The Feeding Biology of the Tiger Mosquito, Aedes albopictus: Bridging Ecology and Behavior to Identify Drivers of Blood and Sugar Feeding Patterns
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Mosquitoes have shaped the natural world and human history through the pathogens that they transmit. Yet, despite millennia of cohabitation with these deadly insects, there is much that remains a mystery about them. In my dissertation, I seek to elucidate the complicated dynamics that drive mosquito feeding biology, including both blood and sugar feeding behavior and ecology. As my model organism to examine these questions, I worked with the tiger mosquito, Aedes albopictus, which can transmit over 20 different pathogens. The incredible invasive potential of Ae. albopictus has allowed it to establish throughout much of the world, leaving many people at risk of contracting disease. Its widespread threat to global health underscores the importance of researching the unanswered and under-studied aspects of its feeding biology critical to its vectorial capacity and life history. In my first chapter, I reviewed the mosquito blood feeding literature, highlighting the distinction between host preference (the innate tendency of a mosquito species to choose one host species or group over others) and feeding patterns (the host usage in the field, influenced by both preference and environmental factors). There are numerous ways to assess preference and feeding patterns, which I described alongside the potential biases that these methods may introduce. Finally, I used Ae. albopictus as a case study to scrutinize the interpretation of feeding patterns and host preference. It serves as an ideal example to demonstrate the limitations of the available data and common obstacles to accurate interpretation. A combination of inconsistency in the interpretation of blood meal analyses and a dearth of host preference research has resulted in conflicting descriptions of Ae. albopictus in the literature. The gaps in the literature identified in this chapter lay the foundation for the following two chapters. The second chapter describes the feeding patterns of Ae. albopictus in Long Island, New York, based on a blood meal analysis of mosquitoes collected across several farms and residential neighborhoods. Blood fed mosquito collections were conducted in tandem with two host availability measurements – household interviews and camera traps. These data were used to calculate two feeding metrics, forage ratios and host feeding indices, providing more context for feeding pattern results. I found that Ae. albopictus fed on ten host species in New York and that it under-utilized humans compared with dogs and cats according to both time and abundance-weighted host feeding indices. Forage ratios also revealed over-utilization of cats and opossums and under-utilization of birds, squirrels, and raccoons. Next, I conducted a life table analysis to assess the impact of host species on mosquito fitness to understand if certain host species provide a fitness advantage, which can serve as an evolutionary pressure to select for host preference. We fed New York Ae. albopictus blood from human, cat, opossum, horse, or rat and individually measured survival and fecundity. We then compared the fitness of Ae. albopictus from New York and Maryland, which have strikingly different feeding patterns, to assess whether differences in feeding patterns may be driven by differential impact of host species on fitness between the two populations. We did not find any major fitness differences by host species, indicating that underlying differences in fitness did not drive the observed feeding patterns. However, this finding did not rule out the possibility of variation in host preference between Ae. albopictus populations, which may exist between other populations in the world or between the populations studied here, but driven by different evolutionary forces. In chapter three, I directly assessed Ae. albopictus host preference. I included six populations from around the world, three with previously reported high levels of anthropophagy (human feeding) and three with low levels of anthropophagy, to assess the hypothesis that underlying differences in host preference drive the divergent feeding patterns. We used a dual-port olfactometer to present the mosquitoes with human and guinea pig odors and measured the host odor preference of each population. We compared the six Ae. albopictus populations to one another and to previously characterized anthropophilic and zoophilic Ae. aegypti colonies. We did not find differences in host preference between the Ae. albopictus populations, indicating that there is little variation for this trait and that the divergent feeding patterns were more likely the result of environmental factors, such as host availability. We also found that Ae. albopictus populations were less likely to choose human odor than the anthrophilic Ae. aegypti and behaved similarly to the zoophilic Ae. aegypti. This provided the first direct comparison of the host preference of these two vector species, which have overlapping ecologies and vector competencies. In the fourth and final chapter, we again investigated the feeding patterns of Ae. albopictus, but with a focus on sugar rather than blood. Male mosquitoes rely strictly on sugar sources for nutrition and energy, whereas female mosquitoes utilize sugar to supplement nutrition from blood meals. The sugar feeding behavior of Ae. albopictus is poorly characterized; prior to this chapter, only three studies had measured sugar feeding in the field. In this study, I used a cold anthrone assay to determine the presence and concentration of fructose in Ae. albopictus collected in Long Island. In tandem with these collections, we measured the temperature, humidity, and presence of flowers to understand the influence of these environmental parameters on sugar feeding. We collected both resting and host seeking mosquitoes, which provided information regarding the relationship between sugar feeding and host seeking in the field. We found that nearly half of Ae. albopictus were sugar fed and that each of the environmental and mosquito parameters that were measured had an impact on either the probability of sugar feeding or the concentration of fructose among sugar fed mosquitoes. Together, the chapters in my dissertation advance our understanding of Ae. albopictus feeding biology, which is critical to predicting whether this invasive species may serve as a vector for the numerous pathogens that it can transmit. The identification and exclusion of certain drivers of feeding patterns through these studies can provide insights into how to harness the blood and sugar feeding behaviors for Ae. albopictus vector control.
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McArt, Scott