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Avian malaria is a parasitic disease of birds, caused by parasite species belonging to the genera '' Plasmodium'' and '' Hemoproteus'' (phylum
Apicomplexa The Apicomplexa (also called Apicomplexia) are a large phylum of parasitic alveolates. Most of them possess a unique form of organelle that comprises a type of non-photosynthetic plastid called an apicoplast, and an apical complex structure. Th ...
, class Haemosporidia, family Plasmoiidae). The disease is transmitted by a dipteran vector including mosquitoes in the case of '' Plasmodium'' parasites and biting midges for ''Hemoproteus.'' The range of symptoms and effects of the parasite on its bird hosts is very wide, from asymptomatic cases to drastic population declines due to the disease, as is the case of the
Hawaiian honeycreeper Hawaiian honeycreepers are a group of small, passerine birds endemic to Hawaii. They are closely related to the rosefinches in the genus ''Carpodacus'', but many species have evolved features unlike those present in any other finch. Their great ...
s. The diversity of parasites is large, as it is estimated that there are approximately as many parasites as there are species of hosts. Co-speciation and host switching events have contributed to the broad range of hosts that these parasites can infect, causing avian malaria to be a widespread global disease, found everywhere except Antarctica.


Cause

Avian malaria is most notably caused by ''Plasmodium relictum'', a
protist A protist () is any eukaryotic organism (that is, an organism whose cells contain a cell nucleus) that is not an animal, plant, or fungus. While it is likely that protists share a common ancestor (the last eukaryotic common ancestor), the exclu ...
that infects birds in all parts of the world apart from Antarctica. There are several other
species In biology, a species is the basic unit of Taxonomy (biology), classification and a taxonomic rank of an organism, as well as a unit of biodiversity. A species is often defined as the largest group of organisms in which any two individuals of ...
of ''Plasmodium'' that infect birds, such as '' Plasmodium anasum'' and ''
Plasmodium gallinaceum ''Plasmodium gallinaceum'' is a species of the genus ''Plasmodium'' (subgenus ''Haemamoeba'') that causes malaria in poultry. Description This species was described by Alexandre Joseph Emile Brumpt (1877–1951) a French professor of parasit ...
'', but these are of less importance except, in occasional cases, for the poultry industry. The disease is found worldwide, with important exceptions. Usually, it does not kill birds. However, in areas where avian malaria is newly introduced, such as the islands of Hawaiʻi, it can be devastating to birds that have lost evolutionary resistance over time.


Parasite species

Avian malaria is a vector-transmitted disease caused by
protozoa Protozoa (singular: protozoan or protozoon; alternative plural: protozoans) are a group of single-celled eukaryotes, either free-living or parasitic, that feed on organic matter such as other microorganisms or organic tissues and debris. Histo ...
in the genera '' Plasmodium'' and ''
Haemoproteus ''Haemoproteus'' is a genus of alveolates that are parasitic in birds, reptiles and amphibians. Its name is derived from Greek: ''Haima'', "blood", and ''Proteus'', a sea god who had the power of assuming different shapes. The name ''Haemoproteu ...
''; these parasites reproduce asexually within bird hosts and both asexually and sexually within their insect vectors, which include mosquitoes (
Culicidae Mosquitoes (or mosquitos) are members of a group of almost 3,600 species of small flies within the family Culicidae (from the Latin ''culex'' meaning "gnat"). The word "mosquito" (formed by ''mosca'' and diminutive ''-ito'') is Spanish for "litt ...
), biting midges (
Ceratopogonidae Ceratopogonidae is a family of flies commonly known as no-see-ums, or biting midges, generally in length. The family includes more than 5,000 species, distributed worldwide, apart from the Antarctic and the Arctic. Ceratopogonidae are holomet ...
), and louse flies (
Hippoboscidae __NOTOC__ Hippoboscidae, the louse flies or keds, are obligate parasites of mammals and birds. In this family, the winged species can fly at least reasonably well, though others with vestigial or no wings are flightless and highly apomorphic. As ...
). The blood-parasites of the genus '' Plasmodium'' and ''
Haemoproteus ''Haemoproteus'' is a genus of alveolates that are parasitic in birds, reptiles and amphibians. Its name is derived from Greek: ''Haima'', "blood", and ''Proteus'', a sea god who had the power of assuming different shapes. The name ''Haemoproteu ...
'', encompass an extremely diverse group of pathogens with global distribution. The large number of parasite lineages along with their wide range of potential host species and the pathogen's capacity for host switching makes the study of this system extremely complex. Evolutionary relationships between hosts and the parasites have only added complexity and suggested extensive sampling is needed to elucidate how global cospeciation events drive disease transmission and maintenance in various ecosystems. In addition to this, the parasite's ability to disperse can be mediated by
migratory birds Bird migration is the regular seasonal movement, often north and south along a flyway, between breeding and wintering grounds. Many species of bird migrate. Migration carries high costs in predation and mortality, including from hunting b ...
and thus increases variation in
prevalence In epidemiology, prevalence is the proportion of a particular population found to be affected by a medical condition (typically a disease or a risk factor such as smoking or seatbelt use) at a specific time. It is derived by comparing the number o ...
patterns and alters host-parasite adaptation processes. Host susceptibility is highly variable as well and numerous efforts have been made to understand the relationship between increased prevalence and host traits such as nesting and foraging height, sexual dimorphism or even incubation time length. So far, the effects of this disease in wild populations is poorly understood. A 2015 study using blood samples from Malawian bird fauna found that close to 80% of were infected with either malaria or closely related alveolates. Closed-cup nesters, such as
weavers Weaver or Weavers may refer to: Activities * A person who engages in weaving fabric Animals * Various birds of the family Ploceidae * Crevice weaver spider family * Orb-weaver spider family * Weever (or weever-fish) Arts and entertainmen ...
and
Cisticola __NOTOC__ Cisticolas (pronounced ''sis-TIC-olas'') are a genus of very small insectivorous birds formerly classified in the Old World warbler family Sylviidae, but now usually considered to be in the separate family Cisticolidae, along with other ...
, were more likely to be infected with Plasmodium than with midge-borne parasites such as Haemoproteus and
Leucocytozoon ''Leucocytozoon '' (or ''Leukocytozoon'') is a genus of parasitic alveolates belonging to the phylum Apicomplexa (which also includes the malaria parasites). The species of this genus use either blackflies (''Simulium'' species) or a biting mid ...
. There exists much controversy on what corresponds as a species in avian malaria parasites. The Latin binomials nomenclature used to describe '' Plasmodium'' and '' Hemoproteus'' parasites is based on a restricted set of morphological characteristics and the restriction to which parasites of birds they are able to infect. Therefore, considering co-speciation events or even species
diversity Diversity, diversify, or diverse may refer to: Business *Diversity (business), the inclusion of people of different identities (ethnicity, gender, age) in the workforce * Diversity marketing, marketing communication targeting diverse customers ...
for malaria parasites is surrounded by much disagreement. Molecular tools have directed classification towards a phylogenetic definition of lineages, based on sequence divergence and the range of hosts in which the parasite can be found. The diversity of avian malaria parasites and other haemosporidia is extremely large, and previous studies have found that the number of parasites approximates the number of hosts, with significant host switching events and parasite sharing. The current approach suggests amplification of the cytochrome b gene of the parasite and the reconstruction of genealogies based on this information. Due to the large amount of lineages and different host species, a public database called MalAvi has been created to encourage sharing these sequences and aid in understanding the diversity of these parasites. Considering that no other
genetic marker A genetic marker is a gene or DNA sequence with a known location on a chromosome that can be used to identify individuals or species. It can be described as a variation (which may arise due to mutation or alteration in the genomic loci) that can be ...
s have been developed for this group of parasites, a ~1.2-4% sequence divergence has been determined as a cutoff value to distinguish between different parasite lineages. The molecular approach has also allowed direct comparisons between host phylogenies and parasite genealogies, and significant co-speciation has been found based on event-based-matching of phylogenetic trees.


Phylogeny of malaria parasites

To date, there is no specific phylogeny for avian
malaria parasites ''Plasmodium'' is a genus of unicellular eukaryotes that are obligate parasites of vertebrates and insects. The life cycles of ''Plasmodium'' species involve development in a blood-feeding insect host which then injects parasites into a verteb ...
and related haemosporidian parasites. However, given that malaria parasites can be found in reptiles, birds and mammals, it is possible to combine the data from these groups and a well resolved large phylogeny is available. For over a century, parasitologists classified malaria parasites based on morphological and life-history traits and new molecular data shows that these have variable phylogenetic signals. The current approach suggests that '' Plasmodium'' species infecting birds and squamate reptiles belong to one clade, and mammalian lineages belonging to a separate clade. In the case of ''
Haemoproteus ''Haemoproteus'' is a genus of alveolates that are parasitic in birds, reptiles and amphibians. Its name is derived from Greek: ''Haima'', "blood", and ''Proteus'', a sea god who had the power of assuming different shapes. The name ''Haemoproteu ...
,'' this group has traditionally been classified based on the vector host, with one clade being transmitted to columbiform birds by hippoboscid flies and a second group transmitted by biting midges to other avian families. The molecular data supports this approach and suggests reclassifying the later group as ''Parahaemoproteous.''


Phylogeography of avian malaria

Although a widespread disease, the culprit most commonly associated with the disease is '' Plasmodium relictum'' and associated lineages''.'' To better understand the parasite's epidemiology and geographical distribution, analysis of genetic variation across large geographical scales have been conducted by looking at the nuclear gene MSP1 ( merozoite surface protein) from '' Plasmodium relictum'' ''.'' Findings have revealed that there are significant differences between lineages from the New and Old World, suggesting different introductions of the parasite to avian populations. In addition to this, considerable variation was found between Europe and African lineages, suggesting different patterns of transmission for temperate and tropical populations. Although this approach is relatively recent, detecting allelic variation in different markers is essential to unveil parasite transmission patterns and the likelihood of introduction to new susceptible host populations.


Vector

Contrary to the state of knowledge on parasite-avian interactions, parasite-vector relationships are relatively less explored. MalAvi does list several known vectors however this is not at all complete. Generally avian malaria organisms are vectored by ''
Culex ''Culex'' is a genus of mosquitoes, several species of which serve as vectors of one or more important diseases of birds, humans, and other animals. The diseases they vector include arbovirus infections such as West Nile virus, Japanese ence ...
''. Its real vector in Hawaiʻi is the mosquito ''
Culex quinquefasciatus ''Culex'' is a genus of mosquitoes, several species of which serve as vectors of one or more important diseases of birds, humans, and other animals. The diseases they vector include arbovirus infections such as West Nile virus, Japanese en ...
'', which was introduced to the Hawaiʻian Islands in 1826. Since then, avian malaria and
avipoxvirus ''Avipoxvirus'' (avian pox) is a genus of viruses within the family ''Poxviridae''. ''Poxviridae'' is the family of viruses which cause the afflicted organism to have poxes as a symptom. Poxviruses have generally large genomes, and other such ex ...
together have devastated the native bird population, resulting in many extinctions. Hawaiʻi has more extinct birds than anywhere else in the world; just since the 1980s, ten unique birds have disappeared. Virtually every individual of endemic species below in elevation has been eliminated by the disease. These mosquitoes are limited to lower elevations, below , by cold temperatures that prevent larval development. However, they appear to be slowly gaining a foothold at higher elevations and their range may be expanding upwards. If so, most remaining Hawaiian land birds may become at risk to extinction. Most of the Hawaiian Islands have a maximum elevation of less than , so with the exception of the island of Hawaiʻi and
East Maui East or Orient is one of the four cardinal directions or points of the compass. It is the opposite direction from west and is the direction from which the Sun rises on the Earth. Etymology As in other languages, the word is formed from the fa ...
, native birds may become extinct on every other island if the mosquito is able to occupy higher elevations.


Disease process and epidemiology

''Plasmodium relictum'' reproduces in red blood cells. If the parasite load is sufficiently high, the bird begins losing red blood cells, causing
anemia Anemia or anaemia (British English) is a blood disorder in which the blood has a reduced ability to carry oxygen due to a lower than normal number of red blood cells, or a reduction in the amount of hemoglobin. When anemia comes on slowly, t ...
(USDI and USGS 2005). Because red blood cells are critical for moving oxygen about the body, loss of these cells can lead to progressive weakness and, eventually, death (USDI and USGS 2005). Malaria mainly affects passerines (perching birds). In Hawaiʻi, this includes most of the native
Hawaiian honeycreeper Hawaiian honeycreepers are a group of small, passerine birds endemic to Hawaii. They are closely related to the rosefinches in the genus ''Carpodacus'', but many species have evolved features unlike those present in any other finch. Their great ...
s and the
Hawaiian crow The Hawaiian crow or alalā (''Corvus hawaiiensis'') is a species of bird in the crow family, Corvidae, that is currently extinct in the wild, though reintroduction programs are underway. It is about the size of the carrion crow at in length, bu ...
. Susceptibility to the disease varies between species, for example, the iiwi is very susceptible to malaria while the
ʻApapane The apapane (''Himatione sanguinea,'' pronounced /ˌ ɑ pɑˈpɑ neɪ/, ''ah-pah-PAH-ney'') is a small, crimson species of Hawaiian honeycreeper endemic to the Hawaiian Islands. They are the most abundant and widely distributed honeycreeper and ...
less so (USDI and USGS 2005). Native Hawaiʻian birds are more susceptible than introduced birds to the disease and exhibit a higher
mortality rate Mortality rate, or death rate, is a measure of the number of deaths (in general, or due to a specific cause) in a particular population, scaled to the size of that population, per unit of time. Mortality rate is typically expressed in units of de ...
(Van Riper et al. 1982; Atkinson et al. 1995). This has serious implications for native bird faunas (SPREP) with P. relictum being blamed for the
range Range may refer to: Geography * Range (geographic), a chain of hills or mountains; a somewhat linear, complex mountainous or hilly area (cordillera, sierra) ** Mountain range, a group of mountains bordered by lowlands * Range, a term used to i ...
restriction and extinctions of a number of bird species in Hawaiʻi, primarily forest birds of low-land forests habitats where the mosquito vector is most common (Warner 1968; Van Riper 1991; USDI and USGS 2005). The incidence of this disease has nearly tripled in the last 70 years. Notable among the species of birds most heavily affected were
house sparrow The house sparrow (''Passer domesticus'') is a bird of the sparrow family Passeridae, found in most parts of the world. It is a small bird that has a typical length of and a mass of . Females and young birds are coloured pale brown and grey, a ...
s, great tits, and
Eurasian blackcap The Eurasian blackcap (''Sylvia atricapilla''), usually known simply as the blackcap, is a common and widespread typical warbler. It has mainly olive-grey upperparts and pale grey underparts, and differences between the five subspecies are s ...
s. Prior to 1990, when global temperatures were cooler than now, less than 10 percent of house sparrows (''Passer domesticus'') were infected with malaria. In recent years, however, this figure has increased to nearly 30 percent. Likewise, since 1995, the percent of malaria-infected great tits has risen from 3 percent to 15 percent. In 1999, some 4 percent of blackcaps—a species once unaffected by avian malaria—were infected. For tawny owls in the UK, the incidence had risen from two or three percent to 60%. Although new epidemics are expected to be driven by
speciation Speciation is the evolutionary process by which populations evolve to become distinct species. The biologist Orator F. Cook coined the term in 1906 for cladogenesis, the splitting of lineages, as opposed to anagenesis, phyletic evolution within ...
events the real situation is still poorly understood. Ellis et al 2015 find host switching is more common in avian haemosporidians including avian malaria organisms. They find secondary importance goes to
adaptation In biology, adaptation has three related meanings. Firstly, it is the dynamic evolutionary process of natural selection that fits organisms to their environment, enhancing their evolutionary fitness. Secondly, it is a state reached by the po ...
to whatever host populations are locally available.


Control

The main way to control avian malaria is to control mosquito populations. Hunting and removing pigs helps, because wallows from
feral pig The feral pig is a domestic pig which has gone feral, meaning it lives in the wild. They are found mostly in the Americas and Australia. Razorback and wild hog are Americanisms applied to feral pigs or boar-pig hybrids. Definition A feral p ...
s and hollowed out logs of the native hapu'u ferns provide dirty standing water where the mosquito breeds (USDI and USGS 2005). Around houses, reducing the number of potential water catchment containers helps reduce the mosquito breeding sites (SPREP Undated). However, in Hawaiʻi, attempts to control the mosquitoes by larval habitat reduction and larvicide use have not eliminated the threat. It may also be possible to find birds that are resistant to malaria, collect eggs and raise young birds for re-introduction into areas where birds are not resistant, giving the species a head-start on spreading resistance. There is evidence for evolution of resistance to avian malaria in two endemic species, Oʻahu ʻamakihi and
Hawaiʻi ʻamakihi The Hawaii amakihi (''Chlorodrepanis virens''), also known as the common amakihi, is a species of Hawaiian honeycreeper. Taxonomy The Hawaii amakihi was formerly placed in the genus ''Hemignathus'' but was assigned to the genus '' Chlorodrepanis ...
. If other species can be preserved for long enough, they may evolve resistance as well. One tactic would be to reforest high-elevation areas on the island of Hawaiʻi, for example above the refuge of Hakalau on land managed by the Department of Hawaiʻian Homelands. This could give birds more time to adapt before climate change or mosquito evolution bring avian malaria to the last remaining bird populations. Extirpating mosquitos from Hawai'i using
CRISPR CRISPR () (an acronym for clustered regularly interspaced short palindromic repeats) is a family of DNA sequences found in the genomes of prokaryotic organisms such as bacteria and archaea. These sequences are derived from DNA fragments of bac ...
editing has also been suggested.


References


Further reading

* .


External links


http://www.issg.org/database/species/ecology.asp?si=39&fr=1&sts=
* * * {{Taxonbar, from=Q2663527 Bird diseases Protozoal diseases Parasites of birds