Malaria prevalence in invasive bird species versus the native Hawaiian bird species

Jeanette Calarco

Jeanette Calarco is a senior at the University of South Florida studying Microbiology. She is currently an undergraduate researcher in Dr. Loren Sackett's Ecology and Evolution of Infectious Diseases lab, where she is conducting research on the prevalence of malaria in native Hawaiian bird species versus nonnative bird species for her Honors thesis. She plans on pursuing a career in research on infectious diseases after obtaining a PhD in a related field. 

Introduction

Biological changes on a large scale often occur simultaneously with the discovery and colonization of land by humans. Introduced diseases are a type of biological change. The emergence of many infectious diseases can be attributed to the human transportation of vectors, pathogens, and infected invasive species into previously unexposed locations . These biological changes are typically destructive and result in the displacement of native species—including plants, animals, and humans .

Malaria, a widespread mosquito-borne disease, is found in multiple host systems. Plasmodium falciparum is one of four Plasmodium species that infects humans, typically in tropical countries with large mosquito populations. In 2015, there were an estimated 212 million malaria cases and as many as 429,000 malaria-related deaths in humans. In areas of high transmission, children under the age of 5 are more susceptible to both infection and death from malaria . Half of the world’s population lives in one of 106 countries and territories that are at risk of malaria transmission . Avian malaria has served as a model for studying various aspects of human malaria. Studies on the life cycle of Plasmodium—including the schizogonic and sporogonic reproductive stages—in birds, a vertebrate host, have been applied to other vertebrate systems including humans. In the shizogonic stage, asexual reproduction within the host’s red blood cells causes the blood cell to burst and infect other red blood cells. During this stage, the host can experience fevers characteristic to malaria. In the sporogonic stage, however, the parasite reproduces sexually and the host may not exhibit any symptoms. During this stage, the disease is transmitted to mosquitoes .

In addition to its utility as a model system for understanding human malaria, avian malaria is an important disease it its own right. Malaria parasites are the most well-studied of avian pathogens and are used to test various hypotheses, including those regarding host shifts that lead to emerging infectious diseases and pathogen range expansions in response to global climate change . Avian malaria is caused by several bird-specific Plasmodium species (most notably P. relictum) and infects tropical and subtropical avian species across the globe. Many species in the native range of malaria have evolved tolerance to the pathogen and do not exhibit fitness effects. However, avian malaria parasites have been introduced globally, and many species outside the native range of the parasite have no tolerance to this introduced pathogen .

Nowhere are the catastrophic effects of introduced malaria more evident than in Hawaii, where the destructive qualities of malaria and the naïveté of local species to the pathogen resulted in the avifauna losing nearly half of its total species to extinction . Between 6.4 and 8.1 million years ago, a sister taxon to Eurasian rosefinches (Carpodacus) migrated to the Hawaiian Islands and diverged into the first species of Hawaiian honeycreepers around 5.8 million years ago. This ancestral finch species radiated into more than 50 different species of Hawaiian honeycreepers, some of the most recent being the Hawaii and Maui amakihi, diverging 0.43 million years ago (Lerner, et al., 2011). Since then, at least 19 of the species have been eradicated, largely in part due to the introduction of malaria (van Riper, et al., 1986). In 2006, 53 of Hawaii’s 71 endemic avian taxa were either extinct or endangered . Mortality in introduced bird species due to malaria is negligible, whereas mortality in many endemic species can range from 50 to 100% .

Anthropogenic effects on the environment of Hawaii have both introduced and continue to evolve the novel mosquito-borne disease malaria. In the early 1800s, the commodity of oil extracted from whale blubber, used in oil lamps, made whaling both popular and profitable. In1826, the European whaling ship Wellington sailed from Mexico to the Hawaiian island of Maui with barrels of water containing mosquito larvae. Once arriving at the island, the crew replaced the water in the barrels with fresh water, dumping the mosquito-larvae into the rivers . The mosquitoes, Culex quinquefasciatus, found the coastal areas of Hawaii to be sufficiently tropical and quickly spread to the lowlands of all the major Hawaiian Islands.

The introduction of both the avian malaria parasite Plasmodium relictum and its primary vector resulted in a near total loss of Hawaiian honeycreeper populations in area of high mosquito density, including several extinctions. The remaining populations of surviving species became restricted to high elevations where the temperatures were too cold for mosquito vectors to survive. The sharp decline in native bird numbers resulting from the invasive disease indicated the lack of resistance or tolerance and higher susceptibility in naïve species . The non-native species are often tolerant to malaria and pose as carriers for the disease. In 1968, Warner found malarial infections in the house finch (Haemorhous mexicanus) and Japanese white-eye (Zosterops japonicus), but not in native species, suggesting that the non-native species are the reservoirs. Species that act as a reservoir for plasmodium can increase malaria infection rates within the regions that are inhabited by the mosquito vectors . The avifauna residing at lower elevations were forced to higher, mosquito-free elevations where they are less susceptible to malaria infection and death.

The reappearance and prevalence of residing and breeding Hawaii amakihi (Chlorodrepanis virens) in mosquito-dense elevations, as opposed to disease-free elevations, provides evidence that the bird species may have evolved resistance or tolerance to the disease . Experimental infections have demonstrated that amakihi survive with infection, lending support to the hypothesis that they have evolved tolerance rather than resistance (Atkinson et al. 2001, 2013).  

In further support of this idea, amakihi captured in natural populations in regions where malaria is transmittable are commonly infected with malaria. The prevalence of malaria in native species versus invasive species can be determined and further support an argument for evolved tolerance in amakihi, as well as indicate spatial differences in susceptibility.

In addition to the effects that anthropogenic introduction of non-native host species has on malaria in Hawaii, the consequences of climate change are also heavily impacting the outbreak of avian disease . Studies have calculated the temperature rise using the pre-industrial (<1850) reference point for global mean temperature change. The temperature increase between pre-industrial and the 1960-1990 mean was 0.3C, and the temperature increase between pre-industrial and 1990 was 0.6C (Warren, et al. 2011). As the climate warms in Hawaii, the range of mosquito populations is expanding upward in elevation. During the 1970s, an elevation limit of malaria of 1500 m was documented (van Riper, et al., 1986). In the last decade, prevalence of malaria in Hawaiian forest birds at 1900 m has more than doubled (Freed, et al., 2005). Coupled with the expansion in elevations mosquitoes are now able to populate, slim rises in ambient temperature and rainfall can extend the breeding season of mosquitoes, resulting in an increase in the time window of malaria transmission . Therefore, climate change can affect the prevalence of malaria by accelerating directly the reproduction of the Plasmodium parasite.

Literature Review

The introduction of novel diseases can heavily impact the widespread presence of avifauna within a region. However, because a suitable vector was not present, the disease could not be passed on to the native avian species . C. quinquefasciatus, the primary vector of avian malaria (Freed, et al., 2005), was accidentally introduced for the first time by Europeans on the ship Wellington. Because mosquito populations between the island of Hawaii and the remaining Hawaiian Islands are relatively isolated, multiple introductions of the vector likely occurred. Experimental data on the distribution of mitochondrial haplotypes combined with microsatellite information support this claim.

Despite the adequate tropical conditions, even in ideal epidemiological conditions, the population density of mosquitoes historically dropped drastically in elevations above 600 150 meters . In 1980, studies have shown that breeding populations of C. quinquefasciatus were present the entire year at elevations up to 1500m. More recently, breeding populations have been found in elevations up to 1900 m. It has also been noted that in elevations higher than 1100 m, pockets of undisturbed vegetation surrounded by relatively barren lava flows (kipukas) have oviposition sites for mosquitoes and vegetation providing both food and roosting sites for birds and mammal hosts .

With a present reservoir and a suitable vector, P. relictum quickly spread across wet lowland habitats in the Hawaiian Islands. In a study conducted by Warner (1968), Laysan finches, a species of Hawaiian honeycreeper, were separated into two groups of 13 birds each–a control group that was placed outside in a mosquito-proof enclosure, and an experimental group that was placed outside in an enclosure exposed to lowland mosquitoes. By the end of the 16th night, 100% of birds exposed to lowland mosquitoes had died, whereas 100% of the birds in the mosquito-proof enclosure had survived . Along with additional experiments on other honeycreeper species (Atkinson, et al., 2000, 2001, 2013), this work demonstrates the universal susceptibility of native honeycreepers to avian malaria, suggesting that the introduction of the invasive disease was the driving force behind the rapid species extinctions in the 20th century and the exceedingly high mortality rates of surviving Hawaiian honeycreeper species.

The population increases in lowland areas by amakihi could result either from the evolution of tolerance within these populations, or the eradication of low-elevation amakihi populations followed by the recolonization from high-elevation dispersing amakihi. Historically, the alleles in amakihi dwelling at higher elevations differentiated from amakihi in elevations below 1000 m. To determine whether the birds recolonizing the lowland areas are of the high-elevation or low-elevation populations, the genetic differentiation between the populations at low and high elevations were determined . The recolonization by remnant low-elevation populations would have evidence of unique local or private alleles among varying elevations as well as a bottleneck at low elevations. In contrast, the recolonization by high-elevation populations would show little genetic differentiation between amakihi at varying elevations . The study concluded that the amakihi at different elevations were highly differentiated genetically for both mtDNA and nuclear markers, suggesting that the low-elevation amakihi populations recolonized the lowland areas and that the evolution of tolerance was likely. The high level of genetic diversity maintained by the low-elevation population also suggests that the recolonized low-elevation populations arose from multiple remnant populations .

The susceptibility of host species to mosquitoes plays a large role in the malarial infectionrates of invasive species versus native species. Likeliness of infectivity can be influenced by behavioral characteristics such as sleeping habits. The Japanese White-eye sleeps with its bill and face tucked into its feathers, exposing fewer soft spots that are available to mosquito attacks. In opposition to this defended sleeping position, the Laysan Finches have their tarsi, corner of their bill, and feet open, leaving them more exposed to mosquito attack. Because the mosquitoes regularly feed during the night hours, the Laysan Finches are more susceptible to mosquito attacks . The likelihood of Laysan Finches to be attacked by mosquitoes was five to ten times higher than that of the Japanese White-eyes, making their projected malarial infection rates higher.

Discussion

Historically, many scientists had a notion that malaria was only present in low elevations. Since the initial observation that mosquitoes cannot exceed 600m , it has been observed in higher elevations of up to 1500m in 1980 and up to 1900m in 2005 . It is unknown how fast malaria is spreading and entering new areas and the role that climate change is playing in it. By researching the infection rates of native species versus non-native species, the spatial differences in susceptibility as well as the elevations at which malaria has been observed can be better understood.

While conservation efforts are actively being made by the people of Hawaii, evolution has also begun to play a role in the conservation of some species. Some native species have shown evidence of evolved tolerance to avian malaria . The evolution of tolerance in species of Hawaiian honeycreepers could prevent the eradication of the species due to malaria. Disease tolerance can be characterized as the ability of a host to tolerate a pathogen’s presence, typically by reducing the negative impact of infection on the host’s fitness .

According to Dr. Loren Sackett, an evolutionary biologist at the University of South Florida, “malaria is now present at all elevations on some islands, removing the birds’ ability to escape disease.” In this situation, it is forcing the birds to evolve a way to survive malaria or face the potential for extinction on that island. By researching the infection rates of native species versus non-native species, evidence further supporting the hypothesis that Hawaii amakihi are evolving tolerance to malaria can be found. In finding evidence to support this hypothesis, it could predict that more Hawaii amakihi and potentially other Hawaiian honeycreeper species will reemerge in low elevations and once again become a common sight for residents of Hawaii.

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