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      Blood smear: Giemsa-stained blood smear from a bird infected with Plasmodium relictum. The intracellular parasites (arrows) develop within nucleated red blood cells and eventually destroy their host cells, causing severe anemia during acute stages of the infection. (Photo: U.S. Geological Survey - Biological Resources Division) - Click for full size   Oocyst: two developing oocysts of Plasmodium relictum on the stomach wall of the mosquito vector, Culex quinquefasciatus. The oocysts contain densely packed, long slender sporozoites (arrows) that are released at maturation and invade the salivary glands of the insect. The sporozoites are capable of infecting another bird with malaria when the mosquito takes another blood meal. (Photo: U.S. Geological Survey - Biological Resources Division) - Click for full size
    Taxonomic name: Plasmodium relictum (Grassi and Feletti 1891)
    Synonyms: Haemamoeba relicta Grassi and Feletti 1891, Plasmodium capistrani Russell 1932, Plasmodium inconsta Hartman 1927
    Common names: avian malaria (English), paludisme des oiseaux (French), Vogelmalaria (German)
    Organism type: micro-organism
    The protozoa, Plasmodium relictum, is one of the causative parasites of avian malaria and may be lethal to species which have not evolved resistance to the disease (e.g. penguins). It may be devastating to highly susceptible avifauna that has evolved in the absence of this organism, such as native Hawaiian birds. The parasite cannot be transmitted directly from one bird to another, but requires a mosquito to move from one bird to another. In Hawaii, the mosquito that transmits Plasmodium relictum is the common house mosquito, Culex quinquefasciatus. Passerine birds are the most common victims of avian malaria.
    Description
    Histopathological examination may reveal numerous intraendothelial schizonts in spleen, lung, liver, heart and kidney (Fix et al. 1988). Schizonts may be 16 to 28 micron by 11 to 16 micron large and contain merozoites of two distinct sizes (macromerozoites, nuclei 1.0 micron; micromerozoites, nuclei 0.5 micron) (Fix et al. 1988).
    The clinical signs of disease are caused by the tissue phase, causing tissue damage (Cranfield et al. Undated). There may not be enough destruction within the red blood cells to cause clinical anemia. The clinical signs in penguins are paleness, anoxia, dyspnea, inappetence, regurgitation, and death. The gross pathology reveals a very enlarged spleen, swollen liver, and congested and extremely edematous lungs. Impression smears from these tissues often reveals schizonts. Schizonts are present in several tissues throughout the body. Histologically, the lungs have acute severe interstitial pneumonia with schizonts present. Post mortem blood samples from major vessels or the heart can be extremely useful in the diagnosis, even up to 48 hours after death (Cranfield et al. Undated).
    Plasmodium pathology observed in native Hawaiian honeycreepers includes: extremely high blood parasitemias (infection in up to 50% of circulating red blood cells), extensive damage to the liver and spleen, weight loss and inappetance and high mortality rates (Trouble in Paradise Undated).
    Occurs in:
    host, vector
    Habitat description
    Presence of the disease is linked with the presence of a suitable vector species. In the case of Hawaii this is the range of the house mosquito Culex quinquefasciatus (USDI and USGS 2005), a primary carrier of the disease causing agent. Studies by researchers at the Pacific Islands Ecosystem Science Center have revealed a lot about the ecology of the bird malaria in Hawaii including the link between the vector range and disease prevalence. Because this species of mosquito is more numerous at lower elevations, avian malaria is found mainly in birds of the lowland forests (USDI and USGS 2005), however, recent evidence suggests the range of the vector and thus disease could be moving into high land areas.
    General impacts
    Several species of the filarial parasite Plasmodium are the causal organism for avian malaria. Plasmodium relictum capistranoae Russell is the parasite found in infected Hawaiian birds (USDI and USGS 2005). In birds, P. relictum reproduces in red blood cells. If the parasite load is sufficiently high, the bird begins losing red blood cells causing anemia (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 birds in the order Passeriformes (perching birds). In Hawaii, this includes most of the native honeycreepers and the Hawaiian crow. Susceptibility to the disease varies between species, for example, the iiwi is very susceptible to malaria while the apapane less so (USDI and USGS 2005). Native Hawaiian birds are more susceptible than introduced birds to the disease and exhibit a higher mortality rate (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 restriction and extinctions of a number of bird species in Hawaii, primarily forest birds of low-land forests habitats where the mosquito vector is most common (Warner 1968; Van Riper 1991; USDI and USGS 2005).
    Recent evidence indicates that some native Hawaiian lowland forest birds have developed some tolerance to P. relictum. For example, the Amakihi are once again breeding in remaining lowland forest habitat although they show a incidence of malaria (60-70%) (Trouble in Paradise Undated). Although this appears encouraging Freed and colleagues (2005) point out that as more of the common species evolve tolerance they increase reservoirs of the disease, which in turn increases the risk of transmission to rarer species that are vulnerable to avian malaria. Most honeycreepers, especially endangered species, now persist only in forests above 1500m elevation, where cool temperatures prevent effective malaria development in mosquitoes (Freed et al. 2005). The prevalence of malaria in Hawaiian forest birds at 1900m on the island of Hawaii has more than doubled over a decade. This increase is associated with breeding of mosquitoes and warmer summertime air temperatures. Tolerance to malaria in native birds is adding to a reservoir of malaria at upper elevations even while vectors are rare and air temperatures are too low for complete development of the parasite in the vector. Freed and colleagues argue that malaria is becoming an emergent infectious disease at upper elevations and that the spread of avian malaria can be partly attributed to climate change and increasing temperatures.
    The parasite does not appear to be pathogenic in birds that have evolved with the parasite, often causing no signs. However, it causes varying degrees of pathology and can cause high mortalities in species of birds that have not evolved with the parasite. These susceptible species may come from areas without the vector, such as very cold, dry, or windy environments. This is why avian malaria is so lethal to penguins (in which it is caused by Plasmodium relictum and P. Elongatum), as illustrated by the 1986 outbreak of the disease in wild-caught Magellanic penguins (see Spheniscus magellanicus in IUCN Red List of Threatened Species) at the Blank Park Zoo in Des Moines, Iowa, USA (Fix et al. 1988). It is the highest cause of mortality in outdoor penguin exhibits and causes 50% or greater mortality in untreated juvenile and adult penguins when first exposed to the vector (Cranfield et al. Undated). For more detailed information of the impacts of P. relictum, click here
    Geographical range
    Native Range: A survey in American Samoa by Jarvi et al (2003) of native and introduced birds detected the presence of Plasmodium relictum. The authors report that "high prevalence of apparently chronic infections, the relative stability of the native land bird communities, and the presence of mosquito vectors which are considered endemic and capable of transmitting avian Plasmodia, suggest that these parasites are indigenous to Samoa and have a long coevolutionary history with their hosts.
    Introduced Range:P. relictum is now widespread among introduced and native birds in Hawaii where it has played a key role in the extinction of approximately half of the endemic bird species (Atkinson & van Riper 1991 in Jarvi et al. 2003). P. relictum has also been reported from England, France and parts of the United States including Maryland, Florida and New York. Recent surveys show that P. relictum is widespread and established in New Zealand, although it is yet to be determined whether it is native or introduced (Tompkins and Gleeson 2006). Surveys for avian malaria in the Pacific have been in Guam (Savidge 1985) and the Cook Islands (Steadman et al. 1990) and results were negative (SPREP).
    Introduction pathways to new locations
    Acclimatisation societies: Introduction by bird clubs (Hui Manu in Hawaii). Infective birds not detected by standard diagnostics.
    Landscape/fauna "improvement": Introduction of game species. Infective birds not detected by standard diagnostics.
    Taken to botanical garden/zoo: Infective birds not detected by standard diagnostics.


    Local dispersal methods
    On animals (local): Dispersal of infective mosquitoes may be enhanced by wind.
    Management information
    Preventative measures: Because P. relictum presence is linked to mosquito populations malaria is very hard to eradicate. To effectively eliminate malaria from a habitat either the vector (mosquito) must be eliminated or prevented from feeding on the bird (USDI and USGS 2005). This is difficult particularly in remote areas in the wet forests of Hawaii where wallows from feral pigs and hollowed out logs of the native apuu ferns provide ample areas of standing water where the mosquito breeds (USDI and USGS 2005). One effective procedure is to reduce the number of potential water catchment containers in order to reduce the mosquito breeding sites available (SPREP Undated). However, in Hawaii attempts to control the mosquitoes by larval habitat reduction and larvicide use have been largely unsuccessful.

    Chemical: Captive bird populations may be treated with pharmaceuticals such as chloroquine and primaquine to cure the disease (Cranfield et al. Undated). To see more detailed information of the management and control of P. relictum, click here

    Nutrition
    This organism is an intracellular parasite that acquires most of its essential nutrients directly from the host cells.
    Reproduction
    Undergoes sexual and asexual reproduction at different stages in both the vertebrate (bird) and invertebrate (mosquito) hosts.

    Sporozoites are the infectious stage of the Plasmodium protozoan parasite and are transmitted to a vertebrate host through blood feeding by a mosquito. The disease to the host is caused by the parasite protozoan attacking red blood cells to continue its development. Fully developed erythrocytic schizonts cause rupturing of the red blood cells to release merozoites (to continue the blood cycle in the host) and gametocytes (capable of initiating sexual development if ingested by a mosquito). It is the merozoites with accompanying toxins that cause the chills and fever of malaria (SPREP, 2000).
    Exponential growth every 36 hours while in circulating blood cells.
    Lifecycle stages
    This disease causing agent is carried and transmitted by a mosquito vector. The mosquito takes a blood meal from the reservoir host and ingests micro and macro gametocytes. These develop into oocysts in the gut of the mosquito. The oocysts then produce numerous sporozoites, which migrate to the salivary gland of the mosquito. These are infectious agents of malaria and are injected into the blood stream of the bird when the mosquito is taking its next blood meal. The cycle through the mosquito takes approximately 13 days (Cranfield et al. Undated).
    The sporozoites, on entering the blood stream of the bird, are picked up by macrophages and reticuloendothelial cells where they develop into merozoites and then further on to schizonts (Cranfield et al. Undated). It is the merozoites with accompanying toxins that cause the chills and fever of malaria (SPREP Undated).The schizonts break apart shedding several more merozoites, which sets up the asexual tissue phase of the infection (Cranfield et al. Undated). After several cycles through the tissue, the merozoites are picked up by the red blood cells and develop into trophozoites and then on to either the sexual stage of the gametocytes or the asexual stage of schizonts (Cranfield et al. Undated). Therefore avians have two cycles going - a tissue phase and a blood phase. Within the blood phase, there is a sexual cycle and an asexual cycle (Cranfield et al. Undated). Fully developed erythrocytic schizonts cause rupturing of the red blood cells to release merozoites (to continue the blood cycle in the host) and gametocytes (capable of initiating sexual development if ingested by a mosquito) (SPREP Undated).
    It is the merozoites with accompanying toxins that cause the chills and fever of malaria (SPREP Undated). Exponential growth every 36 hours while in circulating blood cells (SPREP Undated).
    This species has been nominated as among 100 of the "World's Worst" invaders
    Reviewed by: Carter T. Atkinson, Ph.D. and Dennis A. LaPointe, Ph.D., USGS-BRD Pacific Island Ecosystems Research Center, Volcano, Hawaii
    Compiled by: Carter T. Atkinson, Ph.D. and Dennis A. LaPointe, Ph.D., USGS-BRD Pacific Island Ecosystems Research Center, Volcano, Hawaii & IUCN/SSC Invasive Species Specialist Group (ISSG)
    Last Modified: Thursday, 14 July 2005


ISSG Landcare Research NBII IUCN University of Auckland