Graduation Year

2014

Document Type

Dissertation

Degree

Ph.D.

Degree Granting Department

Biology (Integrative Biology)

Major Professor

Lynn B. Martin, Ph.D.

Committee Member

Jason R. Rohr, Ph.D.

Committee Member

Valerie J. Harwood, Ph.D.

Committee Member

Peter D. Stiling, Ph.D.

Keywords

coccidia, immune response, invasion, malaria, Passer domesticus

Abstract

Introduced species are the greatest threat to biodiversity after habitat loss. Understanding the processes that permit organisms to become successful invaders may provide opportunities to prevent or limit their dispersal and establishment and thereby alleviate some of their harmful effects. The goal of my dissertation research has been to investigate whether invasive species have distinctive interactions with parasites, and some of the mechanisms that may underlie that variation. I used one of the world's most successful vertebrate invaders as a case study: the house sparrow (Passer domesticus; Introduction).

Previous research in the house sparrow suggested that loss of parasite diversity may contribute to invasion success. However, my work demonstrates that infection with common avian malaria parasites is primarily a function of environmental heterogeneity and is not a predictor of time since introduction for house sparrows that are currently expanding their range in Kenya (Chapter 1). Interestingly, in spite of a large proportion of the population being infected with avian malaria, a state that should reduce competitive ability of house sparrow populations, this species is still able to establish themselves among native competitors. Though there are a number of potential mechanisms that could explain this pattern, one of the most convincing explanations is that house sparrows, and perhaps other introduced species, have adaptive differences in immunity.

As such, the findings of Chapter 1 inspired two studies in which my collaborators and I showed that house sparrows from two non-native populations seem capable of maintaining normal health, performance and behavior during immune challenge, a response often referred to as parasite tolerance. Specifically, in Chapter 2, we found that when Floridian house sparrows, established since ~1870, were challenged with synthetic pathogens that mimicked infection with a fungi, an RNA virus or Gram-negative bacteria, only individuals challenged by the synthetic bacteria showed measurable sickness behaviors and secretion of an inflammatory protein. In Chapter 3, we compared parasite tolerance in Kenyan house sparrows (introduced in ~2000) and a native congener, the grey-headed sparrow (P. griseus) to a common intestinal parasite of songbirds. We found that both species were tolerant in that they were able to maintain fat reserves, protein reserves and vertical flight ability during infection. However, house sparrows maintained burdens that were, on average, more than 10x those of grey-headed sparrows. Moreover, when examining nutrient allocation in the two species, house sparrows appeared to assimilate nutrients more efficiently than grey-headed sparrows and did not change how nutrients were allocated among immune and reproductive organs during experimental infection. Grey-headed sparrows, however, did shift nutrient allocation among immune and reproductive organs during experimental infection. Together, the larger nutrient pool and maintenance of nutrient allocation patterns in challenged house sparrows suggests that no physiological trade-offs occurred and that house sparrows experienced a lower cost of parasite exposure.

In the fourth Chapter, I explored why house sparrows had such high coccidia burdens in comparison to their congeners. We suspected burden was a function of the frequency of exposure to coccidia. Consequently, we explored heterogeneity in foraging preferences and other behaviors in Floridian house sparrows and their role in coccidia burden. As expected, we found that house sparrows did not avoid contaminated food. In fact, they ate contaminated and uncontaminated foods indiscriminately. What was surprising was a lack of correlation between burden and consumption of contaminated foods and all of the behaviors we monitored (i.e., aggression, activity, feeding rates and defecation frequency). Overall, these data suggest that house sparrows do not benefit from typical parasite-avoidance behaviors.

In sum, this dissertation research implies that house sparrows respond to parasite infection differently than many other known vertebrates, most likely in an effort to maximize efficient use of resources and, in so doing, augment competitive ability and invasion success.

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