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Table 32 Key to the Haemoproteus species of Passeriformes birds (suborder Passeri) of the families Leiothrichidae, Phylloscopidae, Pycnonotidae, Sylviidae and Zosteropidaea

From: Keys to the avian Haemoproteus parasites (Haemosporida, Haemoproteidae)

Step

Features and species

1 (12)

Advanced dumbbell-shaped gametocytes, which do not touch envelope of infected erythrocytes along their entire margin and have highly constricted (attenuated) central portion and readily thickened roundish ends (Fig. 33j), are absent

2 (13)

The majority of advanced macrogametocytes do not contain one clear roundish discrete vacuole, which is close to 1 µm in diameter (Fig. 33k, l)

3 (16)

Fully grown gametocytes are halteridial (Fig. 33a, f, h, g) or close to circumnuclear (Fig. 33c–e); they reach poles of infected erythrocytes and usually occupy poles of the erythrocytes completely (Fig. 33a, c–h)

4 (17)

Advanced growing macrogametocytes, which are closely appressed to the nuclei of infected erythrocytes but do not touch the envelope of the erythrocytes along their entire margin (Fig. 33n), are absent. Advanced growing gametocytes touch envelope of infected erythrocytes entirely (Fig. 33p) or in one/several points (Fig. 33b)

5 (20)

Advanced growing gametocytes, whose pellicle in the centre does not extend to the envelope of infected erythrocytes causing a ‘dip’ and giving a dumbbell-like appearance (Fig. 33b), are present and usually common

6 (7)

Fully grown gametocytes contain large (1–1.5 µm) elongate pigment granules (Fig. 33a), which are common and might predominate in some cells

 

………………………………………………………………………………………………………………….

H. killangoi (Fig. 33a, b) [3, 93, 163, 164]

7 (6)

Fully grown gametocytes usually do not contain large (1–1.5 µm) elongate pigment granules (Fig. 33a); such pigment granules can occur only occasionally in some cells

8 (9)

Fully grown gametocytes markedly enclose nuclei of infected erythrocytes with their end and tend to assume circumnuclear form (Fig. 33c–e); circumnuclear gametocytes sometimes occur (Fig. 33e), more often among microgametocytes. Fully grown gametocytes are predominantly close to circumnuclear in form (Fig. 33d)

 

………………………………………………………………………………………………………………….

H. parabelopolskyib (Fig. 33c–e) [100, 128, 148, 159]

9 (8)

Fully grown gametocytes slightly enclose nuclei of infected erythrocytes with their ends (Fig. 33f–h), but do not tend to assume circumnuclear form. Fully grown gametocytes are predominantly halteridial (Fig. 33f, g, h)

10 (11)

Growing and fully grown gametocytes markedly displace nuclei of infected erythrocytes laterally (Fig. 33f, g). Fully grown gametocytes often displace erythrocyte nuclei close to the erythrocyte envelope (Fig. 33g). The average NDR is less than 0.7

 

………………………………………………………………………………………………………………….

H. leiothrichus, H. homoleiothrichusc,d (Fig. 33f, g) [7, 165]

11 (10)

Growing and fully grown gametocytes do not markedly displace nuclei of infected erythrocytes laterally (Fig. 33h). Fully grown gametocytes usually do not displace erythrocyte nuclei close to the erythrocyte envelope (Fig. 33g). The average NDR is 0.7 or greater. Early gametocytes often are markedly ameboid in outline (Fig. 33i)

 

………………………………………………………………………………………………………………….

H. timalusd (Fig. 33h, i) [3, 139]

12 (1)

Advanced dumbbell-shaped gametocytes, which do not touch envelope of infected erythrocytes along their entire margin and have highly constricted (attenuated) central portion and readily thickened roundish ends (Fig. 33j), are common

 

………………………………………………………………………………………………………………….

H. philippinensis (Fig. 33j) [3, 166]

13 (2)

The majority of advanced macrogametocytes contain a clear roundish discrete vacuole, which is close to 1 µm in diameter (Fig. 33k, l)

14 (15)

The average number of pigment granules in fully grown gametocytes is greater than 15

 

………………………………………………………………………………………………………………….

H. vacuolatus (Fig. 33k) [63, 100, 167, 168]

15 (14)

The average number of pigment granules in fully grown gametocytes is less than 15

 

………………………………………………………………………………………………………………….

H. palloris (Fig. 33l) [63, 91, 100, 168]

16 (3)

Fully grown gametocytes are microhalteridial, they do not reach poles of infected erythrocytes and do not occupy poles of the erythrocytes (Fig. 33m)

 

………………………………………………………………………………………………………………….

H. homogeneae (Fig. 33m) [100]

17 (4)

Advanced growing macrogametocytes, which are closely appressed to the nuclei of infected erythrocytes but do not touch the envelope of the erythrocytes along their entire margin (Fig. 33n), are common

18 (19)

Nuclei of fully grown macrogametocytes are subterminal in position (Fig. 33)

 

………………………………………………………………………………………………………………….

H. otocompsae (Fig. 33n, o) [3, 166]

19 (18)

Nuclei of fully grown macrogametocytes are median in position (Fig. 33p)

 

………………………………………………………………………………………………………………….

H. sanguinis (Fig. 33p) [3, 166]

20 (5)

Advanced growing gametocytes, whose pellicle in the centre does not extend to the envelope of infected erythrocytes causing a ‘dip’ and giving a dumbbell-like appearance (Fig. 33b), are absent or appear only occasionally. Advanced growing gametocytes are closely appressed both to the nuclei and envelop of infected erythrocytes (Fig. 33v)

21 (24)

Fully grown gametocytes do not contain large (greater than 1 µm) pigment granules (Fig. 33t–v). The macrogametocyte cytoplasm is relatively pale-stained and is similar to microgametocytes based this character (compare Fig. 33q and r)

22 (23)

Fully grown gametocytes contain roundish, small (less than 0.5 µm) pigment granules (Fig. 33q, r). Pigment granules do not change size and shape significantly as parasite matures

 

………………………………………………………………………………………………………………….

H. pallidulus (Fig. 33q, r) [63, 100, 168, 169]

23 (22)

Fully grown gametocytes contain roundish and oval pigment granules (Fig. 33s), which are of medium size (0.5–1.0 μm). Pigment granules readily increase in size as parasite matures

 

………………………………………………………………………………………………………………….

H. homopalloris (Fig. 33s) [63, 168]

24 (21)

Fully grown gametocytes contain large (greater than 1 µm) pigment granules (Fig. 33t–v). Macrogametocytes are readily distinguishable from microgametocytes based on intensity of staining of their cytoplasm (Fig. 33t, u)

 

………………………………………………………………………………………………………………….

H. zosteropis (Fig. 33t–v) [3, 163, 164]

  1. aThis group of Haemoproteus species is difficult to identify due to similar form of growing and mature gametocytes in many species. Visualisation of all gametocyte development stages (young, growing and fully grown) is essential for final conclusion about species identification
  2. bHaemoproteus parabelopolskyi is common in birds of this group, however Haemoproteus belopolskyi might occur in some species of the Sylviidae and Phylloscopidae occasionally. The latter parasite is similar to H. parabelopolskyi. These two parasite species can be distinguished due to differences in size of nuclei of fully grown gametocytes [159]; the average area of the nuclei is greater than 3 µm2 in H. belopolskyi (Fig. 32f), but is less than 3 µm2 in H. parabelopolskyi (Fig. 33e)
  3. cHaemoproteus majoris was seen in some species of the Sylviidae and Phylloscopidae. This parasite is morphologically similar to H. leiothrichus and H. homoleiothrichus. The latter two parasites seem to be of tropical distribution; transmission of H. majoris predominantly occurs in countries with temperate and cold climates
  4. dHaemoproteus leiothrichus and H. homoleiothrichus seem to be cryptic species based on the original description of their gametocytes [165]. Taxonomic status of these species requires confirmation with regard to H. timalus. Gametocytes of H. leiothrichus and H. homoleiothrichus are similar morphologically [165], and they are barely distinguishable from gametocytes of H. timalus because of overlapping most diagnostic characters. Additionally, all three parasites develop in closely related birds of the family Leiothrichidae. Molecular characterization of H. timalus has not been done. Because H. timalus has priority in nomenclature, either H. leiothrichus or H. homoleiothrichus might be synonyms of H. timalus. Molecular characterization of H. timalus is needed to answer this question. More detail examination of these three parasites is needed