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Haemosporina: Garniidae

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Haemosporina: Garniidae 513 Progarnia archosauriae nov. gen., nov. sp. (Haemosporina: Garniidae), a blood parasite of Caiman crocodilus crocodilus (Archosauria: Crocodilia), and comments on the evolution of reptilian and avian haemosporines R. LAINSON Departamentode Parasitologia, Instituto Evandro Chagas,Caixa Postal 691, 66017-970 Belém, Pará, Brasil (Received27 July 1994,. revised5 October 1994,. accepted8 November 1994) SUMMARY Progarnia archosauriaenovo gen., novosp. (Haemosporina: Garniidae) is described in the blood of the South American caiman, Caiman crocodilus crocodilus (Archosauria: Crocodilia). The parasite undergoes merogony and gametogony principally in leucocytes and thrombocytes, but algo invades erythrocytes in which it produces no 'malarial' pigmento It thus sharesfeatures of Fallisia and Garnia which are, respectively, intra-leucocytic and intra-erythrocytic haemosporines of the family Garniidae in present-day lizards. This, and the antiquity of the order Crocodilia, suggeststhat it was from such a parasite that the existing reptilian and avian haemosporinesevolved. An overall evolutionary pattern is suggested. Key words: Haemosporina, Garniidae, Progarnia archosauriaenov. gen., nov. sp., Caiman c. crocodilus,crocodile, Brazil. described further examples in Old World lizards. INTRODUCTION Telford (1988) finally accepted Fallisia as a valid Lainson, Landau & Shaw (1971) erected the family genus, and suggested that Garnia be regarded as a Garniidae, within the suborder Haemosporina (Api-complexa:subgenus of Plasmodium. He maintained his opinion, Eucoccidiida) to house certain 'malaria however, that both parasites should be included in parasites' of lizards which undergo merogony and the family Plasmodiidae -a view with which the dimorphic gametogony in erythrocytes, without the present author, and some others, do not agree production of malarial pigmento By these characters, (Lainson, 1992). the species of the new gentiS Garnia were Until now members of the Garniidae have been differentiated from those of the existing three described only in lizards among the reptiles (Table families of the Haemosporina: from the 1). The following description of an undoubted Plasmodiidae and the Haemoproteidae by the ab- garniid in the South American caiman, Caiman sence of pigment, and from the Leucocytozoidae and crocodilus crocodilus has necessitated the allocation of the Haemoproteidae by the asexual cycle in the blood. a further generic name within the family, and The new family and gentis wer.e: not accepted by stimulates new speculations as to the origin and some workers, notably Telford (1973) who, while evolution of both reptilian and avian haemosporines. acknowledging that the absence of pigment did not accord with the current definitions of the family Plasmodiidae and the gentis Plasmodium, suggested MATERIALS ANO METHOOS that these definitions be modified in arder to allow the inclusion of the new parasites. Young caimans were captured in their riverine Lainson, Landau & Shaw (1974) added a second habitat on the Island of Marajó when they measured gentis, Fallisia, to the family Garniidae when they approximately 20 cm flOro snout to tail tipo Their described other blood parasites of Brazilian lizards age remains doubtful, but is likely to have been only which differed from Garnia in that their merogony a few months. They were maintained .in an insect- and gametogony were restricted to the leucocytes screened animal house, in large aquaria which offered and thrombocytes. lnitially, like Garnia, such the option of wet or dry conditions, and fed largely parasites were thought to be limited to neotropical on new-born laboratory-bred mice. lizards, but Gabaldon, Ulloa & Zerpa (1985) dis- Weekly blood samples were obtained by lightly covered anotherFallisia species in Venezuelan birds, clipping a claw, and thin blood films were rapidly and Telford (1986) and Paperna & Landau (1990) air-dried and fixed either in absolute methyl alcohol Parasitology (1995),110,513-519 Copyright @ 1995 Cambridge University Press R. Lainson 514 Table 1. Recorded speciesof genera within the family Garniidae (Haemosporina)* Genus Garnia Genus Fallisia G. telfordi Lainson, Landau & Shaw 1971 in Ameiva F. effusa Lainson, Landau & Shaw 1974 in Neusticurus ameiva (Teiidae) bicarinatus (Teiidae) G. utingensisLainson, Landau & Shaw 1971 in Anolis TYPE SPECIES punctatus (lguanidae) F. modestaLainson, Landau & Shaw 1974 in Tropidurus G. multiformis Lainson, Shaw & Landau 1975 in Plica torquatus (lguanidae) umbra (lguanidae) F. audaciosaLainson, Shaw & Landau 1975 in Plica G. uranoscodoniLainson, Shaw & Landau 1975 in umbra (lguanidae) Uranoscodonsuperciliosa (lguanidae) F. simplex Lainson, Shaw & Landau 1975 in Plica umbra G. gonatodi (Telford, 1970) Lainson, Landau & Shaw F. copemaniPaperna & Landau 1990 in Carlia rhomboida- (1971) in Gonotodeshumeralis (Sphaerodactylidae) tis (Scincidae) TYPE SPECIES F. siamense(Telford, 1986)Paperna & Landau 1990 in G. morula (Telford, 1970) Lainson, Làndau & Shaw Draco maculatus (Agamidae) (1971) in Mabuya mabouya (Scincidae) F. (Plasmodoides)neotropicalis Gabaldon, Ulloa & Zerpa G. azurophilum (Telford, 1975) Garnharn & Duggan 1985 in various Venezuelan birds (1986) in Anolis lineatopis (lguanidae) Genus Progarnia G. lainsoni (Telford, 1986) Garnham & Duggan 1986 in P. archosauriaeLainson, this paper in Caiman crocodilus Phylodactylus ventralis (Gekkonidae) crocodilus (Crocodilia) G. marginata (Telford, 1979) Garnham & Duggan 1986 in Anolis frenatus (lguanidae) G. scorzai (Telford, 1978) Garnham & Duggan 1986 in P. ventralis (Gekkonidae) * Modified from Lainson (1992). for 3 min or in aqueous Bouin's fixative for 20 mino characters of the family Garniidae Lainson, Landau Methyl alcohol-fixed smears were immediately & Shaw, 1971. Differentiated from the gentiSGarnia stained in Giemsa stain (30 drops to 15 ml of (located only in erythrocytes) and Fallisia (only in distilled water buffered to pH 704)for 90 mino Bouin- thrombocytes and lymphocytes) by its development fixed blood films were washed in 70 % ethyl alcohol in erythrocytes, thromboycytes and a variety of until colourless, and then stained by a modified leucocytes. Giemsa method (Lainson, 1958)0 Photo-micrographs were prepared using a Zeiss Photomicroscope III and Kodak TMX 402 filmo Progarnia archosauriaenovo gen., novosp. Merogony RESULTS The length of the initial merogony cycle remains Of 19 young caimans examined, 7 were infected with undetermined, but the impression gained was that a non-pigmented haemosporine in the leucocytes, severalweeks elapsebefore gametocytes first appear thrombocytes and erythrocytes. Infected animaIs in the blood. In alI of the infected animaIs, meronts appeared unaffected by the presence of the parasite. were most frequent in lymphocytes and monocytes Development of the organism in alI three lines of (Figs 1 A-C and 2A-E), in which the parasite may blood cells precludes its i~lusion in the genera produce from 8 to 22 merozoites of approximately Fallisia and Garnia, and it is consequently given new 3,0 x 1.7pm (Figs 1 D and 2F, G). generic and specific names within the family Merogony in the thrombocytes (Fig. 21) was Garniidae. somewhat less frequent and produced smaller numbers of merozoites. Parasites in the red blood cells were infrequent, and predominantly in the pro- DEFINITION AND DESCRIPTION erythrocytes (Figs 1 F, G and 2J-L). Twenty Progarnia nov. gen. A non-pigmented haemosporine developing erythrocytic meronts were carefully (Apicomplexa: Haemosporina: Garniidae) with the examined under polarized light illumination and no Fig. 1. (A-M) Progarnia archosauriaenovo gen., novosp. in the blood of Caiman crocodilus crocodilus,as seen in Giemsa-stained blood films. (A) Young 2-nucleated meront in a lymphocyte; (B, C) developing meronts in monocytes; (D) 'smear-cell' (disintegrated lymphocyte or monocyte) with liberated merozoites; (E) trophozoite in a thrombocyte; (F, G) developing meronts in pró-erythrocytes; (H, J) young macrogamonts in a thrombocyte and a monocyte; (I, K, L) mature macrogamonts in a monocyte, basophil and a throtnbocyte; (M) mature microgamont in a thrombocyte. Parasitology Vai. 110Part 5 Figo 1 LAlNSON (Facingp.514) Haemosporina of crocodiles 515 ~ o Fig. 2. (A-R) Photo-micrographs of Progarnia archosauriaenovo gen., novo sp., in Giemsa-stained blood films of Caiman crocodiluscrocodilus. (A, B) Early meronts in lymphocytes; (C-E) meronts in monocytes; (F, G) groups of merozoites from ruptured leucocytes (note the azurophilic granules, conspicuous in (D) and (F)); (H, I) young trophozoite and early meront in thrombocytes; a-L) early meronts in pro-erythrocytes; (M-P) developing macrogamonts in thrombocytes, monocytes and lymphocytes; (Q, R) mature macrogamont and microgamont in monocytes. evidence of pigment was detected in any of the speciesof Garnia and Fallisia, occur in the cytoplasm parasites. The only mature erythrocytic meront seen flOro the earliest stagesof division and persist in the produced 8 merozoites. merozoites, where they resemble the kinetoplast of a Azurophilic granules, similar to those described in leishmanial amastigote (Figs 1 D and 2 F). These ~ R. Lainson 516 granules, which are algo very conspicuous in the gamonts, are much less obvious in Bouin-fixed Type locality material. The meronts usually possess abundant Island of Marajó, Pará, north Brazil. vacuoles in their cytoplasm, which stains extremely delicately. This, and the frequent absence of an obvious patasitophórous vacuole makes the
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