complexity of how environmental factors can shape disease transmission.

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The effects of land use and larval density on Aedes albopictus population dynamics

Carl Hintz, a student from North Carolina State University, worked with Emily Cook in the lab of Dr. Courtney Murdock to examine mosquito larvae dynamics.

Abstract:  The Asian Tiger Mosquito, Aedes albopictus, is nonnative to North America and is a vector of Dengue virus (DENV) and Chikungunya virus (CHIKV) in humans.  Like most other mosquito species, A. albopictus larvae develop in small pools of stagnant water and adult A. albopictus typically disperse less than 100 meters. Due to this life history, fine-scale variation in microclimate and larval habitat may have a substantial impact on population characteristics.  We use a semi-field study to examine the impact of land use and larval density on traits that are relevant for the population dynamics of A. albopictus. We examine larval development and adult characteristics at nine field sites in Athens-Clarke County, GA.  Sites are classified as urban, suburban and rural based on amount of impervious surface. Mosquito development rate (MDR) and probability egg to adult survival (PEA) are determined from daily adult emergence. The number of eggs per females per day (EFD) is inferred from wing length data. A. albopictus at urban sites have lower survival, faster development, and smaller body size than those at rural or suburban sites. This difference may result from substantially higher mean temperatures at urban sites. High density replicates have lower survival, slower development, and smaller body size, possibly due to limited food resources. Compared with differences in land use, larval density has a larger impact on A. albopictus population dynamics, but both factors have important consequences for mosquito population dynamics and could be incorporated to improve the accuracy of vector population models.

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Improving Temperature Specific Data Used to Determine Transmission Risk for Malaria

Temitayo Adanlawo, a Biology major from Howard University, worked with Kerri Miazgowicz in the lab of Dr. Courtney Murdock to study an important disease vector.

Abstract: Malaria is a disease endemic to sub-Saharan Africa, India, southeast Asia and parts of Central and South America, and affects 300-600 million people every year. Malaria is a temperature-sensitive disease that varies between species. Currently, there is a disconnect between malaria transmission risk models and actual malaria incidence. This is due to species temperature-specific data substitution which increases uncertainty in results for the transmission risk equation (R0). In order to increase the accuracy of the temperature-dependent malaria transmission risk equation, a life table study was performed on Anopheles stephensi mosquitoes Using thirty mosquitoes at each of six different temperatures (16 °C, 20 °C, 24 °C, 28 °C, 32 °C, 36 °C), mortality, fecundity, and bite rate were recorded daily. Mosquitoes were given the opportunity to feed for fifteen minutes daily. We used the results of this study to create a thermal performance curve to determine a minimum, optimal, and maximum point for thermally-dependent malaria transmission risk and decrease overall malaria transmission risk uncertainty. Bite rate increased with temperature, as did fecundity. We concluded that the three variables study are, in fact, extremely temperature dependent and that mortality plays a huge role in the development of bite rate and fecundity.

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Microclimate affects mosquito body size

Nicole Solano, a dance and biology major from Agnes Scott College,  worked with Michelle Evans in the lab of Dr. Courtney Murdock to examine the effects of temperature on mosquito life history traits.

Abstract: The Asian Tiger mosquito, Aedes albopictus, is an invasive mosquito vector that can transmit up to 27 different arboviruses. Since mosquitoes are small ectotherms, variations in temperature largely impact their physiology, development, and potential to transmit human pathogens. Small changes due to microclimate significantly impact mosquito life history traits relevant for transmission (i.e. body size). Body size is an indicator of fecundity, population growth, and mosquito immunity; therefore understanding the effect of microclimate can inform small-scale variation in disease transmission. Last summer, a study was conducted to test the relationship between microclimate and body size in a semi-field system. They found that mosquitoes in urban sites were significantly smaller than those in rural sites; most likely due to warmer temperatures in urban sites.  To validate these findings in the field, we conducted field mosquito surveys and quantified Ae. albopictus wing length across land use.


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Microclimate effects on Aedes albopictus mosquitoes

Taylor McClanahan, a student at the University of Arkansas at Little Rock, worked with Dr. Courtney Murdock and members of her lab to examine how microclimate affects mosquitoes.

Abstract: Aedes albopictus, (Asian tiger mosquito), has successfully colonized in several countries in North and South America. Ae. albopictus is a highly efficient vector, capable of transmitting at least 27 different arboviruses, and is contributing to the global expansion of both dengue and Chikungunya. However, whether or not dengue or Chikungunya will emerge in a given area will depend on its interaction with local mosquito populations and local environmental conditions. The aim of this study was to characterize variation in local climate conditions and how this variation impacts Ae. albopictus traits important for transmission. An impervious surface map of Athens-Clarke County was used to select three urban, suburban, and rural sites (30m2). Six pots were placed (>10 m apart) at each site in full shade, filled with 200 ml leaf infusion, seeded with 30 Ae. albopictus larvae, and paired with a data logger on the inside and outside of the pot. All pots were checked daily for emerging adults, and any adults present were counted and removed. Urban sites were characterized by the following: warmer daily mean and minimum temperatures, decreased daily diurnal temperature variation, earlier adult emergence, and lower numbers of emerging adults relative to suburban and rural sites. Further, weather station temperature data were not necessarily a good predictor of mosquito microclimate across the three land uses. This cautions against the use of downscaled global climate patterns in predicting how vector-borne diseases may respond to current and future climate change. Ultimately, we see that microclimate data generates a more precise representation of the environments these mosquitoes inhabit.

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