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Plasmodium relictum infection

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Datasheet

Plasmodium relictum infection

Summary

  • Last modified
  • 26 September 2017
  • Datasheet Type(s)
  • Animal Disease
  • Preferred Scientific Name
  • Plasmodium relictum infection
  • Overview
  • Plasmodium relictum is one of more than 40 species of Plasmodium that can infect birds and cause avian malaria (Valkiunas, 2005). This disea...

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PictureTitleCaptionCopyright
Composite figure for comparison: See individual figures for specific caption data.
TitleHistology - Composite comparison figure
CaptionComposite figure for comparison: See individual figures for specific caption data.
CopyrightU.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Composite figure for comparison: See individual figures for specific caption data.
Histology - Composite comparison figureComposite figure for comparison: See individual figures for specific caption data.U.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Early (left (a)) and late (right (b)) trophozoites (arrowed) of Plasmodium relictum in erythrocytes of an endangered Puaiohi (Myadestes palmeri).  Golden brown or black pigment granules (P) are produced as a by-product of haemoglobin digestion and are usually not visible in young trophozoites (left).
TitleHistology
CaptionEarly (left (a)) and late (right (b)) trophozoites (arrowed) of Plasmodium relictum in erythrocytes of an endangered Puaiohi (Myadestes palmeri). Golden brown or black pigment granules (P) are produced as a by-product of haemoglobin digestion and are usually not visible in young trophozoites (left).
CopyrightU.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Early (left (a)) and late (right (b)) trophozoites (arrowed) of Plasmodium relictum in erythrocytes of an endangered Puaiohi (Myadestes palmeri).  Golden brown or black pigment granules (P) are produced as a by-product of haemoglobin digestion and are usually not visible in young trophozoites (left).
HistologyEarly (left (a)) and late (right (b)) trophozoites (arrowed) of Plasmodium relictum in erythrocytes of an endangered Puaiohi (Myadestes palmeri). Golden brown or black pigment granules (P) are produced as a by-product of haemoglobin digestion and are usually not visible in young trophozoites (left).U.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Multinucleated meront (or schizont) of Plasmodium relictum in erythrocyte of an endangered Puaoihi (Myadestes palmeri).  Red, grape-like nuclei (arrowed) surround a central residual mass of pigment (P).  As the meront matures, nuclei will bud into developing merozoites that are released when the infected host cell ruptures.  Each merozoite can invade another erythrocyte to start another round of asexual reproduction.
TitleHistology
CaptionMultinucleated meront (or schizont) of Plasmodium relictum in erythrocyte of an endangered Puaoihi (Myadestes palmeri). Red, grape-like nuclei (arrowed) surround a central residual mass of pigment (P). As the meront matures, nuclei will bud into developing merozoites that are released when the infected host cell ruptures. Each merozoite can invade another erythrocyte to start another round of asexual reproduction.
CopyrightU.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Multinucleated meront (or schizont) of Plasmodium relictum in erythrocyte of an endangered Puaoihi (Myadestes palmeri).  Red, grape-like nuclei (arrowed) surround a central residual mass of pigment (P).  As the meront matures, nuclei will bud into developing merozoites that are released when the infected host cell ruptures.  Each merozoite can invade another erythrocyte to start another round of asexual reproduction.
HistologyMultinucleated meront (or schizont) of Plasmodium relictum in erythrocyte of an endangered Puaoihi (Myadestes palmeri). Red, grape-like nuclei (arrowed) surround a central residual mass of pigment (P). As the meront matures, nuclei will bud into developing merozoites that are released when the infected host cell ruptures. Each merozoite can invade another erythrocyte to start another round of asexual reproduction.U.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Mature macrogametocyte (arrow) in erythrocyte of an endangered Puaiohi (Myadestes palmeri). Female (macrogametocytes) and male (microgametocytes) develop from merozoites and are infectious to mosquitoes.  Macrogametocytes typically stain dark blue and have a single, small compact central nucleus and a number of pigment granules (P). Among members of the subgenus Haemamoeba, gametocytes are typically round or oval and exceed the size of the host cell nucleus (N). The host cell nucleus is usually displaced to one side of the erythrocyte and may be partially or completely turned.
TitleHistology
CaptionMature macrogametocyte (arrow) in erythrocyte of an endangered Puaiohi (Myadestes palmeri). Female (macrogametocytes) and male (microgametocytes) develop from merozoites and are infectious to mosquitoes. Macrogametocytes typically stain dark blue and have a single, small compact central nucleus and a number of pigment granules (P). Among members of the subgenus Haemamoeba, gametocytes are typically round or oval and exceed the size of the host cell nucleus (N). The host cell nucleus is usually displaced to one side of the erythrocyte and may be partially or completely turned.
CopyrightU.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Mature macrogametocyte (arrow) in erythrocyte of an endangered Puaiohi (Myadestes palmeri). Female (macrogametocytes) and male (microgametocytes) develop from merozoites and are infectious to mosquitoes.  Macrogametocytes typically stain dark blue and have a single, small compact central nucleus and a number of pigment granules (P). Among members of the subgenus Haemamoeba, gametocytes are typically round or oval and exceed the size of the host cell nucleus (N). The host cell nucleus is usually displaced to one side of the erythrocyte and may be partially or completely turned.
HistologyMature macrogametocyte (arrow) in erythrocyte of an endangered Puaiohi (Myadestes palmeri). Female (macrogametocytes) and male (microgametocytes) develop from merozoites and are infectious to mosquitoes. Macrogametocytes typically stain dark blue and have a single, small compact central nucleus and a number of pigment granules (P). Among members of the subgenus Haemamoeba, gametocytes are typically round or oval and exceed the size of the host cell nucleus (N). The host cell nucleus is usually displaced to one side of the erythrocyte and may be partially or completely turned.U.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Mature microgametocyte (arrow) in erythrocyte of an endangered Puaiohi (Myadestes palmeri). Female (macrogametocytes) and male (microgametocytes) develop from merozoites and are infectious to mosquitoes.  Microgametocytes typically stain pink or light blue, depending on staining, and have a single, large diffuse central nucleus and a number of pigment granules (P). Among members of the subgenus Haemamoeba, gametocytes are typically round or oval and exceed the size of the host cell nucleus (N). The host cell nucleus is usually displaced to one side of the erythrocyte and may be partially or completely turned.
TitleHistology
CaptionMature microgametocyte (arrow) in erythrocyte of an endangered Puaiohi (Myadestes palmeri). Female (macrogametocytes) and male (microgametocytes) develop from merozoites and are infectious to mosquitoes. Microgametocytes typically stain pink or light blue, depending on staining, and have a single, large diffuse central nucleus and a number of pigment granules (P). Among members of the subgenus Haemamoeba, gametocytes are typically round or oval and exceed the size of the host cell nucleus (N). The host cell nucleus is usually displaced to one side of the erythrocyte and may be partially or completely turned.
CopyrightU.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Mature microgametocyte (arrow) in erythrocyte of an endangered Puaiohi (Myadestes palmeri). Female (macrogametocytes) and male (microgametocytes) develop from merozoites and are infectious to mosquitoes.  Microgametocytes typically stain pink or light blue, depending on staining, and have a single, large diffuse central nucleus and a number of pigment granules (P). Among members of the subgenus Haemamoeba, gametocytes are typically round or oval and exceed the size of the host cell nucleus (N). The host cell nucleus is usually displaced to one side of the erythrocyte and may be partially or completely turned.
HistologyMature microgametocyte (arrow) in erythrocyte of an endangered Puaiohi (Myadestes palmeri). Female (macrogametocytes) and male (microgametocytes) develop from merozoites and are infectious to mosquitoes. Microgametocytes typically stain pink or light blue, depending on staining, and have a single, large diffuse central nucleus and a number of pigment granules (P). Among members of the subgenus Haemamoeba, gametocytes are typically round or oval and exceed the size of the host cell nucleus (N). The host cell nucleus is usually displaced to one side of the erythrocyte and may be partially or completely turned.U.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Giemsa-stained blood smear from an Iiwi (Vestiaria coccinea) with an acute infection with Plasmodium relictum. The normal cellular makeup of the blood is severely altered, with mature erythrocytes being replaced by immature erythrocytes (reticulocytes, R) and erythrocyte precursors (EP) as the bird struggles to compensate for destruction of red blood cells by the parasites. Most of the red blood cells are parasitized (P) with trophozoites and meronts.
TitleHistology
CaptionGiemsa-stained blood smear from an Iiwi (Vestiaria coccinea) with an acute infection with Plasmodium relictum. The normal cellular makeup of the blood is severely altered, with mature erythrocytes being replaced by immature erythrocytes (reticulocytes, R) and erythrocyte precursors (EP) as the bird struggles to compensate for destruction of red blood cells by the parasites. Most of the red blood cells are parasitized (P) with trophozoites and meronts.
CopyrightU.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Giemsa-stained blood smear from an Iiwi (Vestiaria coccinea) with an acute infection with Plasmodium relictum. The normal cellular makeup of the blood is severely altered, with mature erythrocytes being replaced by immature erythrocytes (reticulocytes, R) and erythrocyte precursors (EP) as the bird struggles to compensate for destruction of red blood cells by the parasites. Most of the red blood cells are parasitized (P) with trophozoites and meronts.
HistologyGiemsa-stained blood smear from an Iiwi (Vestiaria coccinea) with an acute infection with Plasmodium relictum. The normal cellular makeup of the blood is severely altered, with mature erythrocytes being replaced by immature erythrocytes (reticulocytes, R) and erythrocyte precursors (EP) as the bird struggles to compensate for destruction of red blood cells by the parasites. Most of the red blood cells are parasitized (P) with trophozoites and meronts.U.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Oocysts of Plasmodium relictum on the outer midgut wall of Culex quinquefasciatus.  The oocysts are spherical in shape and at maturity contain thousands of elongate sporozoites (arrows).  These are released into the haemocoel when the oocysts rupture, travel to the salivary glands, and are injected into a new host when the mosquito takes another blood meal.
TitleHistology
CaptionOocysts of Plasmodium relictum on the outer midgut wall of Culex quinquefasciatus. The oocysts are spherical in shape and at maturity contain thousands of elongate sporozoites (arrows). These are released into the haemocoel when the oocysts rupture, travel to the salivary glands, and are injected into a new host when the mosquito takes another blood meal.
CopyrightU.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Oocysts of Plasmodium relictum on the outer midgut wall of Culex quinquefasciatus.  The oocysts are spherical in shape and at maturity contain thousands of elongate sporozoites (arrows).  These are released into the haemocoel when the oocysts rupture, travel to the salivary glands, and are injected into a new host when the mosquito takes another blood meal.
HistologyOocysts of Plasmodium relictum on the outer midgut wall of Culex quinquefasciatus. The oocysts are spherical in shape and at maturity contain thousands of elongate sporozoites (arrows). These are released into the haemocoel when the oocysts rupture, travel to the salivary glands, and are injected into a new host when the mosquito takes another blood meal.U.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Hematocrit tubes from a wild Apapane (Himatione sanguinea) with a naturally acquired infection with Plasmodium relictum (a) and an uninfected canary (b) for comparison.  After blood was collected into the heparinized tubes, they were sealed at one end with clay and centrifuged at high speed to separate erythrocytes and white blood cells from plasma.  Among most passerines, the hematocrit or volume of packed cells is about 50%.  Birds with acute malaria typically have much lower hematocrits as a result of red blood cell destruction.
TitleHematocrit tubes
CaptionHematocrit tubes from a wild Apapane (Himatione sanguinea) with a naturally acquired infection with Plasmodium relictum (a) and an uninfected canary (b) for comparison. After blood was collected into the heparinized tubes, they were sealed at one end with clay and centrifuged at high speed to separate erythrocytes and white blood cells from plasma. Among most passerines, the hematocrit or volume of packed cells is about 50%. Birds with acute malaria typically have much lower hematocrits as a result of red blood cell destruction.
CopyrightU.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Hematocrit tubes from a wild Apapane (Himatione sanguinea) with a naturally acquired infection with Plasmodium relictum (a) and an uninfected canary (b) for comparison.  After blood was collected into the heparinized tubes, they were sealed at one end with clay and centrifuged at high speed to separate erythrocytes and white blood cells from plasma.  Among most passerines, the hematocrit or volume of packed cells is about 50%.  Birds with acute malaria typically have much lower hematocrits as a result of red blood cell destruction.
Hematocrit tubesHematocrit tubes from a wild Apapane (Himatione sanguinea) with a naturally acquired infection with Plasmodium relictum (a) and an uninfected canary (b) for comparison. After blood was collected into the heparinized tubes, they were sealed at one end with clay and centrifuged at high speed to separate erythrocytes and white blood cells from plasma. Among most passerines, the hematocrit or volume of packed cells is about 50%. Birds with acute malaria typically have much lower hematocrits as a result of red blood cell destruction.U.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Hawaii Amakihi with an acute infection with Plasmodium relictum. When the abdominal cavity is opened, enlargement and discoloration of the liver (arrow) is immediately apparent and, in combination with a stained blood smear, is an important diagnostic criterion for acute malarial infection.
TitlePathology
CaptionHawaii Amakihi with an acute infection with Plasmodium relictum. When the abdominal cavity is opened, enlargement and discoloration of the liver (arrow) is immediately apparent and, in combination with a stained blood smear, is an important diagnostic criterion for acute malarial infection.
CopyrightU.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Hawaii Amakihi with an acute infection with Plasmodium relictum. When the abdominal cavity is opened, enlargement and discoloration of the liver (arrow) is immediately apparent and, in combination with a stained blood smear, is an important diagnostic criterion for acute malarial infection.
PathologyHawaii Amakihi with an acute infection with Plasmodium relictum. When the abdominal cavity is opened, enlargement and discoloration of the liver (arrow) is immediately apparent and, in combination with a stained blood smear, is an important diagnostic criterion for acute malarial infection.U.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Spleens (top) and livers (bottom) from a canary with an acute infection with Plasmodium relictum (left) and an uninfected canary (right). Both the liver and spleen increase dramatically in size during acute infections and become darkly discoloured by deposition of pigment in tissue macrophages.
TitlePathology
CaptionSpleens (top) and livers (bottom) from a canary with an acute infection with Plasmodium relictum (left) and an uninfected canary (right). Both the liver and spleen increase dramatically in size during acute infections and become darkly discoloured by deposition of pigment in tissue macrophages.
CopyrightU.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
Spleens (top) and livers (bottom) from a canary with an acute infection with Plasmodium relictum (left) and an uninfected canary (right). Both the liver and spleen increase dramatically in size during acute infections and become darkly discoloured by deposition of pigment in tissue macrophages.
PathologySpleens (top) and livers (bottom) from a canary with an acute infection with Plasmodium relictum (left) and an uninfected canary (right). Both the liver and spleen increase dramatically in size during acute infections and become darkly discoloured by deposition of pigment in tissue macrophages.U.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
The southern house mosquito (Culex quinquefasciatus) is a proven natural vector of Plasmodium relictum in Hawaii and other parts of the world.
TitleNatural vector
CaptionThe southern house mosquito (Culex quinquefasciatus) is a proven natural vector of Plasmodium relictum in Hawaii and other parts of the world.
CopyrightU.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii
The southern house mosquito (Culex quinquefasciatus) is a proven natural vector of Plasmodium relictum in Hawaii and other parts of the world.
Natural vector The southern house mosquito (Culex quinquefasciatus) is a proven natural vector of Plasmodium relictum in Hawaii and other parts of the world.U.S. Geological Survey/Pacific Island Ecosystems Research Center, Hawaii

Identity

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Preferred Scientific Name

  • Plasmodium relictum infection

International Common Names

  • English: avian malaria

Overview

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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 Affected

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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.

Distribution

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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 Table

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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/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

ArmeniaPresentNative Not invasive Karaseferyan, 1959
AzerbaijanPresentNative Not invasive Zeiniev, 1975
Georgia (Republic of)PresentNative Not invasive Burtikashvili, 1978
IndiaPresentNative Not invasive Beadell et al., 2006; Ishtiaq et al., 2007; Marzal et al., 2011Lineages GRW4, SGS1
IndonesiaPresentNative Not invasive McClure et al., 1978
IraqPresentNative Not invasive Shamsuddin and Mohammad, 1981
IsraelPresentNative Not invasive Bensch et al., 2000; Beadell et al., 2006; Martinsen et al., 2006; Marzal et al., 2011Lineages GRW4, SGS1
JapanPresentNative Not invasive Beadell et al., 2006; Ejiri et al., 2008Lineage GRW4
KazakhstanPresentNative Not invasive Yakunin and Zhazyltaev, 1977
Korea, Republic ofPresentNative Not invasive Beadell et al., 2006Lineages GRW4, SGS1.
KyrgyzstanPresentNative Not invasive Kairullaev and Yakunin, 1982
MalaysiaPresentNative Not invasive Laird, 1998
MyanmarPresentNative Not invasive Beadell et al., 2006
PakistanPresentNative Not invasive Lari, 1959
PhilippinesPresentNative Not invasive McClure et al., 1978
SingaporePresentNative Not invasive Beadell et al., 2006
TaiwanPresentNative Not invasive Manwell et al., 1976
TajikistanPresentNative Not invasive Subkhonov, 1972
ThailandPresentNative Not invasive McClure et al., 1978
TurkeyPresentNative Not invasive Marzal et al., 2011Lineages SGS1 and GRW11

Africa

AlgeriaPresentNative Not invasive Sergent and Sergent, 1904
BotswanaPresentNative Not invasive Beadell et al., 2006
CameroonPresentNative Not invasive Beadell et al., 2006
ChadPresentNative Not invasive Williams et al., 1977
ComorosPresentNative Not invasive Beadell et al., 2006Lineage GRW4, Grand Comore Island
EgyptPresentNative Not invasive MOHAMMED, 1958; Marzal et al., 2011Lineages SGS1 and GRW11
Equatorial GuineaPresentNative Not invasive Beadell et al., 2006
EthiopiaPresentNative Not invasive Ashford et al., 1976
GabonPresentNative Not invasive Beadell et al., 2006
KenyaPresentNative Not invasive Bennett and Herman, 1976; Bensch et al., 2000; Perkins and Schall, 2002Lineage GRW4
MadagascarPresentNative Not invasive Beadell et al., 2006Lineage GRW4
MauritiusPresentNative Not invasive Peirce et al., 1977; Beadell et al., 2006Lineage GRW4
MayottePresentNative Not invasive Beadell et al., 2006Lineage GRW4
NigeriaPresentNative Not invasive Waldenström et al., 2002; Beadell et al., 2006; Hellgren et al., 2007Lineages GRW4, SGS1
RéunionPresentNative Not invasive Peirce et al., 1977; Beadell et al., 2006Lineage GRW4
Rodriguez IslandPresentNative Not invasive Beadell et al., 2006Lineage GRW4
Sao Tome and PrincipePresentNative Not invasive Beadell et al., 2006
SenegalPresentBennett et al., 1978
SeychellesPresentNative Not invasive Beadell et al., 2006Lineage GRW4 on Praslin, other lineages on Fregate
South AfricaPresentNative Not invasive Beadell et al., 2006; Durrant et al., 2007Lineage GRW4
TanzaniaPresentNative Not invasive Bennett and Herman, 1976
UgandaPresentNative Not invasive Bennett et al., 1974b
ZambiaPresentNative Not invasive Peirce, 1984
ZimbabwePresentNative Not invasive Beadell et al., 2006

North America

BermudaPresentIntroducedBeadell et al., 2006; Marzal et al., 2011Lineage GRW4; speculation that it may have played a role in the decline of Bermudan birds
CanadaPresentNative Not invasive Bennett et al., 1974a; Bishop and Bennett, 1992Records from Newfoundland and Saskatchewan; likely widespread throughout Canada
MexicoPresentNative Not invasive Beltran and Pardinas, 1953; Marzal et al., 2011Lineage GRW4
USAWidespreadNative Not invasive Beadell et al., 2006; Kimura et al., 2006; Marzal et al., 2011Multiple records from throughout continental U.S.
-HawaiiWidespreadIntroduced1920s? Invasive Laird and Van Riper, 1981; Beadell et al., 2006Lineage 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 RepublicPresentNative Not invasive Beadell et al., 2006Lineage GRW4
GrenadaPresentNative Not invasive Beadell et al., 2006Lineage GRW4
JamaicaPresentNative Not invasive Bennett et al., 1980
PanamaPresentNative Not invasive Sousa and Herman, 1982

South America

BrazilPresentNative Not invasive Marzal et al., 2011Lineage GRW4
ColombiaPresentNative Not invasive Bennett and Borrero, 1976
GuyanaPresentNative Not invasive Beadell et al., 2006
UruguayPresentNative Not invasive Beadell et al., 2006
VenezuelaPresentNative Not invasive Gabaldon and Ulloa, 1980

Europe

BelarusPresentNative Not invasive Beadell et al., 2006Lineage GRW4
BelgiumPresentNative Not invasive Hellgren et al., 2007Lineages GRW4, SGS1
BulgariaPresentNative Not invasive Shurulinkov and Golemansky, 2003; Hellgren et al., 2007; Zehtindjiev et al., 2008Lineages GRW4, SGS1.
Czech RepublicPresentNative Not invasive Votýpka et al., 2003
Czechoslovakia (former)PresentNative Not invasive Kucera, 1978
FrancePresentNative Not invasive Beadell et al., 2006; Bonneaud et al., 2006; Loiseau et al., 2008; Marzal et al., 2011Lineages SGS1 and GRW4
GermanyPresentNative Not invasive Beadell et al., 2006
GreecePresentNative Not invasive PAPADAKIS, 1935
HungaryPresentNative Not invasive Szöllosi et al., 2009Lineages GRW4, SGS1
ItalyPresentNative Not invasive Corradetti, 1970; Beadell et al., 2006; Hellgren et al., 2007; Marzal et al., 2011Lineages GRW4, SGS1, GRW11
LithuaniaPresentNative Not invasive Hellgren et al., 2007; Palinauskas et al., 2007; Marzal et al., 2011Lineages SGS1, GRW11
NorwayPresentNative Not invasive Beadell et al., 2006; Marzal et al., 2011Lineages GRW4 and SGS1
PolandPresentSulgostowska and Czaplinska, 1987
Russian FederationPresentNative Not invasive Kobyshev et al., 1975; Beadell et al., 2006; Zehtindjiev et al., 2009; Marzal et al., 2011Multiple reports from throughout Russia, including lineages GRW4, SGS1 and GRW11
SpainPresentNative Not invasive Orbaneja Aguero S de, 1934; Beadell et al., 2006; Hellgren et al., 2007; Marzal et al., 2008; Marzal et al., 2011Lineages GRW4, SGS1, GRW11
SwedenPresentNative Not invasive Hellgren, 2005; Beadell et al., 2006; Bensch et al., 2007; Yohannes et al., 2008; Marzal et al., 2011Lineages GRW4, SGS1
UKPresentNative Not invasive Beadell et al., 2006; Wood et al., 2007; Cosgrove et al., 2008Lineages SGS1, GRW11
UkrainePresentNative Not invasive Gluschchenko, 1963; Beadell et al., 2006; Hellgren et al., 2007; Marzal et al., 2011Lineages GRW4, SGS1

Oceania

AustraliaPresentNative Not invasive Beadell et al., 2006Lineage GRW4
Cook IslandsPresentIntroduced1922?Ishtiaq et al., 2007Single report from introduced Common Myna (Acridotheres tristis) based on PCR diagnostics; distribution in indigenous birds unknown
French PolynesiaPresentIntroducedBeadell et al., 2006Lineage GRW4. Single report based on PCR diagnostics from introduced birds on Moorea (Society Islands) and from indigenous birds on Nuku Hiva (Marquesas Islands)
New ZealandWidespreadIntroduced Invasive Beadell et al., 2006; Tompkins and Gleeson, 2006; Marzal et al., 2011Widespread in introduced passerines on North and South Islands, Lineage SGS1
Northern Mariana IslandsPresentBeadell et al., 2006Single report based on PCR diagnostics from the indigenous Rufous Fantail (Rhipidura rufifrons). Not clear if it was introduced with non-native passerines.
Papua New GuineaPresentNative Not invasive Beadell et al., 2006
Solomon IslandsPresentNative Not invasive Laird, 1960

Pathology

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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).

Diagnosis

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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/Signs

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SignLife StagesType
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 Course

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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).

Epidemiology

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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 tarsalisCulex 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).

Impact

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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 Safety

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P. relictum is not a zoonotic threat in domestic poultry and poses no risk of transmission to humans.

Disease Treatment

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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 Control

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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.

Environmental Management

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.

References

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Al-Dabagh MA, 1964. The incidence of blood parasites in wild and domestic birds of Columbus, Ohio. American Midland Naturalist, 72:148-151.

AL-DABAGH MA; GARNHAM PCC, 1966. Mechanisms of death and tissue injury in malaria, with special reference to five species of avian malaria. Baghdad, Iraq: Shafik Press, vi + 240 pp.

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

APPLEGATE JE, 1970. Population changes in latent avian malaria infections associated with season and corticosterone treatment. Journal of Parasitology, 56(3):439-43.

Ashford RW; Palmer TT; Ash JS; Bray RS, 1976. Blood parasites of Ethiopian birds. 1 General survey. Journal of Wildlife Diseases, 12(3):409-426.

Atkinson CT, 2008. Avian malaria. In: Parasitic diseases of wild birds [ed. by Atkinson, C. T.\Thomas, N. J.\Hunter, D. B.]. Ames: Wiley-Blackwell, 35-53.

Atkinson CT; Dusek RJ; Lease JK, 2001. Serological responses and immunity to superinfection with avian malaria in experimentally-infected Hawaii amakihi. Journal of Wildlife Diseases, 37(1):20-27.

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.

Bak UB; Park JC, 1984. An outbreak of malaria in penguins at the Farm-land Zoo. Korean Journal of Parasitology, 22(2):267-272.

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; Fleischer RC, 2005. A restriction enzyme-based assay to distinguish between avian hemosporidians. Journal of Parasitology, 91(3):683-685.

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

Beaudoin RL; Applegate JE; David DE; McLean RG, 1971. A model for the ecology of avian malaria. Journal of Wildlife Diseases, 7:5-13.

Becker ER; Hollander WF; Farmer JN, 1957. Occurrence (1956) of Haemoproteus sacharovi and Plasmodium relictum in a central Iowa pigeon colony. Proceedings of the Iowa Academy of Science, 64:648-649.

Beier JC; Stoskopf MK, 1980. The epidemiology of avian malaria in black-footed penguins (Spheniscus demersus). Journal of Zoo Animal Medicine, 11(4):99-105.

Beier JC; Strandberg J; Stoskopf MK; Craft C, 1981. Mortality in robins (Turdus migratorius) due to avian malaria. Journal of Wildlife Diseases, 17(2):247-250.

Beltran E; Pardinas A, 1953. Blood protozoa of Mexican birds. (Los protozoarios sanguineos de les aves mexicanas.) Memoria Congreso Cientifico Mexicana, 7:117-138.

Bennett GF; Blancou J; White EM; Williams NA, 1978. Blood parasites of some birds from Senegal. Journal of Wildlife Diseases, 14(1):67-73.

Bennett GF; Borrero H JI, 1976. Blood parasites of some birds from Colombia. Journal of Wildlife Diseases, 12(3):454-458.

Bennett GF; Campbell AG; Cameron M, 1974. Haematozoa of passerine birds from insular Newfoundland. Canadian Journal of Zoology, 52:765-772.

Bennett GF; Greiner EC; Whiteley PL; Norman FI, 1977. Blood parasites of some waterfowl from Victoria, Australia. Journal of Wildlife Diseases, 13(2):202-204.

Bennett GF; Herman CM, 1976. Blood parasites of some birds from Kenya, Tanzania and Zaire. Journal of Wildlife Diseases, 12(1):59-65.

Bennett GF; Okia NO; Cameron MF, 1974. Avian hematozoa of some Ugandan birds. Journal of Wildlife Diseases, 10(No.4):458-465.

Bennett GF; Whiteway M; Woodworth-Lynas C, 1982. A host-parasite catalogue of the avian haemoatozoa. unpaginated. [Memorial University of Newfoundland Occasional Papers in Biology No. 5.]

Bennett GF; Witt H; White EM, 1980. Blood parasites of some Jamaican birds. Journal of Wildlife Diseases, 16(1):29-38.

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 Ann; TATE P; THORPE Mary V, 1938. The Duration of Plasmodium relictum Infection in Canaries. Parasitology, 30:388-391.

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

BOX ED, 1966. Blood and Tissue Protozoa of the English Sparrow (Passer domesticus domesticus) in Galveston, Texas. Journal of Protozoology, 13(2):204-8.

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.

Burtikashvili LP, 1978. Blood parasites of wild birds in Georgia. Tbilisi: Metsneireba, 123 pp.

Cassamagnaghi A, 1947. Malaria in the birds of Uruguay. (Malaria en las aves del Uruguay.) Boletin Mensual Direccion de Ganaderia (Montevideo), 29:105-129.

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.

Caum EL, 1933. The exotic birds of Hawaii. Bishop Museum Occasional Papers, 10:1-55.

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.

Clark GW, 1966. Incidence and seasonal variations in blood and tissue parasites of yellow-billed magpies. Journal of Protozoology, 13:108-110.

Coatney GR, 1937. A strain of Plasmodium relictum from doves and pigeons. Journal of Parasitology, 23:556.

Coatney GR, 1938. A strain of Plasmodium relictum from doves and pigeons infective to canaries and the common fowl. American Journal of Hygiene, 27:380-389.

Coatney GR; West E, 1938. Some blood parasites of Nebraska birds. II. American Midland Naturalist, 19:601-602.

Corradetti A, 1970. Plasmodium species of wild birds in Italy. Journal of Parasitology, 56 (Sect. II):412-413.

Cosgrove CL; Wood MJ; Day KP; Sheldon BC, 2008. Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. Journal of Animal Ecology, 77:540-548.

COUCH AB Jr, 1952. Blood parasites of some common Texas birds. Field and Laboratory, 20(4):146-154.

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.

Dore AB, 1920. The occurrence of malaria in the native ground lark. Journal of Science and Technology, 3:118-119.

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

Dyl'ko MI, 1966. Blood parasites of birds in Byelorussia. Vestsi Akademii Navuk BSSR, Seryia Biialahichnykh Navuk, 2:103-110.

Dymowska Z; Zukowski K, 1968. [English title not available]. (Pierwotniaki krwi ptakow odlowionych na terenie Bieszczadow.) Wiadomosci Parazytologiczne, 14:455-459.

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

Ervin S, 1982. Avian malaria at high altitude and the occurrence of Plasmodium (Novyella) vaughani in Zonotrichia. Journal of Parasitology, 68(1):166-167.

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

Fantham HB; Porter A, 1944. On a Plasmodium (Plasmodium relictum var. spheniscidae n. var.) observed in four species of penguins. Proceedings of the Zoological Society of London, 114:279-292.

Farmer JN, 1960. Some blood parasites of birds in central Iowa. Proceedings of the Iowa Academy of Sciences, 67:591-597.

Farmer JN; Moore AK, 1962. Periodicity and synchronicity of Plasmodium relictum in the pigeon. Proceedings of the Iowa Academy of Sciences, 69:634-644.

Feldman RA; Freed LA; Cann RL, 1995. A PCR test for avian malaria in Hawaiian birds. Molecular Ecology, 4(6):663-673.

Fisher HI; Baldwin PH, 1947. Notes on the Red-billed Leiothrix in Hawaii. Pacific Science, 1:45-51.

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.

Forrester DJ; Greiner EC; McFarlane RW, 1977. Blood parasites of some columbiform and passeriform birds from Chile. Journal of Wildlife Diseases, 13(1):94-96.

FRANCHINI G, 1924. The Haematozoa of Birds in Italy. (Observations sur les hématozoaires des oiseaux d'Italie (2e note).) Ann. Inst. Pasteur, 38(6):470-515 pp.

Gabaldon A; Ulloa G, 1980. Holoendemicity of malaria: an avian model. Transactions of the Royal Society of Tropical Medicine and Hygiene, 74(4):501-507.

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.

Galindo P; Sousa O, 1966. Blood parasites of birds from Almirante, Panama, with ecological notes on the hosts. Revista de Biología Tropical, 14:27-46.

GARNHAM PCC, 1950. Blood Parasites of East African Vertebrates, with a Brief Description of Exo-Erythrocytie Schizogony in Plasmodium pitmani. Parasitology, 40(3/4):328-37.

GARNHAM PCC, 1966. Malaria Parasites and other Haemosporidia. 5, Alfred Street, Oxford, UK: Blackwell Scientific Publications Ltd., xviii + 1114 pp.

Gluschchenko VV, 1963. The fauna of parasites of the domestic and wild birds of Pollssje Region, Kiev. Dopovidi Akademii Nauk Ukrainskoi SSR, 11:1-18.

Glushchenko VV, 1962. New data on the blood parasites of domestic and wild birds in the Kiev forest zone. Dopovidi Akademii Nauk Ukrainskoi SSR, 10:1387-1391.

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.

Griner LA; Sheridan BW, 1967. Malaria (Plasmodium relictum) in penguins at the San Diego Zoo. American Journal of Veterinary Clinical Pathology, 1:7-17.

GRUNDMANN AW; NEWSON HD; WARNOCK RG, 1952. Non-Human Malaria in Mosquitoes and the English Sparrow, Passer domesticus Linn., in the Vicinity of Salt Lake City, Utah. Mosquito News, 12(2):53-7.

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.]

HART JW, 1949. Observations on Blood Parasites of Birds in South Carolina. Journal of Parasitology, 35(1):79-82.

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, 2005. The occurrence of haemosporidian parasites in the Fennoscandian bluethroat. Journal of Ornithology, 146:55-60.

Hellgren O; Waldenström J; Bensch S, 2004. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. Journal of Parasitology, 90(4):797-802.

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, 1951. Blood Parasites from California Ducks and Geese. Journal of Parasitology, 37(3):280-82.

Herman CM; Barrow JH, 1967. Three species of Plasmodium from Canada Geese Branta canadensis. Bulletin of the Wildlife Disease Association, 3:88.

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.

HEWITT Redginal, 1940. American Journal of Hygiene, 15. Baltimore: Johns Hopkins Press., xvii + 228 pp.

Huchzermeyer FW, 1993. Pathogenicity and chemotherapy of Plasmodium durae in experimentally infected domestic turkeys. Onderstepoort Journal of Veterinary Research, 60(2):103-110.

Huff CG, 1939. A survey of blood parasites of birds caught for banding purposes. Journal of the American Veterinary Medical Association, 94:615-620.

HUFF CG, 1965. Susceptibility of Mosquitoes to Avian Malaria. Experimental Parasitology, 16(1):107-32.

HUFF CG; SHIROISHI T, 1962. Natural Infection of Humboldt's Penguin with Plasmodium elongatum. Journal of Parasitology, 48(3):495.

HUNNINEN AV, 1951. Comparative Susceptibility of Four Anopheline Mosquitoes to Plasmodium relictum. Journal of the National Malaria Society, 10(3):216-23.

HUNNINEN AV; YOUNG MD, 1950. Blood Protozoa of Birds at Columbia, South Carolina. Journal of Parasitology, 36(3):258-60.

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.

Janovy J Jr, 1965. Epidemiology of malaria in certain birds of the cheyenne bottoms, Barton County, Kansas., USA: University of Oklahoma, 52 pp.

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.

JASWANT SINGH; KEISHNAN KS; DAVID A; 1952, Dec. Natural Infection of P. relictum in Weaver Bird, the Baya (Ploceus philippinus). Indian Journal of Malariology, 6(4):471-3.

Jochen RF, 1966. Research note: Blood parasites of birds trapped in the New Jersey coastal region. Avian Diseases, 10:405-407.

Jordan HB, 1943. Blood protozoa of birds trapped at Athens, Georgia. Journal of Parasitology, 29:260-263.

Joyce CR, 1961. Potentialities for accidental establishment of exotic mosquitoes in Hawaii. Proceedings of the Hawaiian Entomological Society, 17:403-413.

Kairullaev KK, 1979. Blood parasites of wild birds in the floodplain of the middle Ural river in Kazakh SSR. Izvestiya Akademii Nauk Kazakhskoi SSR Seriya Biologicheskikh, 17:19-21.

Kairullaev KK; Yakunin MP, 1982. Blood parasites of migratory birds in the submontane region of the West Tyan-Shan. Izvestiya Akademii Nauk Kazakhskoi SSR Seriya Biologicheskikh Nauk, 4:24-27.

Karaseferyan ET, 1959. Blood parasites of birds in Armenia. Izvestiia Akademii nauk Armianskoi SSR, 2:75-81.

Kilpatrick AM; Gluzberg Y; Burgett J; Daszak P, 2004. Quantitative risk assessment of the pathways by which West Nile Virus could reach Hawaii. EcoHealth, 1:205-209.

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.

Kingston N; Remple JD; Burnham W, 1976. Malaria in a captively-produced F1 gyrfalcon and in two F1 peregrine falcons. Journal of Wildlife Diseases, 12(4):562-565.

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.

Kocan AA; Snelling J; Greiner EC, 1977. Some infectious and parasitic diseases in Oklahoma raptors. Journal of Wildlife Diseases, 13(3):304-306.

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.

Kucera J, 1978. Blood parasites of our birds with special reference to the blood protozoa. Prague, Czechoslovakia: Faculty of Natural Science, Charles University, 180 pp.

Laird M, 1950. Some blood parasites of New Zealand birds. Zoology Publications from the Victoria University College, 15:1-20.

Laird M, 1960. Migratory birds and the dispersal of avian malarial parasites in the South Pacific. Canadian Journal of Zoology, 38:153-155.

Laird M, 1998. Avian malaria in the asian tropical subregion. Singapore, Singapore: Springer-Verlag, 130 pp.

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, 2007. Current and potential impacts of mosquitoes and the pathogens they vector in the Pacific region. Proceedings of the Hawaiian Entomological Society, 39:75-81.

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.

LaPointe DA; Goff ML; Atkinson CT, 2005. Comparative susceptibility of introduced forest-dwelling mosquitoes in Hawai'i to avian malaria, Plasmodium relictum. Journal of Parasitology, 91(4):843-849.

Lari FA, 1959. Observations on avian malaria in Pakistan. Pakistan Journal of Medical Research, 1:53-61.

Laveran A; Lucet E, 1905. Two haematozoans of the partridge and the turkey. (Deux hématozoaires de la perdrix et du dindon.) Comptes rendus de l'Académie des Sciences, 141:673-676.

Lawrence JJ, 1946. Some observations on the Plasmodium and other blood parasites of sparrows. Proceedings of the Linnean Society of N.S.W, 71:1-5.

LAWRENCE JJ; BEARUP AJ, 1961. A New Host Record for Plasmodium relictum: the Silver Gull (Larus novae-hollandiae Stephens). Indian Journal of Malariology, 15(1):11-19.

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

Loiseau C; Zoorob R; Garnier S; Birard J; Federici P; Julliard R; Sorci G, 2008. Antagonistic effects of a MHC class I allele on malaria-infected house sparrows. Ecology Letters, 11:258-265.

LOVE GJ; WILKIN Sara A; GOODWIN MH Jr, 1953. Incidence of Blood Parasites in Birds collected in Southwestern Georgia. Journal of Parasitology, 39(1):52-7.

Lowery RS, 1971. Blood parasites of vertebrates on Aldabra. Philosophical Transactions of the Royal Society, B, 260:577-580.

MACKERRAS MJOSEPHINE; MACKERRAS IM, 1960. The Haematozoa of Australian Birds. Australian J. Zool, 8(2):226-60.

Mandal FB; Nandi NC; Mandal AK, 1989. Incidence of haemoparasites in some Indian birds. Indian Journal of Animal Health, 28(1):33-38.

Manuel MF; Tongson MS; Rosete T; Martin A; Balediata E, 1969. Hematozoa of Philippine weaver birds (Family Ploceidae). Philippine Journal of Animal Sciences, 6:39-49.

Manwell RD, 1955. The blood protozoa of seventeen species of sparrows and other Fringillidae. Journal of Protozoology, 2:21-27.

Manwell RD; Allen CS; Kuntz RE, 1976. Blood parasites of Taiwan birds. Journal of Protozoology, 23(4):571-576.

Manwell RD; Herman CM, 1935. Blood parasites of birds of the Syracuse (N.Y.) region. Journal of Parasitology, 21:415-416.

Manwell RD; Rossi GS, 1975. Blood protozoa of imported birds. Journal of Protozoology, 22(No.1):124-127.

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/

Marullaz M, 1912. Contribution to the study of Haemamoeba relicta. (Contribution à l'étude de Haemamoeba relicta.) Comptes Rendus des Séances de la Société de Biologie et de ses Filiales, 72:526-528.

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.

MATHEY WR Jr, 1955. Two cases of Plasmodium relictum infection in domestic pigeons in the Sacramento area. Veterinary Medicine, 50:318.

McClure HE; Poonswad P; Greiner EC; Laird M, 1978. Haematozoa in the birds of Eastern and Southern Asia. St. John's, Newfoundland: Memorial University of Newfoundland, 296 pp.

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

McLaughlin ET, 1968. Blood parasites of the cowbird, grackle, red-wing and starling in New Jersey. Bird-Banding, 39:193-199.

MICKS DW, 1949. Malaria in the English Sparrow. Journal of Parasitology, 35(5):543-4.

MIELCAREK JE, 1954. The Occurrence of Plasmodium relictum in the Wood Duck (Aix sponsa). Journal of Parasitology, 40(2):232.

MOHAMMED AHH, 1958. Systematic and Experimental Studies on Protozoal Blood Parasites of Egyptian Birds. Vols. I. & II. Cairo, Egypt: Cairo University Press., xi + 298 pp.

MORGAN BB; WALLER EF, 1941. Some parasites of the eastern crow; (Corvus brachyrhynchos brachyrkynchos Brehm). Bird-Banding, 12(1):16-22.

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.]

Nandi NC, 1976. Avian haematozoa from upper stretches of Godavari River basin, Nasik and Ahmednagar districts, Maharashtra. Indian Journal of Animal Health, 15(2):137-138.

Nandi NC, 1978. Blood parasites of Indian avifauna. Calcutta, India: University of Calcutta, unpaginated.

Nandi NC; Mandal AK, 1978. Studies on some avian haematozoa from Orissa, India. Indian Journal of Animal Science, 47:558-561.

Nandi NC; Mandal AK; Choudhury A, 1984. Blood parasites of some birds from West Bengal, India. Bulletin of the Zoological Survey of India, 5(2/3):45-51.

Novy FG; MacNeal WJ, 1905. On the trypanosomes and bird malaria. Proceedings of the Society of Experimental Biology and Medicine, 2:23-28.

OGAKI M, 1949. Bird Malaria Parasites found in Malay Peninsula. American Journal of Tropical Medicine, 29(4):459-62.

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.

Pal NL; Dasgupta B, 1982. Malarial parasites of some Indian birds. Proceedings of the Zoological Society (Calcutta), 33:87-109.

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

PAPADAKIS A, 1935. Avian Malaria Parasites and their Incidence in Greek Birds. Praktika tes Akademias 'Athenon, 10:432-436 pp.

Paperna I; Martelli P, 2008. Haemosporidian infections in captive exotic glossy starling Lamprotornis chalybaeus in Hong Kong. Folia Parasitologica, 55(1):7-12. http://www.paru.cas.cz/folia/

Peirce MA, 1967. Presence of Haemoproteus sp. in house sparrows in England. Nature, 213:315.

Peirce MA, 1976. Haematozoa of East African birds: I. Blood parasites of birds from Marsabit, Nakuru, Ngulia and East Rudolf in Kenya. Journal of Wildlife Diseases, 12(2):148-153.

Peirce MA, 1984. Haematozoa of Zambian birds. I. General survey. Journal of Natural History, 18(1):105-122.

Peirce MA; Backhurst GC; Backhurst DEG, 1977. Haematozoa of East African birds. III. Three years' observations on the blood parasites of birds from Ngulia. East African Wildlife Journal, 15(1):71-79.

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

Perkins SL; Schall JJ, 2002. A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. Journal of Parasitology, 88(5):972-978.

PLIMMER HG, 1912. On the Blood-Parasites found in Animals in the Zoological Gardens during the four Years 1908-1911. Proceedings of the Zoological Society of London, Pt. 2:406-419.

Raethel H, 1960. [English title not available]. (Plasmodieninfektionen bei Pinguinem des Berliner Zoologischen Gartens und ihre Bedeutung fur die Pinguinhaltung.) Kleintier Praxis, 5:64-70.

Ramisz A, 1960. Blood parasites of passerines from Warsaw, and their environment. Wiadomosci parazytologiczne, 6:505-517.

Reed C, 1997. Avian malaria in New Zealand dotterel. Kokako, 4:3.

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.

Remple JD, 2004. Intracelluar hematozoa of raptors: a review and update. Journal of Avian Medicine and Surgery, 18:75-88.

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 C van III; Atkinson CT; Seed TM, 1994. Plasmodia of birds. In: Parasitic protozoa, Vol. 7 [ed. by Kreier, J. P.]. New York, USA: Academic Press, 73-140.

Riper C van III; Riper SG van; Goff ML; Laird M, 1986. The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs, 56:327-344.

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.

RODHAIN J, 1939. P. relictum Infection in Penguins. (L'infection à Plasmodium relictum chez les pingouins.) Ann. Parasit. Humaine et Comparee, 17(2):139-157 pp.

Rodhain J, 1953. Plasmodium relictum infection in penguins. (L'infection à Plasmodium relictum chez les pingouins.) Bulletin de la Societe Royale de Zoologie d'Anvers, 1:1-24.

Rodhain J; Andrianne VF, 1953. [English title not available]. (Deux nouveaux cas d'importation par Plasmodium chez des pingouins.) Annales de parasitologie humaine et comparée, 27:573-577.

Roudabush RL, 1942. Parasites of the American Coot (Fulica Americana) in central Iowa. Iowa State College Journal of Science, 16:437-441.

Rousselot R, 1953. Notes de parasitolgie tropicale. Tom 1. Parasites du sang des animaux (systéme réticuloendothélia). Paris, France: Vigot Frères, 152 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, 1904. The haematozoa of birds in Algeria. Journal of the Royal Army Medical Corps, 3:111.

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.]

Shurulinkov P; Golemansky V, 2003. Plasmodium and Leucocytozoon (Sporozoa: Haemosporida) of wild birds in Bulgaria. Acta Protozoologica, 42(3):205-214.

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.

Sousa OE; Herman CM, 1982. Blood parasites of birds from Chriqui and Panama Provinces in the Republic of Panama. Journal of Wildlife Diseases, 18:205-221.

Stabler RM; Kitzmiller NJ, 1969. Plasmodium spp. in Colorado Passeriformes. Journal of the Colorado-Wyoming Academy of Science, 6:51-52.

Stabler RM; Kitzmiller NJ, 1970. Hematozoa from Colorado birds. III. Passeriformes. Journal of Parasitology, 56:12-16.

Stauber MF; Stauber LA, 1942. Bird malaria in southern New Jersey. In: Proceedings of the 29th Annual Meeting of the New Jersey Mosquito Exterminators Association. 45-46.

Stjernman M; Raberg L; Nilsson JA, 2008. Maximum host survival at intermediate parasite infection intensities. PLos ONE, 3:article number e2463.

Stoskopf MK; Beier J, 1979. Avian malaria in African black-footed penguins. Journal of the American Veterinary Medical Association, 175(9):944-947.

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

Thompson PE, 1943. The relative incidence of animal parasites in the blood of some birds from Georgia. Journal of Parasitology, 29:153-155.

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, 2005. Avian malaria parasites and other haemosporidia. New York, USA: CRC Press, 932 pp.

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

Vanderwerf EA; Groombridge JJ; Fretz JS; Swinnerton KJ, 2006. Decision analysis to guide recovery of the po'ouli, a critically endangered Hawaiian honeycreeper. Biological Conservation, 129:383-392.

Votýpka J; Simek J; Tryjanowski P, 2003. Blood parasites, reproduction and sexual selection in the red-backed shrike (Lanius collurio). Annales Zoologici Fennici, 40(5):431-439.

Waldenström J; Bensch S; Kiboi S; Hasselquist D; Ottosson U, 2002. Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Molecular Ecology, 11:1545-1554.

Warner RE, 1968. The role of introduced diseases in the extinction of the endemic Hawaiian avifauna. The Condor, 70:101-120.

Wasielewski T von, 1896. Sporozoan studies. (Sporozoenkunde.) Jena, Germany: Fischer, 162 pp.

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 NA; Bennett GF; Troncy PM, 1977. Avian hematozoa of some birds from Chad. Journal of Wildlife Diseases, 13:59-61.

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

WOOD SF; HERMAN CM, 1943. The occurrence of blood parasites in birds from southwestern United States. Journal of Parasitology, 29(3):187-196.

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, 1972. Blood parasites of the wild birds of southeast Kazakhastan. Trudy Instituta Zoologii Akademiia Nauk Kazakhskoi SSR, 33:69-79.

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.

Yakunin MP; Zhazyltaev TA, 1977. The blood parasite fauna of wild and domestic birds from Kazakhstan. Trudy Instituta Zoologii Akademiia Nauk Kazakhskoi SSR, 37:124-148.

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.

Links to Websites

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WebsiteURLComment
Global Invasive Species Databasehttp://www.issg.org/databaseThe GISD aims to increase awareness about invasive alien species and to facilitate effective prevention and management. It is managed by the Invasive Species Specialist Group (ISSG) of the Species Survival Commission.
Hawaiian Ecosystems at Risk Project (HEAR)http://www.hear.org/

Organizations

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USA: U.S. Geological Survey, Pacific Island Ecosystems Research Center, PO Box 44, Hawaii National Park, Hawaii 96718, http://biology.usgs.gov/pierc/

Contributors

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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

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