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Hepatozoon Gracilis</Emphasis> (Wenyon, 1909) Comb. Nov Parasitol Res (1987) 73:507-514 Parasitology Ze~schfiff ~r Research.........Parasilenkur~de Springer-Verlag 1987 Developmental stages of Hepatozoon gracilis (Wenyon, 1909) comb. nov., a parasite of the Egyptian skink, Mabuya quinquetaeniata A.-R. Bashtar, F.A. Abdel-Ghaffar, and M.A. Shazly Cairo University, Faculty of Science, Zoology Department, Cairo, Egypt Abstract. Developmental stages of Hepatozoon The coccidial nature of a group of parasites which gracilis (Wenyon, 1909) comb. nov. are described occur in erythrocytes or leucocytes of cold-blooded from the tissues of Mabuya quinquetaeniata, an vertebrate animals was elucidated by Reichenow Egyptian skink, and from the mosquito Culex pi- (1910, 1921). These have long been known by the piens molestus. Schizogony occurred in the paren- name haemogregarines (Danilewsky 1885). chyma cells of the skink liver. There were two types Haemogregarines are cosmopolitan blood par- of schizonts: one with 25-50, average 40, micro- asites which are apparently distributed among all merozoites and the other with 3-16, average 11, reptiles of the world (Hoare 1920, 1924, 1932; Ro- macromerozoites. Gametocytes developed in bin 1936; Ball 1958, 1967; Hull and Camin 1960; erythrocytes and measured 18-22.5 pm in length Beyer 1977, 1982; Allison and Desser 1981; Beyer and 0.9-1.4 gm in width (mean of 21.3 x 1.14). et al. 1983; Bashtar et al. 1984a; Daly et al. 1984; After syzygy in the haemocoel of the mosquito, Abdel-Ghaffar 1985). These intracellular parasites the microgamont produces four uniflagellated mi- may produce a considerable hypertrophy of the crogametes (8 x 3 gm with a flagellum of about parasitized erythrocytes (Ball et al. 1969; Beyer 22.5 pm); on day 3 post infection (p.i.) one of them 1977, 1982; Nadler and Miller 1984) and some- fertilizes the macrogamete. Development of the oo- times also of some internal organs (Hoogstraal cysts took place in the mosquito haemocoel leading 1961 ; Furman 1966). In the majority of the studied to formation of an average of 28 sporoblasts/oo- cases, only stages parasitizing the peripheral blood cyst (range 8-50)on days 10-12 p.i. Beginning at of the vertebrates have been described and few life day 16 p.i. (8-24) averaged by 17 sporozoites per cycles have been completely followed in both the sporocyst were observed. Each sporozoite is curved vertebrate and the invertebrate hosts (Reichenow and banana-shaped with round ends measuring 1921; Robin 1936; Mackerras 1962; Allison and 10 x 32 pro. On the basis of its sporogonic develop- Desser 1981 ; Bashtar et al. 1984a). ment in the mosquito, the haemogregarine from The present study describes the complete life Mabuya quinquetaeniata which Wenyon (1909) cycle of a haemogregarine parasitizing the Egyp- named Karyolysus gracilis is transferred to the gen- tian skink Mabuya quinquetaeniata and the mos- us Hepatozoon. Experimental transmission was quito Culex pipiens molestus. successful by oral administration or by i.p. inocula- tion of the infectious stages (sporozoites) to unin- fected skinks and led to the appearance of blood Materials and methods stages after 5 or 4 weeks, respectively. Animals Abbreviations. DMS developing merozoites; DSP developing Lizards. Adult male and female skinks Mabuya quinquetaeniata, sporoblasts; DSPR developing sporozoites; E erythrocyte; F (Scincidae; Marx 1968) were collected from Abu-Rawash and Flagellum; HC host cell; MS merozoites; MA macrogamete; Kirdasah areas (Egypt) and maintained in glass cages with sand MG microgamete; MIG microgamont; N nucleus; NH nucleus and alluvium in an animal room. Water and food (insect larvae of the host cell; OC Oocyst; P erythrocytic parasite; PV par- and woodlice) were given to them regularly. asitophorous vacuole; RB residual body; SCH Schizont; SP Sporoblast (s); SPC Sporocyst (s); SPR Sporozoite (s); ZY Vectors. Mosquitoes of the species Culexpipiens molestus (Culi- Zygote cidae) were used as the invertebrate vector. They were colonized Reprint requests to." A.R. Bashtar successfully at room temperature in the laboratory. Mosquito 508 A.-R. Bashtar et al. : Studies on Hepatozoon gracilis larvae were fed with Tetramin (commercial fish food) and the was elongated, slender and sometimes tapered. The adults with 5%-10% sugar solution. nucleus of the host cell was displaced laterally or sometimes pushed to the other pole. Uninfected Parasites. Lizards were tested for haemogregarines by making a thin blood film from each by clipping off the tail tip. Blood red blood cells measured 13.15_+ 1.39 gm x 8.65_+ films were fixed in absolute methanol (5 rain) and stained with 0.28 gm. Infected red blood cells showed slight hy- 3% Giemsa solution in phosphate buffer (pH 7.3) for at least pertrophy and faintly stained cytoplasm (Fig. 1) 30 min. Infected lizards were selected and exposed to mosqui- and measured 19.58 _+ 1.84 gm x 5.62_+0.28 gm. toes. The nucleus of the parasite stained dark pink with Giemsa stain and was often elongated, span- Fixation, embedding and microscopy ning the entire breadth of the parasite. It was usu- Pieces of the highly infected skinks of about 3 mm from the ally composed of an aggregation of chromatin liver, lung, spleen, brain, kidney, heart, stomach, ileum and granules and in some cases appeared fragmented. skeletal muscles and mosquito abdomen were taken and fixed in 5% (v/v) glutaraldehyde buffered in 0.1 M sodium cacody- The nucleus measured about 10.2• late (pH 7.3) for at least 4 days at 4 ~ C. After 4-5 washings 1.13_+0.19 gm. The parasite's cytoplasm usually in the cacodylate buffer for I0 15 min each, the specimens were stained pink to light red. No vacuoles were seen dehydrated in a series of alcohols, cleared in butanol, embedded in the cytoplasm (Fig. 1). in Paraplast and sectioned on a rotary microtome. The sections were stained with hematoxylin and eosin. The stained sections and blood smears were examined by a Zeiss research photomi- croseope. Mean values_SDs with number of measurements Schizogony and merozoites in parenthesis are given. Various developmental schizogonic stages were ob- served exclusively in the liver of the infected skinks. The parasitized cells are mainly the liver parenchy- Results ma cells. None of the schizogonic stages were seen in the circulating blood, lung, spleen, skeletal mus- Natural incidence and levels of parasitaemia cles, brain, heart, kidney or in the alimentary canal In all 168 (40%) out of 420 collected skinks, Ma- of the infected skinks. buya quinquetaeniata, were found to harbour hae- The schizogonic process begins in the liver after mogregarines on initial examination. The parasit- leaving the parasitized erythrocytes; the parasite aemia in skinks was high: 1%-8% and in some (sporozoite or later a merozoite) invades the paren- cases 40%-50% of the erythrocytes were parasit- chyma cells, becomes more rounded or ovoid and ized. begins to grow in size (Figs. 2-4). As the parasite invades the parenchyma cell, a parasitophorous vacuole encloses it and enlarges during the Blood stages of the parasite growth of the schizont (Figs. 2-7). The smallest In peripheral blood smears, the parasites were usu- schizont seen within the liver parenchyma cells ally intracellular (Fig. 1), but sometimes extracellu- of the infected skinks (Fig. 6) measured lar parasites were also seen in some smears, per- 9.11 x 9.11 • 0.15 gm, while the largest schizont haps as the result of trauma. The intracellular par- (Figs. 2-4) measured 22.72___1.21 gm x 18.25_+ asites parasitized red blood exclusively. Doubly in- 0.51 gm. The nucleus of the schizont usually di- fected erythrocytes were observed on several occa- vided many times, forming many new nuclei which sions, especially in cases of high parasitaemia. migrate to the periphery of the schizont (Figs. 2, Most parasites were enclosed within a clear par- 3). When the daughter nuclei are at this stage the asitophorous vacuole, but sometimes no space or merozoites develop, leaving a residual body membrane was observed between the parasites and (Figs. 3, 4). The number of merozoites produced the host cell cytoplasm. is variable and may indicate the presence of two Two developmental stages of the parasite oc- types of schizonts. The first type, called macroschi- curred in the blood. The first, a small form, mea- zont, gives rise to 40• 7.75 gm narrow, elongated sured 12.75 • 1.4 gm in length and 0.85 +0.05 gm merozoites (micromerozoites). These measured in width. It was usually smaller than the host cell. 13.45 • gm by 1.02• gm while their elon- The second, a mature form, was crescent-shaped gated nucleus measured 5.32• gm x 1.02_+ and longer than the host cell; it measured 0.15 gm (Fig. 4). The second type of schizont 21.3 • 1.52 gm x 1.14• 0.20 gm and is considered which may be called "microschizont", produces a gamont, whereas the small form represents a re- about 11 ___4.21 gm large merozoites (macromero- centy penetrated and transformed merozoite (tro- zoites) which measured 16.65• gm by phozoite). In all cases, the body of the parasite 1.13-t-1.21 ~tm (Figs. 6, 7). A.-R. Bashtar et al. : Studies on Hepatozoon gracilis 509 Fig. 1. Giemsa stained blood smear of the skink showing intraerythrocytic parasites (P). x 2500 Fig. 2. Macroschizonts (SCIO in liver parenchyma cells showing many nuclei (N) at the periphery. x 2000 Fig. 3. Macroschizont (SCH) with peripheral nuclei (N). x 1800 Fig. 4. Macroschizont (SCH) with micromerozoites (MS) and a residual body (RB). x 2200 Fig. 5. Macroschizont in transverse section with merozoites (MS) and residual body (RB). x 2500 Gamogony syzygy within a parasitophorous vacuole in a host cell, and began to differentiate into micro- and Some merozoites, instead of repeating the schizo- macrogamonts (Fig.
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