Haemoproteus pulcher, Vanstreels & Anjos & Leandro & Andr & Carvalho & Santos & Egert & Hurtado & Queiroz & Carvalho & Erika & Braga & Kirchgatter, 2022

Vanstreels, Ralph Eric Thijl, Anjos, Carolina Clares dos, Leandro, Hassan Jerdy, Andr, Carvalho, ea de Moraes, Santos, Allan Poltronieri, Egert, Leandro, Hurtado, Renata, Queiroz, Eulogio Carlos, Carvalho, de, Erika, Braga, Martins & Kirchgatter, Karin, 2022, A new haemosporidian parasite from the Red-legged Seriema Cariama cristata (Cariamiformes, Cariamidae), International Journal for Parasitology: Parasites and Wildlife 18, pp. 12-19 : 15-17

3.1. Haemoproteus pulcher sp. nov

Type-host: Red-legged Seriema Cariama cristata . Male, adult bird caught on 6 June 2019.

Type-locality: Paulo Cesar ´Vinha State Park , a coastal area of tropical semideciduous forest (“non-flooded forest formation” sensu Assis et al., 2004) within the Atlantic Forest biome, in the Guarapari municipality, Espírito Santo state, Brazil (20 ◦ 36 ′ 02 ′′ S 40 ◦ 25 ′ 34 ′′ W; 3 m above sea level) .

Site of infection: Mature erythrocytes; endothelial cells (lungs, kidneys).

Prevalence: One of one bird.

Type-specimens: Hapantotype (accession number G466233, ex Cariama cristata ; parasitemia intensity approximately 0.1%, 6 June 2019, collected by L. Egert) is deposited at the International Reference Centre for Avian Haematozoa ( IRCAH) of the Queensland Museum (Brisbane, Australia). Parahapantotype deposited at the Coleç˜ao de Protozo´arios, Instituto Oswaldo Cruz (Rio de Janeiro, Brazil; accession code COL- PROT-927) .

Distribution: Only known from type-locality.

Representative DNA sequence: Mitochondrial cytochrome b gene, lineage CARCRI02 (1119 bp, GenBank accession code OL906298).

Etymology: From Latin pulcher = beautiful; the species name should be treated as a Latin adjective. The name is a reference to the statement by Lutz and Meyer (1908) that they had seen “a beautiful species of halterids” (in Portuguese: “uma bonita esp´ecie de halterídeos”) in the blood of Red-legged Seriema.

Description ( Fig. 1 and Table 1)

Young gametocytes ( Fig. 1A–D ). Young gametocytes may develop at any position, with median-to-subpolar positioning being most frequent ( Fig. 1B–D ). Occasionally, growing gametocytes can slightly displace the host cell nucleus laterally ( Fig. 1B ) or slightly rotate it ( Fig. 1D ). Younger gametocytes usually have a smooth membrane and do not touch the host cell nucleus ( Fig. 1A and B ).

Macrogametocytes ( Fig. 1E–P ). Macrogametocytes are relatively pale staining, but still show sufficient staining contrast to be differentiated from microgametocytes. Growing macrogametocytes have a relatively smooth membrane ( Fig. 1E ), but the membrane facing towards the host cell nucleus can become undulated as the parasites grow larger ( Fig. 1F and G ), occasionally developing folds ( Fig. 1H, I, 1M, and 1N ). Growing gametocytes frequently touch the host cell nucleus on the sides but not on the poles ( Fig. 1G, Q, and 1S ), although in some cases they apparently do not touch the host cell nucleus and an evident cleft can be seen between the parasite and the host cell nucleus ( Fig. 1I and N ). Fully grown macrogametocytes are usually appressed to the host cell outer membrane and markedly displace the host cell nucleus laterally ( Fig. 1E–J ), or occasionally towards the pole ( Fig. 1P ). The host cell is slightly elongated when parasitized by a macrogametocyte (on average, the length of parasitized erythrocytes is 0.8 μm greater; Table 1), and the host cell nucleus is often atrophied into a round or ovoid shape (on average, the nuclear length of parasitized erythrocytes is 0.9 μm smaller; Table 1), with a darker staining of its chromatin ( Fig. 1J–M and 11P). A slight rotation (up to 45 ◦) of host cell nucleus occurs occasionally

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( Fig. 1H and O ). Macrogametocytes tend to enclose the host cell nucleus, but the ends of the parasite never encircle the host cell nucleus completely, leaving a small gap where the host cell cytoplasm is visible ( Fig. 1M and O ). The nucleus of macrogametocytes is usually median or subpolar, but never polar, and it is not usually appressed to the host cell nucleus. Small pigment granules (<0.5 μm) are abundant and randomly scattered in the cytoplasm. One or two medium-sized pigment granules (0.5–1.0 μm) are occasionally present ( Fig. 1N ). Large pigment granules (> 1.0 μm) are absent. The number of pigment granules ranges between 17 and 31 ( Table 1). Dumbbell-shaped and discoid macrogametocytes are absent. Macrogametocytes with highly amoeboid outline or fingerlike projections are absent, and the parasites do not enucleate the host cell. Rod-like pigment granules are absent, even though small pigment granules may occasionally appear to be slightly elongated ( Fig. 1J ).

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Large vacuoles are occasionally present ( Fig. 1F ). There are no volutin granules.

Microgametocytes ( Fig. 1Q–X ). Microgametocytes have the same general characteristics as macrogametocytes with the usual sexual dimorphic characters. Microgametocytes tend to be less voluminous (on average, 1.7 μm shorter and 0.4 μm narrower; Table 1) than macrogametocytes. Microgametocytes usually do not touch the host cell nucleus as frequently as macrogametocytes, leaving clefts between the parasite and the host cell nucleus that are more frequent and prominent than those seen in macrogametocytes. Microgametocytes do not encircle the host cell nucleus to the same extent as macrogametocytes. Pigment granules are less abundant than in macrogametocytes ( Table 1), and tend to aggregate near the poles more frequently than in macrogametocytes.

3.2. Remarks

This species is provisionally placed in the genus Haemoproteus because: (a) it parasitizes avian erythrocytes; (b) erythrocytic stages present hemozoin pigment granules; and (c) erythrocytic meronts were not seen. However, analysis of the mitochondrial cytochrome b gene suggests this parasite is a representative of an evolutionary branch that is separate from most known Haemoproteus species. Further studies are therefore necessary to clarify the taxonomy of this parasite.

If Haemoproteus species that infect other avian species within Australaves are considered, H. pulcher is morphologically most similar to Haemoproteus elani from Falconiformes from the Holarctic, Ethiopian and Oriental regions (Valkiunas ¯, 2005). Unlike H. elani , however, H. pulcher shows a greater tendency to enclose and nearly encircle the host cell nucleus, its inner membrane is more undulated and occasionally forms folds, and it lacks volutin granules or small vacuoles. When avian species other than Australaves are considered, arguably the Haemoproteus species with the greatest morphological similarity to H. pulcher is H. rotator , which thus far has only been recorded on the Pin-tailed snipe ( Gallinago stenura ; Charadriiformes : Scolopacidae ) from the Phillipine Islands (Valki¯unas, 2005). However, the gametocytes of H. pulcher do not occupy the cytoplasm of the host cell completely, they cause nuclear atrophy more frequently than H. rotator , and they do not cause the rotation of the host cell nucleus as frequently as H. rotator .

Figures

Fig. 1. Gametocytes of Haemoproteus pulcher sp. nov. from the blood of the Red-legged Seriema (Cariama cristata): A–D, young gametocytes; E–P, macrogametocytes, Q–X, microgametocytes. Legend: ahcn, atrophied host cell nucleus; cl, cleft between the parasite and the host cell nucleus; cv, cytoplasmic vacuoles; epg, elongated pigment granules; g, gap between the ends of the parasite; pn, parasite nucleus; mpg, medium-sized pigment granules; spg, small pigment granules. Eosin–methylene blue stained thin blood films. Scale-bar: 5 μm. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)