Plasmodium relictum infection
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Plasmodium relictum infection
International Common Names
- English: avian malaria
OverviewTop of page
Plasmodium relictum is one of more than 40 species of Plasmodium that can infect birds and cause avian malaria (Valkiunas, 2005). This disease has many similarities to human malaria and these organisms were important early experimental models for studies of the human plasmodia. P. relictum has caused acute, pathogenic infections in captive wild birds in zoological collections when they were moved outside of their natural range and in wild populations when it has been introduced with suitable mosquito vectors to remote islands and some other sites worldwide (Garnham, 1966; Valkiunas, 2005). It has had a substantial effect on the geographic and altitudinal distribution of endemic forest birds in the Hawaiian Islands and has contributed to their decline and extinction over approximately the past 90 years. P. relictum is not infectious to domestic poultry under most circumstances and is not viewed as an economic threat to the poultry industry. Plasmodium currently threatens endemic penguins and passerines in the Galapagos Islands, but has not yet been verified to the species level in this archipelago (Levin et al., 2009). P. relictum may currently be spreading in New Zealand as the range of a highly efficient vector, the introduced Southern House Mosquito (Culex quinquefasciatus) expands there (Tompkins and Gleeson, 2006). Other species of avian Plasmodium that can cause disease outbreaks in domestic poultry include P. gallinaceum and P. juxtanucleare in chickens in South America and SE Asia and P. durae in domestic turkeys in Africa (Atkinson, 2008). These species can cause problems when poultry operations are moved into habitats with natural reservoirs of infection and suitable mosquito vectors.
Hosts/Species AffectedTop of page
P. relictum is primarily a parasite of passerine birds, although species in at least 16 additional avian orders are susceptible to infection. Both penguins (Spheniscidae) and Hawaiian Honeycreepers (Drepanidinae) are particularly susceptible to infection with P. relictum, but the physiological basis for this high susceptibility is not understood. Reports of pathogenicity from infections with P. relictum are more common in zoo settings, where hosts are moved outside of their normal range and exposed to local vectors and transmission of the parasite. The impact of P. relictum on wild birds is poorly known in natural ecosystems, but experimental data show that lineage SGS1 is virulent and might cause severe disease and even mortality in wild birds, particularly during co-infections with other species of Plasmodium (Palinauskas et al., 2008; Palinauskas et al., 2011). Infection with the same lineage of P. relictum causes diseases of different severity in different host species (Palinauskas et al., 2008); this should be taken into consideration in conservation projects.
DistributionTop of page
Reports of P. relictum that have accumulated over the past century are based mostly on morphology of erythrocytic stages. Earlier reports are based primarily on microscopy and may underestimate the true prevalence of the parasite in many host species (Fallon and Ricklefs, 2008), particularly since the morphological stages that are necessary for identification may be absent or in extremely low numbers in chronic, low intensity infections. Many recent studies have attempted to "type" parasites based on sequence of conserved mitochondrial DNA (Beadell et al., 2006; Marzal et al., 2011), and molecular markers for identification of this parasite have been developed (Beadell et al., 2006; Palinauskas et al., 2007), but are of low sensitivity for the detection of mixed infections of different Plasmodium spp. -- a combination of optical microscopy and PCR-based tools is recommended in studies of distribution of malaria parasites in wildlife (Valkiunas et al., 2006). In addition, most reports in migratory species do not distinguish where transmission of the parasites occurs. Transmission may take place either in breeding or wintering grounds, or in some cases in both locations (Perez-Tris and Bensch, 2005); lineage GRW4, the one that has caused problems for native Hawaiian birds, is present in northern Europe in birds that have migrated from Africa, but is not transmitted there (Palinauskas et al., 2007). Many early reports of P. relictum are not backed by museum voucher specimens and need to be verified by more detailed field studies. The patchy distribution by countries and host species is most likely a sampling artifact. The parasite has been reported in all zoogeographic regions of the world with the exception of Antarctica and is a relatively common parasite of passerine birds.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Armenia||Present||Native||Not invasive||Karaseferyan, 1959|
|Azerbaijan||Present||Native||Not invasive||Zeiniev, 1975|
|Georgia (Republic of)||Present||Native||Not invasive||Burtikashvili, 1978|
|India||Present||Native||Not invasive||Beadell et al., 2006; Ishtiaq et al., 2007; Marzal et al., 2011||Lineages GRW4, SGS1|
|Indonesia||Present||Native||Not invasive||McClure et al., 1978|
|Iraq||Present||Native||Not invasive||Shamsuddin and Mohammad, 1981|
|Israel||Present||Native||Not invasive||Bensch et al., 2000; Beadell et al., 2006; Martinsen et al., 2006; Marzal et al., 2011||Lineages GRW4, SGS1|
|Japan||Present||Native||Not invasive||Beadell et al., 2006; Ejiri et al., 2008||Lineage GRW4|
|Kazakhstan||Present||Native||Not invasive||Yakunin and Zhazyltaev, 1977|
|Korea, Republic of||Present||Native||Not invasive||Beadell et al., 2006||Lineages GRW4, SGS1.|
|Kyrgyzstan||Present||Native||Not invasive||Kairullaev and Yakunin, 1982|
|Malaysia||Present||Native||Not invasive||Laird, 1998|
|Myanmar||Present||Native||Not invasive||Beadell et al., 2006|
|Pakistan||Present||Native||Not invasive||Lari, 1959|
|Philippines||Present||Native||Not invasive||McClure et al., 1978|
|Singapore||Present||Native||Not invasive||Beadell et al., 2006|
|Taiwan||Present||Native||Not invasive||Manwell et al., 1976|
|Tajikistan||Present||Native||Not invasive||Subkhonov, 1972|
|Thailand||Present||Native||Not invasive||McClure et al., 1978|
|Turkey||Present||Native||Not invasive||Marzal et al., 2011||Lineages SGS1 and GRW11|
|Algeria||Present||Native||Not invasive||Sergent and Sergent, 1904|
|Botswana||Present||Native||Not invasive||Beadell et al., 2006|
|Cameroon||Present||Native||Not invasive||Beadell et al., 2006|
|Chad||Present||Native||Not invasive||Williams et al., 1977|
|Comoros||Present||Native||Not invasive||Beadell et al., 2006||Lineage GRW4, Grand Comore Island|
|Egypt||Present||Native||Not invasive||MOHAMMED, 1958; Marzal et al., 2011||Lineages SGS1 and GRW11|
|Equatorial Guinea||Present||Native||Not invasive||Beadell et al., 2006|
|Ethiopia||Present||Native||Not invasive||Ashford et al., 1976|
|Gabon||Present||Native||Not invasive||Beadell et al., 2006|
|Kenya||Present||Native||Not invasive||Bennett and Herman, 1976; Bensch et al., 2000; Perkins and Schall, 2002||Lineage GRW4|
|Madagascar||Present||Native||Not invasive||Beadell et al., 2006||Lineage GRW4|
|Mauritius||Present||Native||Not invasive||Peirce et al., 1977; Beadell et al., 2006||Lineage GRW4|
|Mayotte||Present||Native||Not invasive||Beadell et al., 2006||Lineage GRW4|
|Nigeria||Present||Native||Not invasive||Waldenström et al., 2002; Beadell et al., 2006; Hellgren et al., 2007||Lineages GRW4, SGS1|
|Réunion||Present||Native||Not invasive||Peirce et al., 1977; Beadell et al., 2006||Lineage GRW4|
|Rodriguez Island||Present||Native||Not invasive||Beadell et al., 2006||Lineage GRW4|
|Sao Tome and Principe||Present||Native||Not invasive||Beadell et al., 2006|
|Senegal||Present||Bennett et al., 1978|
|Seychelles||Present||Native||Not invasive||Beadell et al., 2006||Lineage GRW4 on Praslin, other lineages on Fregate|
|South Africa||Present||Native||Not invasive||Beadell et al., 2006; Durrant et al., 2007||Lineage GRW4|
|Tanzania||Present||Native||Not invasive||Bennett and Herman, 1976|
|Uganda||Present||Native||Not invasive||Bennett et al., 1974b|
|Zambia||Present||Native||Not invasive||Peirce, 1984|
|Zimbabwe||Present||Native||Not invasive||Beadell et al., 2006|
|Bermuda||Present||Introduced||Beadell et al., 2006; Marzal et al., 2011||Lineage GRW4; speculation that it may have played a role in the decline of Bermudan birds|
|Canada||Present||Native||Not invasive||Bennett et al., 1974a; Bishop and Bennett, 1992||Records from Newfoundland and Saskatchewan; likely widespread throughout Canada|
|Mexico||Present||Native||Not invasive||Beltran and Pardinas, 1953; Marzal et al., 2011||Lineage GRW4|
|USA||Widespread||Native||Not invasive||Beadell et al., 2006; Kimura et al., 2006; Marzal et al., 2011||Multiple records from throughout continental U.S.|
|-Hawaii||Widespread||Introduced||1920s?||Invasive||Laird and Van Riper, 1981; Beadell et al., 2006||Lineage GRW4. Common in wet habitats at elevations below 1500 m on main Hawaiian Islands; not present in NW Hawaiian Islands with possible exception of Midway Atoll|
Central America and Caribbean
|Dominican Republic||Present||Native||Not invasive||Beadell et al., 2006||Lineage GRW4|
|Grenada||Present||Native||Not invasive||Beadell et al., 2006||Lineage GRW4|
|Jamaica||Present||Native||Not invasive||Bennett et al., 1980|
|Panama||Present||Native||Not invasive||Sousa and Herman, 1982|
|Brazil||Present||Native||Not invasive||Marzal et al., 2011||Lineage GRW4|
|Colombia||Present||Native||Not invasive||Bennett and Borrero, 1976|
|Guyana||Present||Native||Not invasive||Beadell et al., 2006|
|Uruguay||Present||Native||Not invasive||Beadell et al., 2006|
|Venezuela||Present||Native||Not invasive||Gabaldon and Ulloa, 1980|
|Belarus||Present||Native||Not invasive||Beadell et al., 2006||Lineage GRW4|
|Belgium||Present||Native||Not invasive||Hellgren et al., 2007||Lineages GRW4, SGS1|
|Bulgaria||Present||Native||Not invasive||Shurulinkov and Golemansky, 2003; Hellgren et al., 2007; Zehtindjiev et al., 2008||Lineages GRW4, SGS1.|
|Czech Republic||Present||Native||Not invasive||Votýpka et al., 2003|
|Czechoslovakia (former)||Present||Native||Not invasive||Kucera, 1978|
|France||Present||Native||Not invasive||Beadell et al., 2006; Bonneaud et al., 2006; Loiseau et al., 2008; Marzal et al., 2011||Lineages SGS1 and GRW4|
|Germany||Present||Native||Not invasive||Beadell et al., 2006|
|Greece||Present||Native||Not invasive||PAPADAKIS, 1935|
|Hungary||Present||Native||Not invasive||Szöllosi et al., 2009||Lineages GRW4, SGS1|
|Italy||Present||Native||Not invasive||Corradetti, 1970; Beadell et al., 2006; Hellgren et al., 2007; Marzal et al., 2011||Lineages GRW4, SGS1, GRW11|
|Lithuania||Present||Native||Not invasive||Hellgren et al., 2007; Palinauskas et al., 2007; Marzal et al., 2011||Lineages SGS1, GRW11|
|Norway||Present||Native||Not invasive||Beadell et al., 2006; Marzal et al., 2011||Lineages GRW4 and SGS1|
|Poland||Present||Sulgostowska and Czaplinska, 1987|
|Russian Federation||Present||Native||Not invasive||Kobyshev et al., 1975; Beadell et al., 2006; Zehtindjiev et al., 2009; Marzal et al., 2011||Multiple reports from throughout Russia, including lineages GRW4, SGS1 and GRW11|
|Spain||Present||Native||Not invasive||Orbaneja Aguero S de, 1934; Beadell et al., 2006; Hellgren et al., 2007; Marzal et al., 2008; Marzal et al., 2011||Lineages GRW4, SGS1, GRW11|
|Sweden||Present||Native||Not invasive||Hellgren, 2005; Beadell et al., 2006; Bensch et al., 2007; Yohannes et al., 2008; Marzal et al., 2011||Lineages GRW4, SGS1|
|UK||Present||Native||Not invasive||Beadell et al., 2006; Wood et al., 2007; Cosgrove et al., 2008||Lineages SGS1, GRW11|
|Ukraine||Present||Native||Not invasive||Gluschchenko, 1963; Beadell et al., 2006; Hellgren et al., 2007; Marzal et al., 2011||Lineages GRW4, SGS1|
|Australia||Present||Native||Not invasive||Beadell et al., 2006||Lineage GRW4|
|Cook Islands||Present||Introduced||1922?||Ishtiaq et al., 2007||Single report from introduced Common Myna (Acridotheres tristis) based on PCR diagnostics; distribution in indigenous birds unknown|
|French Polynesia||Present||Introduced||Beadell et al., 2006||Lineage GRW4. Single report based on PCR diagnostics from introduced birds on Moorea (Society Islands) and from indigenous birds on Nuku Hiva (Marquesas Islands)|
|New Zealand||Widespread||Introduced||Invasive||Beadell et al., 2006; Tompkins and Gleeson, 2006; Marzal et al., 2011||Widespread in introduced passerines on North and South Islands, Lineage SGS1|
|Northern Mariana Islands||Present||Beadell et al., 2006||Single report based on PCR diagnostics from the indigenous Rufous Fantail (Rhipidura rufifrons). Not clear if it was introduced with non-native passerines.|
|Papua New Guinea||Present||Native||Not invasive||Beadell et al., 2006|
|Solomon Islands||Present||Native||Not invasive||Laird, 1960|
PathologyTop of page
Avian malaria is primarily a disease of the blood and reticuloendothelial system and the progress of the disease and clinical signs closely parallel increases in the number of parasites in the peripheral circulation (van Riper et al., 1994). The hallmark gross lesions produced by acute infections with Plasmodium spp. include thin, watery blood and enlargement and discoloration of the liver and spleen by deposition of malarial pigment in tissue macrophages. Development of gross lesions closely corresponds to a steady increase in peripheral parasitaemia, intravascular haemolysis of infected erythrocytes as meronts mature, phagocytosis of parasitized erythrocytes, and increased fragility of unparasitized erythrocytes (Al-Dabagh, 1966; van Riper et al., 1994; Williams, 2005). Regenerative, haemolytic anaemia is associated with a drop in erythrocyte counts, replacement with immature erythrocytes, and drops in haemoglobin concentration that peak during the crisis. Anoxia and intravascular agglutinations of erythrocytes ("sludging" of blood) may lead to damage of endothelial cells lining the capillaries (Al-Dabagh, 1966). Deposition of malarial pigment in macrophages of various organs, particularly liver and spleen, as infected cells are removed from the circulation can be extensive. In intense fatal infections, thrombi or emboli can form in some organs, particularly the spleen. Secondary shock may also occur during the terminal stages of some acute infections, resulting from destruction of large numbers of infected and uninfected erythrocytes. Capillaries and venules may be dilated and exhibit increased permeability, oedema and stasis of blood flow. Haemorrhage may be evident within the capillaries. Lowered blood pressure, lowered blood volume, disturbed fluid balance, increased coagulation times, and increased levels of potassium may also be evident in severe infections (Al-Dabagh, 1966).
DiagnosisTop of page
Birds infected with avian species of Plasmodium develop strong antibody and cell mediated responses to erythrocytic parasites (van Riper et al., 1994), but appear to be unable to completely clear their infections. Limited evidence based on experimental studies in canaries and Hawaii Amakihi (Hemignathus virens) indicates that birds likely remain infected for life, but at chronic levels that stimulate immunity to reinfection with homologous strains of the parasite (Bishop et al., 1938; Jarvi et al., 2002). This phenomenon, termed premunition, was recognized in the early part of the 20th century (Hewitt, 1940).
Because of the long duration of erythrocytic infections, the gold standard for diagnosis of Plasmodium parasites and the method of choice for field use in remote regions is microscopic examination of a Giemsa-stained thin blood smear where it is possible to demonstrate the presence of erythrocytic meronts and/or gametocytes with prominent golden-brown or black pigment granules. Individual species are traditionally defined by size and shape of intraerythrocytic gametocytes and meronts, number of merozoites produced by mature meronts, changes in morphology of the host erythrocyte, and other biological characteristics such as host range, susceptibility to species of mosquitoes, morphology and location of exoerythrocytic meronts (Garnham, 1966; Valkiunas, 2005). Since most identifications are made from blood smears, life history characteristics may be unknown and it becomes essential to be able to find enough mature meronts and gametocytes on a smear to be able to make an accurate assessment of parasite morphology. Detailed keys and species descriptions have been recently revised by Valkiunas (2005) and his monograph is currently the most up-to-date resource for identifying species of avian Plasmodium.
Most infections of Plasmodium parasites in wild birds are chronic, however, and intensity may be extremely low. In these cases, it may be impossible to identify parasites below the level of subgenus. When erythrocytic meronts are not present, it may become difficult to distinguish gametocytes of Plasmodium parasites from those of the closely related genus Haemoproteus. In these situations, PCR (polymerase chain reaction) amplification of portions of the parasite mitochondrial genome can distinguish Haemoproteus from Plasmodium and identify specific lineages of P. relictum if PCR products are sequenced (Hellgren, et al. 2004; Beadell and Fleischer, 2005; Beadell et al., 2006; Palinauskas et al., 2007). However, currently used PCR-based diagnostic methods underestimate co-infections of malaria parasites, and so should preferably be used in parallel with microscopy (Valkiunas et al., 2006).
Plasmodium appears to be antigenically distinct from Haemoproteus and crude antigen extracts have been used to develop an ELISA (enzyme linked immunosorbent assay) test for antibodies to P. relictum in captive and wild penguins (Graczyk et al., 1994b). Standard immunoblotting techniques can also be used to identify antibodies to Plasmodium parasites in wild and experimentally-infected passerines (Atkinson et al., 2001a), but neither method can distinguish species of Plasmodium. These serological techniques are useful for making diagnoses to the level of genus in birds with low intensity infections that may be missed by microscopy or PCR, particularly during the latent phase of infection.
List of Symptoms/SignsTop of page
|Digestive Signs / Anorexia, loss or decreased appetite, not nursing, off feed||Sign|
|Digestive Signs / Hepatosplenomegaly, splenomegaly, hepatomegaly||Sign|
|General Signs / Generalized weakness, paresis, paralysis||Sign|
|General Signs / Increased mortality in flocks of birds||Sign|
|General Signs / Lack of growth or weight gain, retarded, stunted growth||Sign|
|General Signs / Pale comb and or wattles in birds||Sign|
|General Signs / Pale mucous membranes or skin, anemia||Sign|
|General Signs / Reluctant to move, refusal to move||Sign|
|General Signs / Sudden death, found dead||Sign|
|General Signs / Underweight, poor condition, thin, emaciated, unthriftiness, ill thrift||Sign|
|General Signs / Weight loss||Sign|
|Nervous Signs / Dullness, depression, lethargy, depressed, lethargic, listless||Sign|
|Respiratory Signs / Increased respiratory rate, polypnea, tachypnea, hyperpnea||Sign|
|Skin / Integumentary Signs / Ruffled, ruffling of the feathers||Sign|
Disease CourseTop of page
During acute phases of infection with P. relictum, the number of parasites in the peripheral circulation increases steadily and reaches a peak or crisis approximately 9 days after parasites first appear in the blood. The number of circulating parasites begins to drop rapidly after the crisis, when the host immune response begins to control the infection. Haematocrits may fall by more than 50% as infected erythrocytes are ruptured by developing parasites and removed from the circulation by the spleen and phagocytic cells of the reticuloendothelial system. Increases in white blood cell counts, relative and absolute lymphocytosis and total plasma solids have been documented in Hawaiian Crows (Corvus hawaiiensis), penguins and other birds with acute infections with P. relictum (Graczyk et al., 1994a; Massey et al., 1996; Palinauskas et al., 2008). Haematological changes are much less evident in birds with chronic infections and birds are usually asymptomatic (Ricklefs and Sheldon, 2007; Atkinson et al., 2001a). Simultaneous P. relictum infections with other malaria parasites are common; such infections are highly virulent and often act synergetically (Palinauskas et al., 2011).
EpidemiologyTop of page
P. relictum is an intracellular protozoan parasite with a complex life cycle that involves alternating sexual and asexual phases of reproduction and obligate, temperature-dependent development within a suitable mosquito vector. The life cycle begins when infective sporozoites are inoculated by a mosquito vector into a susceptible host. Sporozoites invade macrophages and fibroblasts near the site of the mosquito bite and undergo asexual reproduction (termed merogony or schizogony) as cryptozoites. These mature in approximately 36 to 48 hours and release ovoid merozoites that invade cells of the lymphoid-macrophage system in brain, spleen, kidney, lung, and liver tissue to begin a second generation of asexual merogony as metacryptozoites. Metacryptozoites mature and release merozoites that are capable of invading circulating erythrocytes and capillary endothelial cells of the major organs. Merozoites that continue with a third generation of merogony in fixed tissues of the host are called phanerozoites and produce merozoites that can either invade circulating erythrocytes or reinvade endothelial cells to continue additional generations of merogony in fixed tissues. Merozoites that invade the circulating erythrocytes develop within 36 hours into either mature segmenters containing 8 to 32 ovoid merozoites or gametocytes that are infective to mosquito vectors. Merogony can continue indefinitely in the peripheral circulation and evidence suggests that merozoites from some erythrocytic meronts can reinvade fixed tissues and continue development as phanerozoites (Garnham, 1966; Atkinson, 2008).
When a suitable mosquito vector takes a blood meal from an infected bird, circulating gametocytes undergo gametogenesis in the midgut or stomach of the mosquito to produce mature female macrogametes and mature male microgametes. Fertilization takes place in the midgut and produces a zygote, which undergoes meiosis to form a mobile ookinete. The ookinete penetrates the peritrophic membrane that surrounds the digesting blood meal and the midgut epithelium and moves to the basal lamina of the mosquito midgut. Here it rounds up and differentiates into an oocyst. The oocyst grows and undergoes asexual reproduction or sporogony to produce thousands of elongate sporozoites that bud from the surface of residual bodies within the oocyst. When mature, the oocyst ruptures, releasing sporozoites into the haemocoel of the mosquito. They subsequently penetrate the salivary glands and accumulate within the salivary ducts and lobes, eventually passing into a new host through the salivary ducts with the next blood meal (Garnham, 1966; Atkinson, 2008).
More than 20 species of anopheline and culicine mosquitoes in four different genera (Culex, Aedes, Culiseta, and Anopheles) are capable of transmitting P. relictum in the laboratory, but only four - Culex quinquefasciatus, Culex tarsalis, Culex pipiens and Culex stigmatasoma - are proven natural vectors of P. relictum in the wild (Reeves et al., 1954; LaPointe et al., 2005; Woodworth et al., 2005; Valkiunas, 2005).
Transmission of P. relictum in the wild is seasonal in temperate habitats and typically follows a spring relapse in chronically-infected adult birds, where numbers of parasites in the peripheral circulation increase. This relapse or recrudescence of infective stages of the parasites coincides with seasonal increases in mosquito vectors and hatching of highly susceptive juvenile birds (Beaudoin et al., 1971). Transmission in more tropical climates can occur throughout the year when suitable vectors are present (Woodworth et al., 2005).
ImpactTop of page
P. relictum has had environmental impacts in the Hawaiian archipelago where it has contributed substantially to loss of biodiversity in native forest bird communities on the main Hawaiian Islands. Loss of ecosystem services such as pollination and seed dispersal have been compensated in part by replacement of native forest birds with introduced species.
Impact of P.relictum on wild birds more generally is poorly investigated in natural ecosystems, but experimental data show that it is virulent and might cause severe disease and even mortality in some wild birds (Palinauskas et al., 2011).
Zoonoses and Food SafetyTop of page
P. relictum is not a zoonotic threat in domestic poultry and poses no risk of transmission to humans.
Disease TreatmentTop of page
Chloroquine phosphate, primaquine phosphate, pyramethamine-sulfadoxine combinations, and mefloquine are effective in treating avian malaria (Remple, 2004). The anticoccidial drugs sulfamonomethoxine, sulfachloropyrazine, and halofuginone are somewhat effective in treating Plasmodium durae in domestic turkeys and may also be effective against P. relictum (Huchzermeyer et al., 1993). Palinauskas et al. (2009) found that Malarone™ (atovaquone/proguanil) was highly effective against blood stages of P. relictum, but exoerythrocytic stages were unaffected. Dosage and administration of treatments should be determined in consultation with a veterinarian.
Prevention and ControlTop of page
Immunization and Vaccines
While birds were some of the first experimental models for development of vaccines against Plasmodium parasites, practical methods for immunizing wild birds have not been developed and this probably presents the most significant challenge to controlling infection with this approach. A variety of different experimental vaccines have been used, including use of ultraviolet-light-inactivated, formalin-inactivated, and irradiated sporozoites, merozoites, and gametes, and synthetic vaccines based on parasite surface molecules (van Riper et al., 1994), but none are in current use. Two DNA vaccines based on the circumsporozoite protein of P. gallinaceum and P. relictum have recently been evaluated in Jackass Penguins (Spheniscus demersus) (Grim et al., 2004) and canaries (McCutchan et al., 2004) exposed to natural transmission of P. relictum in a zoological park. Both provided protection against natural exposure to P. relictum, but immunity was short lived in canaries, and vaccinated birds were just as susceptible as unvaccinated controls when exposed to mosquito vectors one year later.
As has been demonstrated with human malaria, reductions of populations of mosquito vectors can reduce transmission of Plasmodium parasites, but this method has not been widely used to control infections in wild or captive birds. Efforts to control avian malaria in Hawaiian forest birds have focused on reducing larval habitat for the introduced mosquito, Culex quinquefasciatus (LaPointe et al., 2008). The most cost-effective measures for captive or domestic birds include housing cage birds in screened, mosquito-proof buildings or locating birds in areas that are isolated from wild reservoir hosts.
ReferencesTop of page
Alley MR; Fairley RA; Martin DG; Howe L; Atkinson T, 2008. An outbreak of avian malaria in captive yellowheads/mohua (Mohoua ochrocephala). New Zealand Veterinary Journal, 56(5):247-251. http://www.vetjournal.org.nz
Atkinson CT; LaPointe DA, 2009. Introduced avian diseases, climate change, and the future of Hawaiian honeycreepers. Journal of Avian Medicine and Surgery, 23(1):53-63. http://www.bioone.org/perlserv/?request=get-current-issue
Atkinson CT; Lease JK; Drake BM; Shema NP, 2001. Pathogenicity, serological responses, and diagnosis of experimental and natural malarial infections in native Hawaiian thrushes. Condor, 103(2):209-218.
Atkinson CT; Utzurrum RC; Seamon JO; Savage AF; LaPointe DA, 2006. Hematozoa of forest birds in American Samoa - evidence for a diverse, indigenous parasite fauna from the South Pacific. Pacific Conservation Biology, 12:229-237.
Baldwin PH, 1941. Checklist of the birds of the Hawaii National Park, Kilauea-Mauna Loa Section, with remarks on their present status and a field key for their identification. Hawaii National Park Historical Bulletin 7:38 pp.
Beadell JS; Ishtiaq F; Covas R; Melo M; Warren BH; Atkinson CT; Bensch S; Graves GR; Jhala YV; Peirce MA; Rahmani AR; Fonseca DM; Fleischer RC, 2006. Global phylogeographic limits of Hawaii's avian malaria. Proceedings of the Royal Society of London. Series B, Biological Sciences, 273(1604):2935-2944. http://www.pubs.royalsoc.ac.uk/proc_bio_homepage.shtml
Bensch S; Stjernman M; Hasselquist D; Östman Ö; Hansson B; Westerdahl H; Pinheiro RT, 2000. Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society of London. Series B, Biological Sciences, 267(1452):1583-1589.
Bensch S; Waldenström J; Jonzén N; Westerdahl H; Hansson B; Sejberg D; Hasselquist D, 2007. Temporal dynamics and diversity of avian malaria parasites in a single host species. Journal of Animal Ecology, 76(1):112-122. http://www.blackwell-synergy.com/servlet/useragent?func=showIssues&code=jae
Berson JP, 1964. [English title not available]. (Les protozoaires parasites des hématies et du système histiocytaire des oiseaux. Essai de nomenclature.) Revue D'élevage et de Médicine Vétérinare des pays Tropicaux, 17:43-96.
Bishop MA; Bennett GF, 1992. Host-parasite catalogue of the avian haematozoa supplement 1 and bibliography of the avian blood-inhabiting haematozoa supplement 2. unpaginated. [Memorial University of Newfoundland Occasional Papers in Biology No 15.]
Bonneaud C; Pérez-Tris J; Federici P; Chastel O; Sorci G, 2006. Major histocompatibility alleles associated with local resistance to malaria in a passerine. Evolution, 60(2):383-389. http://lifesciences.asu.edu/evolution
Burtikashvili LP, 1973. A new species of blood parasite Haemoproteus zasukhini sp. nov. (Sporozoa, Haemoproteidae) from the house sparrow (Passer domesticus) in the Georgian SSR. (Novyi vid krovoparazita.) Soobshcheniya Akademii Nauk Gruzinskoi SSR, 72(3):697-700.
Cassamagnaghi A, 1950. Haemoproteosis: New contribution to knowledge of it in Uruguay. (Le haemoproteosis: Nueva contribucion para su conocimiento en el Uruguay.) Boletin Mensual Direccion de Ganaderia (Montevideo), 31:369-378.
Choudhury A; Misra KK; 1976, publ. 1980. A new species of trypanosome from a bird, the blackheaded shrike, Lanius schach tricolor (Hodgson). Proceedings of the Zoological Society, Calcutta, 29(1/2):29-45.
Derraik JGB; Tompkins DM; Alley MR; Holder P; Atkinson T, 2008. Epidemiology of an avian malaria outbreak in a native bird species (Mohoua ochrocephala) in New Zealand. Journal of the Royal Society of New Zealand, 38:237-242.
Durrant KL; Reed JL; Jones PJ; Dallimer M; Cheke RA; McWilliam AN; Fleischer RC, 2007. Variation in haematozoan parasitism at local and landscape levels in the red-billed quelea Quelea quelea. Journal of Avian Biology, 38(6):662-671. http://www.blackwell-synergy.com/loi/jav
Earlé RA; Bennett GF; Toit H du; Swardt DH de; Herholdt JJ, 1991. Regional and seasonal distribution of avian blood parasites from northern South Africa. South African Journal of Wildlife Research, 21(2):47-53.
Ejiri H; Sato Y; Sasaki E; Sumiyama D; Tsuda Y; Sawabe K; Matsui S; Horie S; Akatani K; Takagi M; Omori S; Murata K; Yukawa M, 2008. Detection of avian Plasmodium spp. DNA sequences from mosquitoes captured in Minami Daito Island of Japan. Journal of Veterinary Medical Science, 70(11):1205-1210. http://www.jstage.jst.go.jp/browse/jvms/-char/en
Fallon SM; Ricklefs RE, 2008. Parasitemia in PCR-detected Plasmodium and Haemoproteus infections in birds. Journal of Avian Biology, 39(5):514-522. http://www3.interscience.wiley.com/journal/121403026/abstract
Fix AS; Waterhouse C; Greiner EC; Stoskopf MK, 1988. Plasmodium relictum as a cause of avian malaria in wild-caught magellanic penguins (Spheniscus magellanicus). Journal of Wildlife Diseases, 24(4):610-619.
GABALDON A; ULLOA G; MONTCOURT AG, 1975. Survey of avian malaria in Venezuela. Results of second year. (Encuesta sobre malaria aviaria en Venezuela: Resultados del segundo año.) Boletin de la Direccion de Malariologia y Saneamiento Ambiental, 15(3/4):73-92.
Gajanana A; Naseema M, 1980. Occurrence of avian malaria parasite species with resemblance to Plasmodium (Novyella) hexamerium outside its recorded habitat. Indian Journal of Medical Research, 72(October):492-496.
Graczyk TK; Cranfield MR; McCutchan TF; Bicknese EJ, 1994. Characteristics of naturally acquired avian malaria infections in naive juvenile African black-footed penguins (Spheniscus demersus). Parasitology Research, 80(8):634-637.
Graczyk TK; Cranfield MR; Shiff CJ, 1993. ELISA method for detecting anti-Plasmodium relictum and anti-Plasmodium elongatum antibody in infected duckling sera using Plasmodium falciparum antigens. Journal of Parasitology, 79(6):879-885.
Graczyk TK; Cranfield MR; Skjoldager ML; Shaw ML, 1994. An ELISA for detecting anti-Plasmodium spp. Antibodies in African black-footed penguins (Spheniscus demersus). Journal of Parasitology, 80:60-66.
GREWAL MS, 1962. Studies on the Blood-Parasites of the White-Throated Munia, Uroloncha malabarica Linnaeus. Plasmodium (relictum) praecox Grassi and Feletti, 1890. Indian Journal of Malariology, 16(1):99-109.
Grim KC; McCutchan T; Li J; Sullivan M; Graczyk TK; McConkey G; Cranfield M, 2004. Preliminary results of an anticircumsporozoite DNA vaccine trial for protection against avian malaria in captive African black-footed penguins (Spheniscus demersus). Journal of Zoo and Wildlife Medicine, 35(2):154-161.
Hale KA, 2008. Disease outbreak amongst South Island saddlebacks (Philesturnus carunculatus carunculatus) on Long Island. Disease outbreak amongst South Island saddlebacks (Philesturnus carunculatus carunculatus) on Long Island. Wellington: Department of Conservation, 14 pp. [Research and Development Series 289.]
Hartup BK; Oberc A; Stott-Messick B; Davis AK; Swarthout ECH, 2008. Blood parasites of House Finches (Carpodacus mexicanus) from Georgia and New York. Journal of Wildlife Diseases, 44(2):469-474. http://www.wildlifedisease.org
Hellgren O; Waldenström J; Peréz-Tris J; Ösi ES; Hasselquist D; Krizanauskiene A; Ottosson U; Bensch S, 2007. Detecting shifts of transmission areas in avian blood parasites - a phylogenetic approach. Molecular Ecology, 16(6):1281-1290. http://www.blackwell-synergy.com/loi/mec
Herman CM; Gray C; Knisley JO Jr; Kocan RM, 1974. Malarial infections in the avian collection of the National Zoo in Washington, D.C., U.S.A. and in indigenous birds. In: Third International Congress of Parasitology. 1677-1678.
HERMAN CM; REEVES WC; McCLURE HE; FRENCH EM; HAMMON WMcD, 1954. Studies on Avian Malaria in Vectors and Hosts of Encephalitis in Kern County, California. I. Infections in Avian Hosts. American Journal of Tropical Medicine and Hygiene, 3(4):676-695 pp.
Ishtiaq F; Beadell JS; Baker AJ; Rahmani AR; Jhala YV; Fleischer RC, 2006. Prevalence and evolutionary relationships of haematozoan parasites in native versus introduced populations of common myna Acridotheres tristis. Proceedings of the Royal Society of London. Series B, Biological Sciences, 273(1586):587-594. http://www.pubs.royalsoc.ac.uk/proc_bio_homepage.shtml
Ishtiaq F; Gering E; Rappole JH; Rahmani AR; Jhala YV; Dove CJ; Milensky C; Olson SL; Peirce MA; Fleischer RC, 2007. Prevalence and diversity of avian hematozoan parasites in Asia: a regional survey. Journal of Wildlife Diseases, 43(3):382-398. http://www.wildlifedisease.org
Jacobs B; Shortt HE, 1951. Plasmodium relictum in the English blackbird. Blood and brain smears and sections showing exo-erythrocytic schizogony. Transactions of the Royal Society of Tropical Medicine and Hygiene, 44:356.
Jarvi SI; Schultz JJ; Atkinson CT, 2002. PCR diagnostics underestimate the prevalence of avian malaria (Plasmodium relictum) in experimentally-infected passerines. Journal of Parasitology, 88(1):153-158.
Kimura M; Dhondt AA; Lovette IJ, 2006. Phylogeographic structuring of Plasmodium lineages across the North American range of the house finch (Carpodacus mexicanus). Journal of Parasitology, 92(5):1043-1049.
Kobyshev NM; Markov GS; Ryzhikov KM, 1975. Ecological analysis of the parasitic fauna of common species of falconid birds from the lower Volga region. In: Parasity I Parazitozy Zhivotnykh. Kiev, USSR: Naukova Duma, 392 pp.
Krizanauskiene A; Hellgren O; Kosarev V; Sokolov L; Bensch S; Valkiunas G, 2006. Variation in host specificity between species of avian hemosporidian parasites: evidence from parasite morphology and cytochrome b gene sequences. Journal of Parasitology, 92(6):1319-1324.
Laird M; Van Riper C, 1981. Questionable reports of Plasmodium from birds in Hawaii, with the recognition of P. relictum ssp. capistranoae (Russell, 1932) as the avian malaria parasite there. Parasitological topics -- a presentation volume to P.C.C. Garnham, F.R.S. on the occasion of his 80th birthday, 1981 [ed. by : Canning, E.U.]. Lawrence, Kansas, USA: society of Protozoologists, Inc., 159-165.
LaPointe DA; Atkinson CT; Jarvi SI, 2008. Management of mosquito-borne disease in Hawaiian forest bird populations. In: Hawaiian forest birds: their biology and conservation [ed. by Pratt, T. K.\Atkinson, C. T.\Banko, P. C.\Jacobi, J.\Woodworth, B. L.]. New Haven, USA: Yale University Press, 405-424.
Levin II; Outlaw DC; Vargas FH; Parker PG, 2009. Plasmodium blood parasite found in endangered Galapagos penguins (Spheniscus mendiculus). Biological Conservation, 142(12):3191-3195. http://www.sciencedirect.com/science/journal/00063207
Martinsen ES; Paperna I; Schall JJ, 2006. Morphological versus molecular identification of avian Haemosporidia: an exploration of three species concepts. Parasitology, 133(3):279-288. http://journals.cambridge.org/
Marzal A; Bensch S; Reviriego M; Balbontin J; Lope F de, 2008. Effects of malaria double infection in birds: one plus one is not two. Journal of Evolutionary Biology, 21(4):979-987. http://www.blackwell-synergy.com/loi/jeb
Marzal A; Ricklefs RE; Valkiunas G; Albayrak T; Arriero E; Bonneaud C; Czirják GA; Ewen J; Hellgren O; Horáková D; Iezhova TA; Jensen H; Krizanauskiene A; Lima MR; Lope F de; Magnussen E; Martin LB; Møller AP; Palinauskas V; Pap PL; Pérez-Tris J; Sehgal RNM; Soler M; Szöllosi E; Westerdahl H, Zetindjiev P (et al. ), 2011. Diversity, loss, and gain of malaria parasites in a globally invasive bird. PLoS ONE, July:e21905. http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0021905
Massey JG; Graczyk TK; Cranfield MR, 1996. Characteristics of naturally acquired Plasmodium relictum capistranoae infections in naive Hawaiian crows (Corvus hawaiiensis) in Hawaii. Journal of Parasitology, 82(1):182-185.
McCutchan TF; Grim KC; Li J; Weiss W; Rathore D; Sullivan M; Graczyk TK; Kumar S; Cranfield MR, 2004. Measuring the effects of an ever-changing environment on malaria control. Infection and Immunity, 72(4):2248-2253. http://iai.asm.org/cgi/content/full/72/4/2248
Moulton MP; Miller KE; Tillman EA, 2001. Patterns of success among introduced birds in the Hawaiian Islands. In: Evolution, ecology, conservation and management of Hawaiian birds: a vanishing avifauna, 22 [ed. by Scott, J. M.\Conant, S.\Riper, C. van, III]. 31-46. [Cooper Ornithological Society: Studies in Avian Biology.]
Orbaneja Aguero S de, 1934. Observations on the parasitic protozoa of the blood of birds in Spain. (Observaciones sobre los protozoos parasitos del la sangre de aves en Espana.) Medicina de los Paises Calidos, 7:257-266.
Osipov PP; Kairullaev KK, 1984. Blood parasitic fauna of migratory birds in the Piedmont plain of the trans-Ilian Ala-Tau USSR. Izvestiya Akademii Nauk Kazakhskoi SSR Seriya Biologicheskikh Nauk:22-23.
Palinauskas V; Kosarev V; Shapoval A; Bensch S; Valkiunas G, 2007. Comparison of mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites of the subgenera haemamoeba and giovannolaia (Haemosporida: Plasmodiidae). Zootaxa, 1626:39-50.
Palinauskas V; Valkiunas G; Bolshakov CV; Bensch S, 2008. Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds. Experimental Parasitology, 120(4):372-380. http://www.sciencedirect.com/science/journal/00144894
Palinauskas V; Valkiunas G; Bolshakov CV; Bensch S, 2011. Plasmodium relictum (lineage SGS1) and Plasmodium ashfordi (lineage GRW2): the effects of the co-infection on experimentally infected passerine birds. Experimental Parasitology, 127(2):527-533. http://www.sciencedirect.com/science/journal/00144894
Palinauskas V; Valkiunas G; Krizanauskiene A; Bensch S; Bolshakov CV, 2009. Plasmodium relictum (lineage P-SGS1): further observation of effects on experimentally infected passeriform birds, with remarks on treatment with Malarone™. Experimental Parasitology, 123(2):134-139. http://www.sciencedirect.com/science/journal/00144894
Pérez-Reyes R; Pelaez D, 1953. [English title not available]. (Estudios sôbre hematozoàrios. IV. Compoortamieto de una cepa de Plasmodium relictum en palomas.) Revista del Instituto de Salubridad y Enfermedades Tropicales, 13:111-120.
Pérez-Tris J; Bensch S, 2005. Dispersal increases local transmission of avian malarial parasites. Ecology Letters, 8(8):838-845. http://www.blackwell-synergy.com/servlet/useragent?func=showIssues&code=ele
REEVES WC; HEROLD BC; ROSEN L; BROOKMAN B; HAMMON WMcD, 1954. Studies on Avian Malaria in Vectors and Hosts of Encephalitis in Kern County, California. II. Infections in Mosquito Vectors. American Journal of Tropical Medicine and Hygiene, 3(4):696-703.
RENJIFO SALCEDO S, 1950. [English title not available]. (Contribuciones a la parasitología Colombiana. II. Hemoparásitos de aves y otros vertebrados de los llanos orientales.) Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, 7(28):539-547.
Rey Vila F, 1945. Studies on some parasitic protozoa, in particular those of the genus Plasmodium, in the vertebrate host. (Estuidios sobre algunos protozoos paràsitos, en especial los del género Plasmodium, en el hospedador vertebrado.) Revista de sanidad e higiene pública, 19:81-101 and 145-159.
Ricklefs RE; Sheldon KS, 2007. Malaria prevalence and white-blood-cell response to infection in a tropical and in a temperate thrush. Auk, 124(4):1254-1266. http://www.bioone.org/archive/0004-8038/124/4/pdf/i0004-8038-124-4-1254.pdf
Riper SG van; Riper C van III, 1985. A summary of known parasites and diseases recorded from the avifauna of the Hawaiian Islands. In: Hawai'i's Terrestrial Ecosystems: Preservation and Management [ed. by Stone, C. P.\Scott, J. M.]. Honolulu, USA: University of Hawaii, Cooperative National Park Resources Studies Unit, 298-371.
RODHAIN J, 1938. Non-pigmented Schizonts In Penguins infected with P. praecox. (Schizogonie sans pigment chez les pingouins infectes de Plasmodium praecox (relictum).) Compte rendu des seances de la Societe de biologie, 127(4):368-372 pp.
Schwetz J, 1935. [English title not available]. (Sur un Haemoproteus et deux Plasmodium du hibou Syrnium nuchale et sur les Plasmodium d'un petit tisserin Africain Brachycope anomalia (Fam. Ploceidae).) Comptes rendus des séances de la Société de biologie et de ses filiales, 118:815-818.
Sergent E; Sergent E, 1907. Studies on the haematozoa of birds, Plasmodium relictum, Leucocytozoon ziemanni, Haemoproteus noctuae, Haemoproteus columbae, swallow trypanosome. Algeria, 1906: infection of Stegomyia fasciata by Plasmodium relictum. (Études sur les hématozoaires d'oiseaux, Plasmodium relictum, Leucocytozoon ziemanni, Haemoproteus noctuae, Haemoproteus columbae, trypanosome de l'hirondelle. Algérie, 1906: infection de Stegomyia fasciata par Plasmodium relictum.) Annales de l'Institut Pasteur (Paris), 21:251-280.
SERGENT Ed; SERGENT Et, 1948. Haemoproteus wenyoni sp. nov. Parasite of the Algerian Sparrow, recovered in Cage Reared Canaries. (Haemoproteus wenyoni nov. sp., parasite du moineau algérien retrouvé chez des canaris élevés en cage.) Arch. Inst. Pasteur d'Algerie, 26(4):394-6.
Shamsuddin M; Mohammad MK, 1981. Haematozoa of some Iraqi birds with description of two new species, Haemoproteus pteroclis and Leucocytozoon nycticoraxi (Protozoa: Haemosporina). Bulletin of the Natural History Research Centre, Baghdad, 7(4):111-155.
Shehata C; Freed L; Cann RL, 2001. Changes in native and introduced bird populations on O'ahu: infectious diseases and species replacement. In: Evolution, ecology, conservation and management of Hawaiian birds: a vanishing avifauna, 22 [ed. by Scott, J. M.\Conant, S.\Riper, C. van, III]. Lawrence, USA: Cooper Ornithological Society, 64-273. [Cooper Ornithological Society, Studies in Avian Biology.]
SINGH J; NAIR CP; DAVID A, 1951. Five Years' Observation on the Incidence of Blood Protozoa in House Sparrows (Passer domesticus Linnaeus) and in Pigeons (Columba livia Gmelin) in Delhi. Indian Journal of Malariology, 5(2):229-33.
Sladen WJL; Gailey-Phipps JJ; Divers BJ, 1979. Medical problems and treatments of penguins at the Baltimore Zoo. International Zoo Yearbook, Volume 19 [ed. by : Olney, P.J.S.]. London, UK: Zoological Society of London., 202-209.
Sturrock HJW; Tompkins DM, 2007. Avian malaria (Plasmodium spp.) in yellow-eyed penguins: investigating the cause of high seroprevalence but low observed infection. New Zealand Veterinary Journal, 55(4):158-160. http://www.vetjournal.org.nz
Subkhonov M, 1972. Malaria parasites in the birds of Tadzhikistan. In: Voprosy Zoologii Tadzhikistana, Trudy Instituta Zoologii i Parazitologii [ed. by Narzkiulov, M. N.\Abdusalyamov, I. A.]. Dushanbe: Donish, USSR: Akademia Nauk Tadzhikskoi SSR, 279-286.
Sulgostowska T; Czaplinska D, 1987. Catalogue of the parasite fauna of Poland. Part IV. Parasites of birds. No. 1 Protozoa and Trematoda. (Katalog fauny pasozytniczej Polski. Czesc IV. Pasozyty ptaków. Zeszyt 1. Pierwotniaki i przywry.) Warsaw, Poland: Panstwowe Wydawnictwo Naukowe, 210 pp.
Szöllosi E; Rosivall B; Hasselquist D; Török J, 2009. The effect of parental quality and malaria infection on nestling performance in the Collared Flycatcher (Ficedula albicollis). Journal of Ornithology, 150(3):519-527. http://springerlink.metapress.com/content/nw534862311473v4/?p=fead500264bc4cf4b3c00b7db8eb0695&pi=0
Tompkins DM; Gleeson DM, 2006. Relationship between avian malaria distribution and an exotic invasive mosquito in New Zealand. Journal of the Royal Society of New Zealand, 36(2):51-62. http://www.rsnz.org/publish/jrsnz/
Valkiunas G; Bensch S; Iezhova TA; Krizanauskiene A; Hellgren O; Bolshakov CV, 2006. Nested cytochrome b polymerase chain reaction diagnostics underestimate mixed infections of avian blood haemosporidian parasites: microscopy is still essential. Journal of Parasitology, 92(2):418-422.
Valkiunas G; Zehtindjiev P; Hellgren O; Ilieva M; Iezhova TA; Bensch S, 2007. Linkage between mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites, with a description of Plasmodium (Novyella) ashfordi sp. nov. Parasitology Research, 100(6):1311-1322. http://www.springerlink.com/link.asp?id=100447
Vanderwerf EA; Burt MD; Rohrer JL; Mosher SM, 2006. Distribution and prevalence of mosquito-borne diseases in O'ahu 'Elepaio. Condor, 108(4):770-777. http://www.bioone.org/perlserv/?request=get-document&doi=10.1650%2F0010-5422%282006%29108%5B770%3ADAPOMD%5D2.0.CO%3B2
Westerdahl H; Waldenström J; Hansson B; Hasselquist D; Schantz Tvon; Bensch S, 2005. Associations between malaria and MHC genes in a migratory songbird. Proceedings of the Royal Society of London. Series B, Biological Sciences, 272(1571):1511-1518. http://www.pubs.royalsoc.ac.uk/proc_bio_homepage.shtml
Whiteman NK; Goodman SJ; Sinclair BJ; Walsh T; Cunningham AA; Kramer LD; Parker PG, 2005. Establishment of the avian disease vector Culex quinquefasciatus Say, 1823 (Diptera: Culicidae) on the Galápagos Islands, Ecuador. Ibis (London), 147(4):844-847. http://www.blackwell-synergy.com/servlet/useragent?func=showIssues&code=ibi
Williams RB, 2005. Avian malaria: clinical and chemical pathology of Plasmodium gallinaceum in the domesticated fowl Gallus gallus. Avian Pathology, 34(1):29-47. http://taylorandfrancis.metapress.com/link.asp?id=102204
Wood MJ; Cosgrove CL; Wilkin TA; Knowles SCL; Day KP; Sheldon BC, 2007. Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus. Molecular Ecology, 16(15):3263-3273. http://www.blackwell-synergy.com/loi/mec
Woodworth BL; Atkinson CT; LaPointe DA; Hart PJ; Spiegel CS; Tweed EJ; Henneman C; LeBrun J; Denette T; DeMots R; Kozar KL; Triglia D; Lease D; Gregor A; Smith T; Duffy D, 2005. Host population persistence in the face of introduced vector-borne diseases: Hawaii amakihi and avian malaria. Proceedings of the National Academy of Sciences of the United States of America, 102(5):1531-1536. http://www.pnas.org/
Yakunin MP, 1976. Parasitic protozoa from the blood of wild birds in Kazakhstan. (Paraziticheskie prosteishie krovi dikikh ptits Kazakhstana.) Materialy II Vsesoyuznogo S"ezda Protozoologov. Chast' 1. Obshchaya protozoologiya. Kiev, USSR: "Naukova Dumka"., 166-167.
Yohannes E; Hansson B; Lee RW; Waldenström J; Westerdahl H; Akesson M; Hasselquist D; Bensch S, 2008. Isotope signatures in winter moulted feathers predict malaria prevalence in a breeding avian host. Oecologia, 158(2):299-306. http://springerlink.metapress.com/content/h2rjj20457737j87/fulltext.html
Zehtindjiev P; Ilieva M; Krizanauskiene A; Oparina O; Oparin M; Bensch S, 2009. Occurrence of haemosporidian parasites in the paddyfield warbler, Acrocephalus agricola (Passeriformes, Sylviidae). Acta Parasitologica, 54(4):295-300. http://www.springerlink.com/content/j17j126180n13317/?p=1212d86a2ba34c43812cceab35536dc6&pi=1
Zehtindjiev P; Ilieva M; Westerdahl H; Hansson B; Valkiunas G; Bensch S, 2008. Dynamics of parasitemia of malaria parasites in a naturally and experimentally infected migratory songbird, the great reed warbler Acrocephalus arundinaceus. Experimental Parasitology, 119(1):99-110. http://www.sciencedirect.com/science/journal/00144894
Zeiniev NR, 1975. Parasitic blood protozoa from birds in north-eastern Azerbaidzhan. (Parasiticheskie prosteishie krovi ptits severo-vostochnogo Azerbaidzhana.) Izvestiya Akademii Nauk Azerbaidzhanskoi SSR (AZarbajcan SSR Elmlar Akademijasynyn Habarlari), Biologicheskie Nauk, 4:86-89.
OrganizationsTop of page
USA: U.S. Geological Survey, Pacific Island Ecosystems Research Center, PO Box 44, Hawaii National Park, Hawaii 96718, http://biology.usgs.gov/pierc/
ContributorsTop of page
03/11/09 Original text by:
Carter Atkinson, USGS Pacific Island Ecosystems Research Center, Kilauea Field Station, P.O. Box 44, Bldg 343, Hawaii National Park, HI 96718, USA
Distribution MapsTop of page
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