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Table 3 Key to the Haemamoeba species

From: Keys to the avian malaria parasites

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Features and species

1 (16)

Roundish or oval pigment granules predominate in gametocytes (Fig. 4u–x). Elongate rod-like in form pigment granules (Fig. 5n) are absent, but single slightly elongate pigment granules might occur occasionally

2 (22)

A residual body (Fig. 5s) is absent in mature erythrocytic meronts. Of oval-elongate form gametocytes, which are over 10 µm in length (Fig. 5i), are present

3 (17)

Large (≥ 1 µm in diameter) vacuoles (Figs. 2g, h, 5u) are absent from growing erythrocytic meronts. Markedly vacuolated erythrocytic meronts (Fig. 2f–h) are absent

4 (9)

Maximum number of merozoites in mature (Figs. 2e, j, 3n–r, y, 5r, s) erythrocytic meronts is ≤ 12

5 (8)

Maturing and mature erythrocytic meronts enlarge infected erythrocytes < ½ in area in comparison to uninfected erythrocytes (compare infected and uninfected erythrocytes in Fig. 2g, h, see also Fig. 5s); numerous mature meronts adhere to erythrocyte nuclei (Fig. 2j)

6 (7)

Merozoites locate haphazardly in mature meronts (Fig. 1c). Residuum cytoplasm (Fig. 5s) is invisible in mature meronts, and merozoites never appear to have connections to the residuum cytoplasm

…………………………………………… P. subpraecox [1, 8, 82]

7 (6)

Nuclei locate on periphery of maturing and mature meronts (Fig. 5r). Residuum cytoplasm is visible and locates centrally in maturing meronts (Fig. 5r). Maturing merozoites have connections to the residuum cytoplasm, and these connections look like small wisps of cytoplasm extending towards merozoites (Fig. 5r)

…………………………………………… P. parvulum [51]

8 (5)

Maturing and mature meronts enlarge infected erythrocytes over ½ in area in comparison to uninfected erythrocytes (Fig. 5p). The majority of maturing meronts are rounded in shape, they locate away from erythrocyte nuclei, which are markedly displaced toward erythrocyte envelope from earliest stages of meronts development (Fig. 5p)

…………………………………………… P. calotia [57]

9 (4)

Maximum number of merozoites in mature erythrocytic meronts is > 12. Mature meronts and gametocytes are large (size is significantly greater than erythrocyte nuclei); they occupy > 1/2 of the cytoplasm in infected erythrocytes (Figs. 2j; 4u–x)

10 (23)

Pigment granules in gametocytes do not tend to be clumped in a spot, which is usually located near a margin of the parasite (Fig. 4t, w). If present occasionally, such position of pigment granules does not predominate in mature gametocytes

11 (10)

Pigment granules in mature gametocytes show markedly different patterns of position in the cytoplasm; they often are randomly scattered (Figs. 1b, 5v), but also might be variously grouped (Fig. 5t) and even aggregated in solid masses (Fig. 4u, v, x)

12 (15)

Largest fully grown gametocytes can occupy all available cytoplasmic space in infected erythrocytes (Fig. 5x, y). Length of the largest gametocytes exceed 10 µm

13 (14)

Development in the blood is asynchronous, with all blood stages present in circulation simultaneously. Periodicity of erythrocytic merogony is 36 h; Specific parasite of domestic chicken. Passeriform birds are resistant. In the nature, transmission does not occur outside the Oriental zoogeographical region

…………………………………………… P. gallinaceum [1, 8, 83]

14 (15)

Development in the blood is synchronous, with not all blood stages present in circulation simultaneously. Periodicity of erythrocytic merogony is 24 h. Domestic chicken was reported to be resistant. In the nature, transmission occurs outside the Oriental zoogeographical region

…………………………………………… P. coturnixi [8, 84]

15 (12)

Largest fully-grown gametocytes do not occupy all available cytoplasmic space in infected erythrocytes; a small non-occupied space is usually visible in infected erythrocytes (Fig. 4u–x). Length of the largest gametocytes does not exceed 10 µm. Domestic chicken is resistant. Development in the blood is asynchronous, with all blood stages (trophozoites, growing and mature meronts as well gametocytes) present in blood films simultaneously. Periodicity of erythrocytic merogony is 36 h

…………………………………………… P. relictum [8, 26, 85]

16 (1)

Pigment granules in gametocytes are roundish, oval and elongate rod-like (Fig. 5n). Rod-like pigment granules are common and might predominate in microgametocytes (Fig. 5n), but they are less common and often do not predominate in macrogametocytes

…………………………………………… P. cathemerium [1, 8, 86]

17 (3)

Large (≥ 1 µm in diameter) vacuoles (Figs. 2h; 5u) are common in erythrocytic meronts

18 (21)

One or several large vacuoles, which do not exceed 2 µm in diameter, are often present in growing erythrocytic meronts. Markedly vacuolated erythrocytic meronts are common (Fig. 2f–h). Pigment granules do not gather around these vacuoles. Trophozoites lack large (> 1 µm in diameter) vacuoles. Lobulated in form gametocytes (Fig. 4x) are absent or develop only occasionally

19 (20)

Vacuoles are absent or occur occasionally in erythrocytic trophozoites. Pigment granules in fully grown gametocytes distinctly vary in size, and small (< 0.5 µm) and medium (0.5–1.0 µm) size granules occur simultaneously (Fig. 5v). The medium-size pigment granules are common (Fig. 5v). Phanerozoites do not develop in brain of domestic canaries

…………………………………………… P. giovannolai [1, 8, 87]

20 (19)

Vacuoles often present in erythrocytic trophozoites. Pigment granules in fully grown gametocytes are more or less similar in size, usually they are small (< 0.5 µm) (Fig. 5t). Medium-size (0.5–1.0 µm) pigment granules (Fig. 5v) might occur, but are not characteristic. Phanerozoites develop in brain of domestic canaries

…………………………………………… P. matutinum [1, 8, 66, 88]

21 (19)

Each advanced trophozoites possess one large (> 1 µm in diameter) roundish centrally located vacuole. One large (> 2 µm in diameter) vacuole is present in growing erythrocytic meronts (Fig. 5u). Pigment granules gather around this vacuole. Lobulated in form gametocytes (Fig. 4x) are common

…………………………………………… P. tejerai [8, 50, 89]

22 (2)

A residual body (Fig. 5s) is present in mature erythrocytic meronts. Of oval-elongate form gametocytes, which are over 10 µm in length (Fig. 5i), are present. Growing erythrocytic meronts often possess vacuoles (Fig. 2g, h)

…………………………………………… P. griffithsi [1, 8]

23 (10)

Pigment granules in gametocytes clearly tend to be clumped in a spot, which is located near a margin of the parasite (Fig. 4t, w). Such position of pigment granules predominates in mature gametocytes. Pigment granules can be aggregated into a solid mass of pigment, which also usually locates near a margin of the parasite

…………………………………………… P. lutzi [8, 90, 91]

  1. aPlasmodium caloti was described from the Eurasian skylarks Alauda arvensis co-infected with several other Plasmodium species, and this races a question if all blood stages (particularly gametocytes), which were reported in the original description [57], truly belong to this parasite. However, because of (1) the marked influence on host cell (marked enlargement of infected erythrocytes and displacement of their nuclei) and (2) the relatively regular rounded form and smooth margins of mature meronts (Fig. 5p), which produce small number of merozoites < 10), this parasite is morphologically unique and can be distinguished from other Haemamoeba species. The original description is fragmentary [57], and re-description of this parasite is needed