Plasmodium

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A plasmodium is also the macroscopic form of the protist known as a slime mould.
Plasmodium
Plasmodium sporozoite
Scientific classification
Kingdom: Chromalveolata
Superphylum: Alveolata
Phylum: Apicomplexa
Class: Aconoidasida
Order: Haemosporida
Family: Plasmodiidae
Genus: Plasmodium
Species

See text

Plasmodium is a large genus of parasitic protozoa. Infection with these protozoans is known as malaria. The parasite always has two hosts in its life cycle: a mosquito vector and a vertebrate host. The genus contains about 200 species in divided into several subgenera. At least ten species infect humans; other species infect other animals, including birds, reptiles and rodents.

Taxonomy and host range[edit]

The genus Plasmodium was created in 1885 by Marchiafava and Celli and there are over 200 species recognized. New species continue to be described.[1]

As of 2006, the genus is in need of reorganization as it has been shown that parasites belonging to the genera Haemocystis and Hepatocystis appear to be closely related to Plasmodium. It is likely that other species such as Haemoproteus meleagridis will be included in this genus once it is revised.

Host range among the mammalian orders is non uniform. At least 29 species infect non-human primates; rodents outside the tropical parts of Africa are rarely affected; a few species are known to infect bats, porcupines and squirrels; carnivores, insectivores and marsupials are not known to act as hosts.

In 1898 Ronald Ross demonstrated the existence of Plasmodium in the wall of the midgut and salivary glands of a Culex mosquito. For this discovery he won the Nobel Prize in 1902. However credit must also be given to the Italian professor Giovanni Battista Grassi, who showed that human malaria could only be transmitted by Anopheles mosquitoes. For some species the vector may not be a mosquito.

Mosquitoes of the genera Culex, Anopheles, Culiseta, Mansonia and Aedes may act as vectors. The known vectors for human malaria (more than 100 species) belong to the genus Anopheles. Bird malaria is commonly carried by species belonging to the genus Culex. Only female mosquitoes bite. Aside from blood both sexes live on nectar, but one or more blood meals are needed by the female for egg laying as the protein content of nectar is very low. The life cycle of Plasmodium was discovered by Ross who worked with species from the genus Culex.

The life cycle of Plasmodium is very complex. Sporozoites from the saliva of a biting female mosquito are transmitted to either the blood or the lymphatic system[2] of the recipient. The sporozoites then migrate to the liver and invade hepatocytes. This latent or dormant stage of the Plasmodium sporozoite in the liver is called the hypnozoite.

The development from the hepatic stages to the erythrocytic stages has been obscure. In 2006[3] it was shown that the parasite buds off the hepatocytes in merosomes containing hundreds or thousands of merozoites. These merosomes have been subsequently shown[4] to lodge in the pulmonary capilaries and to slowly disintergrate there over 48–72 hours releasing merozoites. Erythrocyte invasion is enhanced when blood flow is slow and the cells are tightly packed: both of these conditions are found in the alveolar capilaries.

and then to a larger trophozoite form. In the schizont stage, the parasite divides several times to produce new merozoites, which leave the red blood cells and travel within the bloodstream to invade new red blood cells. Most merozoites continue this replicative cycle, but some merozoites differentiate into male or female sexual forms (gametocytes) (also in the blood), which are taken up by the female mosquito.

In the mosquito's midgut, the gametocytes develop into gametes and fertilize each other, forming motile zygotes called ookinetes. The ookinetes penetrate and escape the midgut, then embed themselves onto the exterior of the gut membrane. Here they divide many times to produce large numbers of tiny elongated sporozoites. These sporozoites migrate to the salivary glands of the mosquito where they are injected into the blood of the next host the mosquito bites. The sporozoites move to the liver where they repeat the cycle.

Reactivation of the hypnozoites has been reported for up to 30 years after the initial infection in humans. The factors precipating this reactivation are not known. In the species Plasmodium malariae, Plasmodium ovale and Plasmodium vivax hypnozoites have been shown to occur. Reactivation does not occur in infections with Plasmodium falciparum. It is not known if hypnozoite reactivaction may occur with any of the remaining species that infect humans but this is presumed to be the case.

Species list[edit]

Plasmodium accipiteris

Plasmodium achiotense
Plasmodium achromaticum
Plasmodium acuminatum
Plasmodium adunyinkai
Plasmodium aegyptensis
Plasmodium aeuminatum
Plasmodium agamae
Plasmodium alloelongatum
Plasmodium anasum
Plasmodium anomaluri
Plasmodium arachniformis
Plasmodium ashfordi
Plasmodium atheruri
Plasmodium aurulentum
Plasmodium australis
Plasmodium attenuatum
Plasmodium azurophilum
Plasmodium balli
Plasmodium bambusicolai
Plasmodium basilisci
Plasmodium beebei
Plasmodium beltrani
Plasmodium berghei
Plasmodium bertii
Plasmodium bigueti
Plasmodium biziurae
Plasmodium booliati
Plasmodium bouillize
Plasmodium bowiei
Plasmodium brodeni
Plasmodium brasilianum
Plasmodium brasiliense
Plasmodium brumpti
Plasmodium brucei
Plasmodium brygooi
Plasmodium bubalis
Plasmodium bucki
Plasmodium buteonis
Plasmodium capistrani
Plasmodium cathemerium
Plasmodium cephalophi
Plasmodium cercopitheci
Plasmodium chabaudi
Plasmodium chalcidi
Plasmodium chiricahuae
Plasmodium circularis
Plasmodium circumflexum
Plasmodium clelandi
Plasmodium cordyli
Plasmodium cnemaspi
Plasmodium cnemidophori
Plasmodium coatneyi
Plasmodium coggeshalli
Plasmodium colombiense
Plasmodium columbae
Plasmodium corradettii
Plasmodium coturnixi
Plasmodium coulangesi
Plasmodium cuculus
Plasmodium cyclopsi
Plasmodium cynomolgi
Plasmodium diminutivum
Plasmodium diploglossi
Plasmodium dissanaikei
Plasmodium divergens
Plasmodium dominicana
Plasmodium draconis
Plasmodium durae
Plasmodium egerniae
Plasmodium elongatum
Plasmodium eylesi
Plasmodium fabesia
Plasmodium fairchildi
Plasmodium falciparum
Plasmodium falconi
Plasmodium fallax
Plasmodium fieldi
Plasmodium fischeri
Plasmodium foleyi
Plasmodium formosanum
Plasmodium forresteri
Plasmodium floridense
Plasmodium fragile
Plasmodium galbadoni
Plasmodium garnhami
Plasmodium gallinaceum
Plasmodium giganteum
Plasmodium giovannolai
Plasmodium girardi
Plasmodium gonderi
Plasmodium georgesi
Plasmodium gologoense
Plasmodium gracilis
Plasmodium griffithsi
Plasmodium guangdong
Plasmodium gundersi
Plasmodium guyannense
Plasmodium heischi
Plasmodium hegneri
Plasmodium hermani
Plasmodium heteronucleare
Plasmodium hexamerium
Plasmodium holaspi
Plasmodium huffi
Plasmodium hylobati
Plasmodium icipeensis
Plasmodium iguanae
Plasmodium inconstans
Plasmodium inopinatum
Plasmodium inui
Plasmodium japonicum
Plasmodium jefferi
Plasmodium jiangi
Plasmodium josephinae
Plasmodium joyeuxi
Plasmodium juxtanucleare
Plasmodium kempi
Plasmodium knowlesi
Plasmodium kentropyxi
Plasmodium lacertiliae
Plasmodium lainsoni
Plasmodium landauae
Plasmodium leanucteus
Plasmodium lemuris
Plasmodium lepidoptiformis
Plasmodium lionatum
Plasmodium lophurae
Plasmodium loveridgei
Plasmodium lutzi
Plasmodium lygosomae
Plasmodium mabuiae
Plasmodium mackerrasae
Plasmodium maculilabre
Plasmodium maior
Plasmodium majus
Plasmodium malariae
Plasmodium marginatum
Plasmodium matutinum
Plasmodium melanipherum
Plasmodium mexicanum
Plasmodium michikoa
Plasmodium minasense
Plasmodium morulum
Plasmodium murinus
Plasmodium necatrix
Plasmodium nucleophilium
Plasmodium octamerium
Plasmodium odocoilei
Plasmodium osmaniae
Plasmodium ovale
Plasmodium paddae
Plasmodium papernai
Plasmodium paranucleophilum
Plasmodium parvulum
Plasmodium pedioecetii
Plasmodium pelaezi
Plasmodium percygarnhami
Plasmodium pessoai
Plasmodium petersi
Plasmodium pifanoi
Plasmodium pinotti
Plasmodium pinorrii
Plasmodium pitheci
Plasmodium pitmani
Plasmodium polare
Plasmodium pulmophilum
Plasmodium reichenowi
Plasmodium relictum
Plasmodium rhadinurum
Plasmodium rhodaini
Plasmodium robinsoni
Plasmodium rouxi
Plasmodium sandoshami
Plasmodium sasai
Plasmodium saurocaudatum
Plasmodium schweitzi
Plasmodium scorzai
Plasmodium semiovale
Plasmodium semnopitheci
Plasmodium shortii
Plasmodium silvaticum
Plasmodium simium
Plasmodium tanzaniae
Plasmodium tenue
Plasmodium tejerai
Plasmodium telfordi
Plasmodium tomodoni
Plasmodium torrealbai
Plasmodium traguli
Plasmodium tribolonoti
Plasmodium tropiduri
Plasmodium tumbayaensis
Plasmodium tyrio
Plasmodium uilenbergi
Plasmodium uluguruense
Plasmodium uncinatum
Plasmodium uzungwiense
Plasmodium watteni
Plasmodium wenyoni
Plasmodium vacuolatum
Plasmodium vastator
Plasmodium vaughani
Plasmodium vautieri
Plasmodium vinckei
Plasmodium vivax
Plasmodium volans
Plasmodium voltaicum
Plasmodium yoelii
Plasmodium youngi

Plasmodium zonuriae

Evolution[edit]

This life cycle is best understood in terms of its evolution.

The Apicomplexa — the phylum to which Plasmodium belongs — are thought to have originated within the Dinoflagellates — a large group of photosynthetic protozoa. It is thought that the ancestors of the Apicomplexa were originally prey organisms that evolved the ability to invade the intestinal cells and subsequently lost their photosynthetic ability. Some extant dinoflagelates, however, can invade the bodies of jellyfish and continue to photosynthesize, which is possible because jellyfish bodies are almost transparent. In other organisms with opaque bodies this ability would most likely rapidly be lost.

It is thought that Plasmodium evolved from a parasite spread by the orofaecal route which infected the intestinal wall. At some point this parasite evolved the ability to infect the liver. This pattern is seen in the genus Cryptosporidium to which Plasmodium is distantly related. At some later point this ancestor developed the ability to infect blood cells and to survive and infect mosquitoes. Once mosquito transmission was firmly established the previous orofecal route of transmission was lost.

Current (2007) theory suggests that the genera Plasmodium, Hepatocystis and Haemoproteus evolved from Leukocytozoon species. Parasites of the genus Leukocytozoan infect white blood cells (leukocytes), liver and spleen cells and are transmitted by 'black flies' (Simulium species) — a large genus of flies related to the mosquitoes.

Leukocytes, hepatocytes and most spleen cells actively phagocytose particulate matter making entry into the cell easier for the parasite. The mechanism of entry of Plasmodium species into erythrocytes is still very unclear taking as it does less than 30 seconds. It is not yet known if this mechanism evolved before mosquitoes became the main vectors for transmission of Plasmodium.

Plasmodium evolved about 130 million years ago. This period is coincidental with the rapid spread of the angiosperms (flowering plants). This expansion in the angiosperms is thought to be due to at least one genomic duplication event. It seems probable that the increase in the number of flowers led to an increase in the number of mosquitoes and their contact with vertebrates.

Mosquitoes evolved in what is now South America about 230 million years ago. There are over 3500 species recognised but to date their evolution has not been well worked out so a number of gaps in our knowledge of the evolution of Plasmodium remain.

It seems probable that birds were the first group infected by Plasmodium followed by the reptiles — probably the lizards. At some point primates and rodents became infected. The remaining species infected outside these groups seem likely to be due to relatively recent events.

Template:Aosof, DNA sequences are available from fewer than sixty species and most of these are from species infecting either rodent or primate hosts. The evolution proposed here should be regarded as speculative and subject to revision as data becomes available.

Reproduction[edit]

The pattern of alternation of sexual and asexual reproduction which may seem confusing at first is a very common pattern in parasitic species. The evolutionary advantages of this type of life cycle were recognised by Mendel.

Under favourable conditions asexual reproduction is superior to sexual as the parent is well adapted to its environment and its descendents share these genes. Transferring to a new host or in times of stress, sexual reproduction is generally superior as this produces a shuffling of genes which on average at a population level will produce individuals better adapted to the new environment.

Molecular biology[edit]

All the species examined to date have 14 chromosomes, one mitochondrion and one plastid. The chromosomes vary from 500 kilobases to 3.5 megabases in length. It is presumed that this is the pattern throughout the genus.

The plastid unlike those found in algae is not photosynthetic. Its function is not known but there is some suggestive evidence that it may be involved in reproduction.

On a molecular level, the parasite damages red blood cells using plasmepsin enzymes — aspartic acid proteases which degrade hemoglobin.

Diagnostic characteristics of the genus Plasmodium[edit]

  • Forms gamonts in erythrocytes
  • Merogony occurs in erythrocytes and in other tissues
  • Hemozoin is present
  • Vectors are either mosquitos or sandflies
  • Vertebrate hosts include mammals, birds and reptiles

Taxonomy[edit]

Plasmodium belongs to the family Plasmodiidae (Levine, 1988), order Haemosporidia and phylum Apicomplexa. There are 450 recognised species in this order. Many species of this order are undergoing reexamination of their taxonomy with DNA analysis. It seems likely that many of these species will be re-assigned after these studies have been completed.[5][6] For this reason the entire order is outlined here.

Notes:

The genera Plasmodium, Fallisia and Saurocytozoon all cause malaria in lizards. All are carried by Dipteria (roughly speaking the flies). Pigment is absent in the Garnia. Non pigmented gametocytes are typically the only forms found in Saurocytozoon: pigmented forms may be found in the leukocytes occasionally. Fallisia produce non pigmented asexual and gametocyte forms in leukocytes and thrombocytes.

Subgenera[edit]

The full taxonomic name of a species includes the subgenus but this is often omitted. The full name indicates some features of the morphology and type of host species.

The only two species in the sub genus Laverania are P. falciparum and P. reichenowi.

Species infecting monkeys and apes (the higher primates) with the exceptions of P. falciparum and P. reichenowi are classified in the subgenus Plasmodium.

Parasites infecting other mammals including lower primates (lemurs and others) are classified in the subgenus Vinckeia.

The distinction between P. falciparum and P. reichenowi and the other species infecting higher primates was based on the morphological findings but have since been confirmed by DNA analysis. Vinckeia while previously considered to be something of a taxonomic 'rag bag' has been recently shown — perhaps rather surprisingly — to form a coherent grouping.

The remaining groupings here are based on the morphology of the parasites. Revisions to this system are likely to occur in the future as more species are subject to analysis of their DNA.

The four subgenera Giovannolaia, Haemamoeba, Huffia and Novyella were created by Corradetti et al.[7] for the known avian malarial species. A fifth — Bennettinia — was created in 1997 by Valkiunas.[8] The relationships between the subgenera are a matter of current investigation. Martinsen et al 's recent (2006) paper outlines what was known at the time.[9]

As of 2007, P. juxtanucleare is the only known member of the subgenus Bennettinia.

Unlike the mammalian and bird malarias those affecting reptiles have been more difficult to classify. In 1966 Garnham classified those with large schizonts as Sauramoeba, those with small schizonts as Carinamoeba and the single then known species infecting snakes (Plasmodium wenyoni) as Ophidiella.[10] He was aware of the arbitrariness of this system and that it might not prove to be biologically valid. Telford in 1988 used this scheme as the basis for the accepted (2007) system.[11]

Classification criteria

Avian species:

Species in the subgenus Bennettinia have the following characteristics:

  • Schizonts contain scant cytoplasm, are often round, do not exceed the size of the host nucleus and stick to it.
  • Gametocytes while varying in shape tend to be round or oval, do not exceed the size of the nucleus and stick to it.

Species in the subgenus Giovannolaia have the following characteristics:

  • Schizonts contain plentiful cytoplasm, are larger than the host cell nucleus and frequently displace it. They are found only in mature erythrocytes.
  • Gametocytes are elongated.
  • Exoerythrocytic schizogony occurs in the mononuclear phagocyte system.

Species in the subgenus Haemamoeba have the following characteristics:

  • Mature schizonts are larger than the host cell nucleus and commonly displace it.
  • Gametocytes are large, round, oval or irregular in shape and are substantially larger than the host nucleus.

Species in the subgenus Huffia have the following characteristics:

  • Mature schizonts, while varying in shape and size, contain plentiful cytoplasm and are commonly found in immature erthryocytes.
  • Gametocytes are elongated.

Species in the subgenus Novyella have the following characteristics:

  • Mature schisonts are either smaller than or only slightly larger than the host nucleus. They contain scanty cytoplasm.
  • Gametocytes are elongated. Sexual stages in this subgenus resemble those of Haemoproteus.
  • Exoerythrocytic schizogony occurs in the mononuclear phagocyte system

Reptile species:

Species in the subgenus Carinamoeba have the following characteristics:

  • Infect lizards
  • Schizonts normally give rise to less than 8 merozoites

Species in the subgenus Sauramoeba have the following characteristics:

  • Infect lizards
  • Schizonts normally give rise to more than 8 merozoites

Notes

  • The erythrocytes of both reptiles and birds retain their nucleus, unlike those of mammals. The reason for the loss of the nucleus in mammalian erythocytes remains unknown.
  • The presence of elongated gametocytes in several of the avian subgenera and in Laverania in addition to a number of clinical features suggested that these might be closely related. This is no longer thought to be the case.
  • The subgenera Haemamoeba, Huffia, and Bennettinia As of 2007 appear to be monphylitic. Novyella appears to be well defined with occasional exceptions. The subgenus Giovannolaia needs revision.[9]

Species listed by subgenera[edit]

Plasmodium (Asiamoeba) draconis
Plasmodium (Asiamoeba) vastator

Plasmodium (Bennettinia) juxtanucleare

Plasmodium (Carinamoeba) basilisci

Plasmodium (Carinamoeba) clelandi
Plasmodium (Carinamoeba) lygosomae
Plasmodium (Carinamoeba) mabuiae
Plasmodium (Carinamoeba) minasense
Plasmodium (Carinamoeba) rhadinurum

Plasmodium (Carinamoeba) volans
Plasmodium (Giovannolaia) anasum

Plasmodium (Giovannolaia) circumflexum
Plasmodium (Giovannolaia) dissanaikei
Plasmodium (Giovannolaia) durae
Plasmodium (Giovannolaia) fallax
Plasmodium (Giovannolaia) formosanum
Plasmodium (Giovannolaia) gabaldoni
Plasmodium (Giovannolaia) garnhami
Plasmodium (Giovannolaia) gundersi
Plasmodium (Giovannolaia) hegneri
Plasmodium (Giovannolaia) lophurae
Plasmodium (Giovannolaia) pedioecetii
Plasmodium (Giovannolaia) pinnotti

Plasmodium (Giovannolaia) polare
Plasmodium (Haemamoeba) cathemerium

Plasmodium (Haemamoeba) coggeshalli
Plasmodium (Haemamoeba) coturnixi
Plasmodium (Haemamoeba) elongatum
Plasmodium (Haemamoeba) gallinaceum
Plasmodium (Haemamoeba) giovannolai
Plasmodium (Haemamoeba) lutzi
Plasmodium (Haemamoeba) matutinum
Plasmodium (Haemamoeba) paddae
Plasmodium (Haemamoeba) parvulum
Plasmodium (Haemamoeba) relictum

Plasmodium (Haemamoeba) tejera
Plasmodium (Huffia) elongatum
Plasmodium (Huffia) hermani
Plasmodium (Lacertaemoba) floridense
Plasmodium (Lacertaemoba) tropiduri
Plasmodium (Laverania) falciparum
Plasmodium (Laverania) reichenowi
Plasmodium (Novyella) ashfordi

Plasmodium (Novyella) bertii
Plasmodium (Novyella) bambusicolai
Plasmodium (Novyella) columbae
Plasmodium (Novyella) corradettii
Plasmodium (Novyella) dissanaikei
Plasmodium (Novyella) hexamerium
Plasmodium (Novyella) jiangi
Plasmodium (Novyella) kempi
Plasmodium (Novyella) nucleophilum
Plasmodium (Novyella) papernai
Plasmodium (Novyella) paranucleophilum
Plasmodium (Novyella) rouxi

Plasmodium (Novyella) vaughani
Plasmodium (Paraplasmodium) chiricahuae

Plasmodium (Paraplasmodium) mexicanum

Plasmodium (Paraplasmodium) pifanoi
Plasmodium (Plasmodium) bouillize

Plasmodium (Plasmodium) brasilianum
Plasmodium (Plasmodium) cercopitheci
Plasmodium (Plasmodium) coatneyi
Plasmodium (Plasmodium) cynomolgi
Plasmodium (Plasmodium) eylesi
Plasmodium (Plasmodium) fieldi
Plasmodium (Plasmodium) fragile
Plasmodium (Plasmodium) georgesi
Plasmodium (Plasmodium) girardi
Plasmodium (Plasmodium) gonderi
Plasmodium (Plasmodium) inui
Plasmodium (Plasmodium) jefferyi
Plasmodium (Plasmodium) joyeuxi
Plasmodium (Plasmodium) knowlei
Plasmodium (Plasmodium) hyobati
Plasmodium (Plasmodium) malariae
Plasmodium (Plasmodium) ovale
Plasmodium (Plasmodium) petersi
Plasmodium (Plasmodium) pitheci
Plasmodium (Plasmodium) rhodiani
Plasmodium (Plasmodium) schweitzi
Plasmodium (Plasmodium) semiovale
Plasmodium (Plasmodium) semnopitheci
Plasmodium (Plasmodium) silvaticum
Plasmodium (Plasmodium) simium
Plasmodium (Plasmodium) vivax

Plasmodium (Plasmodium) youngi
Plasmodium (Sauramoeba) achiotense

Plasmodium (Sauramoeba) adunyinkai
Plasmodium (Sauramoeba) aeuminatum
Plasmodium (Sauramoeba) agamae
Plasmodium (Sauramoeba) beltrani
Plasmodium (Sauramoeba) brumpti
Plasmodium (Sauramoeba) cnemidophori
Plasmodium (Sauramoeba) diploglossi
Plasmodium (Sauramoeba) giganteum
Plasmodium (Sauramoeba) heischi
Plasmodium (Sauramoeba) josephinae
Plasmodium (Sauramoeba) pelaezi

Plasmodium (Sauramoeba) zonuriae
Plasmodium (Vinckeia) achromaticum

Plasmodium (Vinckeia) aegyptensis
Plasmodium (Vinckeia) anomaluri
Plasmodium (Vinckeia) atheruri
Plasmodium (Vinckeia) berghei
Plasmodium (Vinckeia) booliati
Plasmodium (Vinckeia) brodeni
Plasmodium (Vinckeia) bubalis
Plasmodium (Vinckeia) bucki
Plasmodium (Vinckeia) caprae
Plasmodium (Vinckeia) cephalophi
Plasmodium (Vinckeia) chabaudi
Plasmodium (Vinckeia) coulangesi
Plasmodium (Vinckeia) cyclopsi
Plasmodium (Vinckeia) foleyi
Plasmodium (Vinckeia) girardi
Plasmodium (Vinckeia) inopinatum
Plasmodium (Vinckeia) lemuris
Plasmodium (Vinckeia) melanipherum
Plasmodium (Vinckeia) odocoilei
Plasmodium (Vinckeia) percygarnhami
Plasmodium (Vinckeia) sandoshami
Plasmodium (Vinckeia) traguli
Plasmodium (Vinckeia) tyrio
Plasmodium (Vinckeia) uilenbergi
Plasmodium (Vinckeia) vinckei
Plasmodium (Vinckeia) watteni

Plasmodium (Vinckeia) yoelli

Notes

Ophidiella was a subgenus created by Garnham in 1966 for the species infecting snakes. As of 2007 it was no longer in use.

Species infecting humans[edit]

Red blood cell infected with malaria

The species of Plasmodium that infect humans include:

The first four listed here are the most common species that infect humans. With the use of the polymerase chain reaction additional species have been and are still being identified that infect humans.

One possible experimental infection has been reported with Plasmodium eylesi. Fever and low grade parasitemia were apparent at 15 days. The volunteer (Dr Bennett) had previously been infected by Plasmodium cynomolgi and the infection was not transferable to a gibbon (P. eylesi 's natural host) so this cannot be regarded as definitive evidence of its ability to infect humans. A second case has been reported that may have been a case of P. eylesi but the author was not certain of the infecting species.[12]

A possible infection with Plasmodium tenue has been reported.[13] This report described a case of malaria in a three-year-old black girl from Georgia, US, who had never been outside the US. She suffered from both P. falciparum and P. vivax malaria and while forms similar to those described for P. tenue were found in her blood even the author was skeptical about the validity of the diagnosis.

Confusingly, Plasmodium tenue was proposed in the same year (1914) for a species found in birds. The human species is now considered to be likely to have been a misdiagnosis and the bird species is described on the Plasmodium tenue page.

Notes:

The only known host of P. falciparum are humans; neither is any other host known for P. malariae.

P. vivax will infect chimpanzees. Infection tends to be low grade but may be persistent and remain as source of parasites for humans for some time.

P. vivax is also known to infect orangutans.[14]

Like P. vivax, P. ovale has been shown to be transmittable to chimpanzees. P. ovale has an unusual distribution pattern being found in Africa, the Philippines and New Guinea. In spite of its admittedly poor transmission to chimpanzees given its discontigous spread, it is suspected that P. ovale may in fact be a zooenosis with an as yet unidentified host. If this is actually the case, the host seems likely to be a primate.

The remaining species capable of infecting humans all have other primate hosts.

Plasmodium shortii and Plasmodium osmaniae are now considered to be junior synonyms of Plasmodium inui

Species no longer recognised as valid

Taxonomy in parasitology until the advent of DNA based methods has always been a problem, and revisions in this area are continuing. A number of synonyms have been given for the species infecting humans that are no longer recognised as valid.[15] Since perusal of the older literature may be confusing, some of these are listed here.

P. camerense

P. causiasium
P. golgi
P. immaculatum
P. laverani var. tertium
P. laverani var. quartum
P. malariae var. immaculatum
P. malariae var. incolor
P. malariae var. irregularis
P. malariae var. parva
P. malariae var. quartanae
P. malariae var. quotidianae
P. perniciosum
P. pleurodyniae
P. praecox
P. quartana
P. quotidianum
P. sedecimanae
P. tenue
P. undecimanae
P. vegesio-tertaniae

P. vivax-minuta

Infections in primates[edit]

Listing

The species that infect primates other than humans include: P. bouillize, P. brasilianum, P. bucki, P. cercopitheci,P. coatneyi, P. coulangesi, P. cynomolgi, P. eylesi, P. fieldi, P. foleyi, P. fragile, P. girardi, P. georgesi, P. gonderi, P. hylobati, P. inui, P. jefferyi, P. joyeuxi, P. knowlesi, P. lemuris, P. percygarnhami, P. petersi, P. reichenowi, P. rodhaini, P. sandoshami, P. semnopitheci, P. silvaticum, P. simiovale, P. simium, P. uilenbergi, P. vivax and P. youngei.

Host records — Most if not all Plasmodium species infect more than one host: the host records shown here should be regarded as being incomplete.

  • P. reichenowi — chimpanzee (Pan) species and gorilla (Gorilla) species
  • P. rodhaini — chimpanzee (Pan) species and gorilla (Gorilla) species
  • P. schwetzi — chimpanzee (Pan) species and gorilla (Gorilla) species

Primate mosquito vectors[edit]

Primate subspecies[edit]

  • P. cynomolgiP. cynomolgi bastianelli and P. cynomolgi ceylonensis.
  • P. inuiP. inui inui and P. inui shortii
  • P. knowlesiP. knowlesi edesoni and P. knowlesi knowlesi.
  • P. vivaxP. vivax hibernans, P. vivax chesson and P. vivax multinucleatum.

Interrelatedness — The evolution of these species is still being worked out and the relationships given here should be regarded as tentative. This grouping, while originally made on morphological grounds, now has considerable support at the DNA level.

  • P. brasilianum, P. inui and P. rodhaini are similar to P. malariae
  • P. cynomolgi, P. fragile, P. knowlesi, P. simium and P. schwetzi are similar to P. vivax
  • P. fieldi and P. simiovale are similar to P. ovale
  • P. falciparum is closely related to P. reichenowi.

Notes

  • P. kochi has been described as a parasite of monkeys. This species is classified as Hepatocystis kochi. This may be subject to revision.
  • P. brasilianum and P. rodhaini seem likely to be the same species as P. malariae.
  • P. lemuris may actually belong to the Haemoproteus genus. Clarification of this point awaits DNA examination.
  • P. shortii is As of 2007 regarded as a junior synonym of P. inui.

Infections in non-primate mammals[edit]

The subgenus Vinckeia was created by Garnham to accommodate the mammalian parasites other than those infecting primates. Species infecting lemurs have also been included in this subgenus.

P. aegyptensis, P. bergei, P. chabaudi, P. inopinatum, P. yoelli and P. vinckei infect rodents. P. bergei, P. chabaudi, P. yoelli and P. vinckei have been used to study malarial infections in the laboratory. Other members of this subgenus infect other mammalian hosts.

Host records

Vectors

Subspecies

  • P. bergheiP. berghei yoelii
  • P. chabaudiP. chabaudi adami and P. chabaudi chabaudi
  • P. melanipherumP. melanipherum monosoma
  • P. vinkeiP. vinckei brucechwatti, P. vinckei petteri and P. vinckei vinckei.
  • P. yoelliiP. yoelli nigeriensis and P. yoelli yoelli.

Notes

  • Calomys callosus seems unlikely to be a natural host for P. atheruri as P. atheruri is found in Africa and Calomys callosus in South America.

Less well documented species

The species listed here from taken from Courtney et al.[15] should be regarded as dubious.

P. achromaticum — the bat (Achromaticatus vesperuginis)

P. brodini — the jumping rat (Petrodromus tetradactylus)

P. melanipherum — Schreiber's bat (Miniopterus schreibersi)

P. melanipherum monosoma — the bat (Vesperugo abramus)

P. murinum — the bat (Vespertilio murinus)

Reclassification

The literature is replete with species initially classified as Plasmodium that have been subsequently reclassified. With DNA taxonomy some of these may be once again be classified as Plasmodium. Some of these species are listed here for completness.

P. epomophori of the bat (Hypsignathus monstruosus) has been reclassified as Hepatocystis epomophori.

Infections in birds[edit]

Species in five of these subgenera infect birdsBennettinia, Giovannolaia, Haemamoeba, Huffia and Novyella.[26] Giovannolaia appears to be a polyphytic group and may be sudivided in the future.[9]

Parasite listing

Species infecting birds include: P. accipiteris, P. alloelongatum, P. anasum, P. ashfordi, P. bambusicolai, P. bigueti, P. biziurae, P. buteonis, P. cathemerium, P. circumflexum, P. coggeshalli, P. corradettii, P. coturnix, P. dissanaikei, P. durae, P. elongatum, P. fallax, P forresteri, P. gallinacium, P. garnhami, P. giovannolai, P. griffithsi, P. gundersi, P. guangdong, P. hegneri, P. hermani, P. hexamerium, P. huffi, P. jiangi, P. juxtanucleare, P. kempi, P. lophurae, P.lutzi, P. matutinum, P. nucleophilum, P. papernai, P. paranucleophilum, P. parvulum, P. pediocetti, P. paddae, P. pinotti, P. polare, P. relictum, P. rouxi, P. tenue, P. tejerai, P. tumbayaensis and P. vaughani.

Avian host records[edit]

  • P. paranucleophilum — South American tanager
  • P. parvulumvanga species

Vectors of avian malaria[edit]


Subspecies of avian malaria[edit]

  • P. relictum has been divided into subspecies: P. relictum capistranoae, P. relicturn matutinum and P. relictum relictum.
  • P. nucleophilum has at least one subspecies — P. nucleophilum toucani

Interelatedness

  • P. durae is related to P. asanum, P. circumflexum, P. fallax, P. formosanum, P. gabaldoni, P. hegneri, P. lophrae, P. lophrae, P. pediocetti, P. pinotti, and P. polare.
  • P. gallinacium is related to P. griffithsi
  • P. relictum is related to P. cathemerium, P. giovannolai and P. matutinum. P. relictum may be difficult to distinguish from P. giovannolai on either morphological grounds or on the basis of host species.
  • P. hexamerium is related to P. vaughni.
  • P. ashfordi is related to P. vaughni.

Avian malaria notes[edit]

  • P. relictum is known to infect over 70 bird families and 359 wild bird species so the record here should be regarded as incomplete. Additional host species can be found under the link Plasmodium relictum. It is likely that this species has been responsible for more bird extinctions than any other protist.
  • P. vaughani is the second commonest species of avian malaria parasites after P. relictum.
  • P. inconstans, P. irae, P. praecox, P. subpraecox and P. wasielewski have been re classified as P. relictum. P. subpraecox was described by Grassi and Feletti in 1892. P. wasielewski was described by Brumpt in 1909.
  • P. elongatum infects 21 bird families and 59 species of bird. Additional host species are given under the link P. elongatum.
  • P. dominicana is species known only from fossil amber.[36] It is thought to have been a species infecting birds.
  • The taxonomic status of P. corradettii (Laird, 1998) is regarded as dubious and may be revised.
  • P. huffi may be the same species as P. nucleophilum toucani.
  • P. oti is now regarded as the same species as P. hexamerium.
  • There are 13 species recognised in the subgenus Novyella all of which are listed here.

A number of additional species have been described in birds — P. centropi, P. chloropsidis, P. gallinuae, P. herodialis, P. heroni, P. mornony, P. pericorcoti and P. ploceii — but the suggested speciation was based at least in part on the idea — 'one host — one species'. It has not been possible to reconcile the descriptions with any of the recognised species and these are not regarded as valid species. As further investigations are made into this genus these species may be resurrected.

A species P. japonicum has been reported[37] but this appears to be the only report of this species and it should therefore be regarded of dubious validity.

Infections in reptiles[edit]

Species in the subgenera Asiamoeba, Carinamoeba, Lacertaemoba, Paraplasmodium and Sauramoeba infect reptiles.[38]

Over 90 species and subspecies of Plasmodium infect lizards and they have been reported from over 3200 species of lizard and 29 species of snake. Only three species — P. pessoai, P. tomodoni and P. wenyoni — infect snakes.

Listing

Species infecting reptiles include: P. achiotense, P. aeuminatum, P. agamae, P. arachniformis, P. attenuatum,P. aurulentum, P. australis, P. azurophilum, P. balli, P. basilisci, P. beebei, P. beltrani , P. brumpti, P. brygooi, P. chiricahuae, P. circularis, P. cnemaspi, P. cnemidophori, P. colombiense, P. cordyli, P. diminutivum, P. diploglossi, P. egerniae, P. fairchildi, P. floridense, P. gabaldoni, P. giganteum, P. gologoense, P. gracilis, P. guyannense, P. heischi, P. holaspi, P. icipeensis, P. iguanae, P. josephinae, P. kentropyxi, P. lacertiliae, P. lainsoni, P. lepidoptiformis, P. lionatum, P. loveridgei, P. lygosomae, P. mabuiae, P. mackerrasae, P. maculilabre, P. marginatum, P. mexicanum, P. michikoa, P. minasense, P. pelaezi, P. pessoai, P. pifanoi, P. pitmani, P. rhadinurum, P. sasai,P. saurocaudatum, P. scorzai, P. siamense, P. robinsoni, P. sasai, P. scorzai, P. tanzaniae, P. tomodoni, P. torrealbai, P. tribolonoti, P. tropiduri, P. uluguruense, P. uzungwiense, P. vacuolatum, P. vastator, P. volans, P. wenyoni and P. zonuriae.

Host records


Vectors

Culex:

Aedes:

Subspecies

  • P. fairchildiP. fairchildi fairchildi and P. fairchildi hispaniolae
  • P. lygosomaeP. lygosomae nucleoversans and P. lygosomae nucleoversans
  • P. minasenseP. minasense anolisi, P. minasense capitoi, P. minasense carinii,

P. minasense diminutivum, P. minasense minasense, P. minasense plicae, and P. minasense tegui.[42] An additional subspecies P. minasense calcaratae has also been described.[43]

-

  • P. traguliP. traguli traguli and P. traguli memmina.
  • P. tropiduriP. tropiduri aquaticum, P. tropiduri panamense and P. tropiduri tropiduri.[42]

Interrelatedness

  • P. floridense is closely related to P. tropiduri and P. minasense

Species reclassified into other genera[edit]

As of 2007 the following species are regarded as belonging to the genus Hepatocystis rather than Plasmodium.

  • Plasmodium epomophori
  • Plasmodium kochi
  • Plasmodium limnotragi Van Denberghe 1937
  • Plasmodium pteropi Breinl 1911
  • Plasmodium ratufae Donavan 1920
  • Plasmodium vassali Laveran 1905
  • Plasmodium gonatodi has been reclassified as a species of Garnia and has been renamed Garnia gonatodi.

General references[edit]

The standard reference books for the identification of Plasmodium species are:

  • Laird, M. (1998). Avian Malaria in the Asian Tropical Subregion. Singapore: Springer. ISBN 9813083190. 
  • Garnham, P.C.C. (1966). Malaria Parasites And Other Haemosporidia. Oxford: Blackwell. ISBN 0397601328.  This book remains the standard reference work on malarial species classification.
  • Hewitt, R.I. (1940). Bird Malaria. American Journal of Hygiene 15. Baltimore: Johns Hopkins Press. 

Other useful references include


Some history of malaria — Slater LB (2005). "Malarial birds: modeling infectious human disease in animals". Bull Hist Med 79 (2): 261–94. doi:10.1353/bhm.2005.0092. PMID 15965289. 

References[edit]

  1. ^ Chavatte JM, Chiron F, Chabaud A, Landau I (March 2007). "[Probable speciations by "host-vector 'fidelity'": 14 species of Plasmodium from magpies]". Parasite (in French) 14 (1): 21–37. PMID 17432055. 
  2. ^ "Malaria Parasites Develop in Lymph Nodes". HHMI News. Howard Hughes Medical Institute. 22 January 2006. 
  3. ^ Sturm A, Amino R, van de Sand C, et al. (September 2006). "Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids". Science 313 (5791): 1287–90. doi:10.1126/science.1129720. PMID 16888102. 
  4. ^ Baer K, Klotz C, Kappe SH, Schnieder T, Frevert U (November 2007). "Release of hepatic Plasmodium yoelii merozoites into the pulmonary microvasculature". PLoS Pathog. 3 (11): e171. doi:10.1371/journal.ppat.0030171. PMC 2065874. PMID 17997605. 
  5. ^ Perkins SL, Schall JJ (October 2002). [0972:AMPOMP2.0.CO;2 "A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences"]. J. Parasitol. 88 (5): 972–8. doi:10.1645/0022-3395(2002)088[0972:AMPOMP]2.0.CO;2. PMID 12435139. 
  6. ^ Yotoko, K.S.C.; Elisei C. (November 2006). "Malaria parasites (Apicomplexa, Haematozoea) and their relationships with their hosts: is there an evolutionary cost for the specialization?". J. Zoo. Syst. Evol. Res. 44 (4): 265–273. doi:10.1111/j.1439-0469.2006.00377.x. 
  7. ^ Corradetti A., Garnham P.C.C., Laird M. (1963). "New classification of the avian malaria parasites". Parassitologia 5: 1–4. 
  8. ^ Valkiunas G (1997). "Bird Haemosporidia". Acta Zoologica Lituanica 3–5: 1–607. ISSN 1392-1657. 
  9. ^ a b c Martinsen ES, Waite JL, Schall JJ (April 2007). "Morphologically defined subgenera of Plasmodium from avian hosts: test of monophyly by phylogenetic analysis of two mitochondrial genes". Parasitology 134 (Pt 4): 483–90. doi:10.1017/S0031182006001922. PMID 17147839. 
  10. ^ Garnham 1966
  11. ^ Telford S (1988). "A contribution to the systematics of the reptilian malaria parasites, family Plasmodiidae (Apicomplexa: Haemosporina)". Bulletin of the Florida State Museum Biological Sciences 34 (2): 65–96. 
  12. ^ Tsukamoto M (1977). "An imported human malarial case characterized by severe multiple infections of the red blood cells". Ann. Trop. Med. Parasit. 19 (2): 95–104. 
  13. ^ Russel P.F. (1928). "Plasmodium tenue (Stephens): A review of the literature and a case report". Am. J. Trop. Med. s1–8 (5): 449–479. 
  14. ^ Reid MJ, Ursic R, Cooper D, et al. (December 2006). "Transmission of human and macaque Plasmodium spp. to ex-captive orangutans in Kalimantan, Indonesia". Emerging Infect. Dis. 12 (12): 1902–8. doi:10.3201/eid1212.060191. PMC 3291341. PMID 17326942. 
  15. ^ a b Coatney G.R., Roudabush R.L. (1936). "A catalog and host-index of the genus Plasmodium". J. Parasitol. 22 (4): 338–353. 
  16. ^ Collins WE, Sullivan JS, Nace D, Williams T, Williams A, Barnwell JW (February 2008). "Observations on the sporozoite transmission of Plasmodium vivax to monkeys". J. Parasitol. 94 (1): 287–8. doi:10.1645/GE-1283.1. PMID 18372652. 
  17. ^ Collins WE, Richardson BB, Morris CL, Sullivan JS, Galland GG (July 1998). "Salvador II strain of Plasmodium vivax in Aotus monkeys and mosquitoes for transmission-blocking vaccine trials". Am. J. Trop. Med. Hyg. 59 (1): 29–34. PMID 9684622. 
  18. ^ Collins WE, Sullivan JS, Nace D, et al. (April 2002). [0295:EIOAFW2.0.CO;2 "Experimental infection of Anopheles farauti with different species of Plasmodium"]. J. Parasitol. 88 (2): 295–8. doi:10.1645/0022-3395(2002)088[0295:EIOAFW]2.0.CO;2. PMID 12054000. 
  19. ^ Collins WE, Morris CL, Richardson BB, Sullivan JS, Galland GG (August 1994). "Further studies on the sporozoite transmission of the Salvador I strain of Plasmodium vivax". J. Parasitol. 80 (4): 512–7. PMID 8064516. 
  20. ^ Tan CH, Vythilingam I, Matusop A, Chan ST, Singh B (2008). "Bionomics of Anopheles latens in Kapit, Sarawak, Malaysian Borneo in relation to the transmission of zoonotic simian malaria parasite Plasmodium knowlesi". Malar. J. 7: 52. doi:10.1186/1475-2875-7-52. PMC 2292735. PMID 18377652. 
  21. ^ Abd-el-Aziz GA, Landau I, Miltgen F (1975). "[Description of Plasmodium aegyptensis n. sp., presumed parasite of the Muridae Arvicanthis noloticus in Upper Egypt]". Ann Parasitol Hum Comp (in French) 50 (4): 419–24. PMID 1211772. 
  22. ^ Sandosham AA, Yap LF, Omar I (September 1965). "A malaria parasite, plasmodium (Vinckeia) booliati sp.nov., from a Malayan giant flying squirrel". Med J Malaya 20 (1): 3–7. PMID 4221411. 
  23. ^ Keymer IF (June 1966). "Studies on Plasmodium (Vinckeia) cephalophi of the grey duiker (Sylvicapra grimmia)". Ann Trop Med Parasitol 60 (2): 129–38. PMID 5962467. 
  24. ^ Landau I, Chabaud AG (1978). "[Description of P. cyclopsi n. sp. a parasite of the microchiropteran bat Hipposideros cyclops in Gabon (author's transl)]". Ann Parasitol Hum Comp (in French) 53 (3): 247–53. PMID 697287. 
  25. ^ Lien JC, Cross JH (December 1968). "Plasmodium (Vinckeia) watteni sp. n. from the Formosan giant flying squirrel, Petaurista petaurista grandis". J. Parasitol. 54 (6): 1171–4. PMID 5757690. 
  26. ^ Wiersch SC, Maier WA, Kampen H (May 2005). "Plasmodium (Haemamoeba) cathemerium gene sequences for phylogenetic analysis of malaria parasites". Parasitol. Res. 96 (2): 90–4. doi:10.1007/s00436-005-1324-8. PMID 15812672. 
  27. ^ Valkiūnas G, Zehtindjiev P, Hellgren O, Ilieva M, Iezhova TA, Bensch S (May 2007). "Linkage between mitochondrial cytochrome b lineages and morphospecies of two avian malaria parasites, with a description of Plasmodium (Novyella) ashfordi sp. nov". Parasitol. Res. 100 (6): 1311–22. doi:10.1007/s00436-006-0409-3. PMID 17235548. 
  28. ^ Landau I, Chabaud AG, Bertani S, Snounou G (December 2003). "Taxonomic status and re-description of Plasmodium relictum (Grassi et Feletti, 1891), Plasmodium maior Raffaele, 1931, and description of P. bigueti n. sp. in sparrows". Parassitologia 45 (3-4): 119–23. PMID 15267099. 
  29. ^ Kirkpatrick CE, Lauer DM (January 1985). "Hematozoa of raptors from southern New Jersey and adjacent areas". J. Wildl. Dis. 21 (1): 1–6. PMID 3981737. 
  30. ^ Earlé RA, Horak IG, Huchzermeyer FW, Bennett GF, Braack LE, Penzhorn BL (September 1991). "The prevalence of blood parasites in helmeted guineafowls, Numida meleagris, in the Kruger National Park". Onderstepoort J. Vet. Res. 58 (3): 145–7. PMID 1923376. 
  31. ^ Valkiūnas G, Zehtindjiev P, Dimitrov D, Krizanauskiene A, Iezhova TA, Bensch S (May 2008). "Polymerase chain reaction-based identification of Plasmodium (Huffia) elongatum, with remarks on species identity of haemosporidian lineages deposited in GenBank". Parasitol. Res. 102 (6): 1185–93. doi:10.1007/s00436-008-0892-9. PMID 18270739. 
  32. ^ Murata K, Nii R, Sasaki E, et al. (February 2008). "Plasmodium (Bennettinia) juxtanucleare infection in a captive white eared-pheasant (Crossoptilon crossoptilon) at a Japanese zoo". J. Vet. Med. Sci. 70 (2): 203–5. PMID 18319584. 
  33. ^ Christensen BM, Barnes HJ, Rowley WA (July 1983). "Vertebrate host specificity and experimental vectors of Plasmodium (Novyella) kempi sp. n. from the eastern wild turkey in Iowa". J. Wildl. Dis. 19 (3): 204–13. PMID 6644918. 
  34. ^ Manwell RD (November 1968). "Plasmodium octamerium n. sp., an avian malaria parasite from the pintail whydah bird Vidua macroura". J. Protozool. 15 (4): 680–5. PMID 5719065. 
  35. ^ Valkiũnas G, Iezhova TA (August 2001). [0930:ACOTBP2.0.CO;2 "A comparison of the blood parasites in three subspecies of the yellow wagtail Motacilla flava"]. J. Parasitol. 87 (4): 930–4. doi:10.1645/0022-3395(2001)087[0930:ACOTBP]2.0.CO;2. PMID 11534666. 
  36. ^ Poinar G (May 2005). "Plasmodium dominicana n. sp. (Plasmodiidae: Haemospororida) from Tertiary Dominican amber". Syst. Parasitol. 61 (1): 47–52. doi:10.1007/s11230-004-6354-6. PMID 15928991. 
  37. ^ Manwell RD (February 1966). "Plasmodium japonicum, P. juxtanucleare and P. nucleophilum in the Far East". J. Protozool. 13 (1): 8–11. PMID 5912391. 
  38. ^ Schall JJ (December 2000). "Transmission success of the malaria parasite Plasmodium mexicanum into its vector: role of gametocyte density and sex ratio". Parasitology 121 (Pt 6): 575–80. PMID 11155927. 
  39. ^ Southgate BA (1970). "Plasmodium (Sauramoeba) giganteum in Agama cyanogaster: a new host record". Trans. R. Soc. Trop. Med. Hyg. 64 (1): 12–3. PMID 5462484. 
  40. ^ Garnham PC, Telford SR (November 1984). "A new malaria parasite Plasmodium (Sauramoeba) heischi in skinks (Mabuya striata) from Nairobi, with a brief discussion of the distribution of malaria parasites in the family Scincidae". J. Protozool. 31 (4): 518–21. PMID 6512723. 
  41. ^ Telford SR (October 1986). "Fallisia parasites (Haemosporidia: Plasmodiidae) from the flying lizard, Draco maculatus (Agamidae) in Thailand". J. Parasitol. 72 (5): 766–9. PMID 3100759. 
  42. ^ a b Telford SR (1979). "A taxonomic revision of small neotropical saurian Malarias allied to Plasmodium minasense". Ann Parasitol Hum Comp 54 (4): 409–22. PMID 533109. 
  43. ^ Telford SR, Telford SR (April 2003). [0362:RAROPP2.0.CO;2 "Rediscovery and redescription of Plasmodium pifanoi and description of two additional Plasmodium parasites of Venezuelan lizards"]. J. Parasitol. 89 (2): 362–8. doi:10.1645/0022-3395(2003)089[0362:RAROPP]2.0.CO;2. PMID 12760655. 

External links[edit]