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In the Brazilian Lizard Polychrus Marmoratus (Iguanidae): Experimental Transmission by Culex Pipiens Fatigans

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In the Brazilian Lizard Polychrus Marmoratus (Iguanidae): Experimental Transmission by Culex Pipiens Fatigans (1976), 72, 225-243With 6 plates and 8 figures in the text Schellackia landauae sp.nov.(Eimeriorina: Lankesterellidae) in the Brazilian lizard Polychrus marmoratus (Iguanidae): experimental transmission by Culex pipiens fatigans LAINSON, J. J. SHA W and R. D. W ARD The WellcomeBelém, Parasitology Pará State, Unit, Brazil Caixa Postal' 3, I Received 19 September1975) SUMMARY A new haemogregarine, Schellackia landauae sp.nov., is described in the Brazilian lizard Polychrus marmoratus (Linn) from Pará State, north Brazil. Sporozoites are found principally in the red blood cells (840;0) in the peripheral blood but algo occur in lymphocytes and monocytes. Experimental transmission to three uninfected P. marmoratus was achieved after feeding them with laboratory-bred Oulex pipiens fatigans which had engorged on an infected lizard 14 days previously. The cycle of development in the smáll intestine of P. marmoratus takes approximately 30 days: schizogony, gametogony and fertilization of the macro- gametocytes is in the epithelial cells of the gut, with zygotes penetrating the lamina propria, where the mature oocysts develop. Living oocysts average 14-3 x 13.3 /lm, and are approximately 10-0/lm as seen in histological sections. During the period of intestinal development, the parasite algo undergoes asexual multiplication within cells of the spleen and liver by a process which appears to be endodyogeny. The exact time required before the first invasion of the peripheral blood by the sporozoites remains to be ascertained, but is some time within 30-45 days after the lizard ingests the infected mosquitoes. Morphology of the sporozoite in the vertebrate host is variable and depends on the host cell occupied; there may be 1 or 2 refractile bodies. Reduction or fusion of these to a single refractile body in those sporozoites within the gut cells of the infected mosquito suggests that the bodies may represent some form of energy source that is used up during this latent phase in the insect vector. Accumulation of sporozoites takes place in the reticulo-endothelial cells of the viscera, in particular the pigment- laden cells of the liver and lung. Attempts to infect other species of lizards, Tropidurus torquatus (Iguanidae) and Ameiva a.meiva (Teiidae) failed. Other specics of Schellackia are comparcd with S. landauae. There is a gradation of predilection for the gut epithelium among the known species which supports the hypothesis of evolution of the 'higher coccidia' (Eimeria, Isospora, etc.) from a line originating from a faecally transmitted, octozoic parasite such as a Tyzzeria. 225R.Parasitolf!gY 226 LAINSON, J. J. SHAW AND R. D. WARD INTRODUCTION Polychrus marmoratus (Linn) is a beautifully marked iguanid, commonly found in low trees and shrubs. Over the last 10 years we have examined blood films from 148 specimens, most from Capanéma, Pará, north Brazil, and 17 (11.5%) of these \Vere infected with the new species of Schellackia described below. It is named Schellackia landauae sp.nov., in honour of our good friend Irene Landau, who has contributed much to our better understanding of the haemogregarines. MATERIALS AND METHODS Methods ofmaintenance and bleeding oflizards from the orbital sinus have been given elsewhere (Lainson, Landau & Shaw, 1971; Lainson, Shaw & Landau, 1975). We might add, here, that the insect diet of P. marmoratus was conveniently sup- plemented by hand-feeding with small pieces of freshly killed baby mice. Blo()d films were air-dried as rapidly as possible, fixed in absolute methanol and stained for 90 min in double-strength Giemsa stain (30 drops of stain to 15 ml buffered distilIed water, pH 7-4). Tissue smears of liver, spleen, lung, kid- ney, bone-marrow and brain were treated in the garoe manner or were fixed in aqueous .Bouin's fixative and stained by a modified Giemsa method (Lainson, 1959). Pieces of tissue were fixed in Oarnoy's fluid and histological sections were cut at 4 pm: these were stained by the Giemsa-colophonium method (Bray & Garnham, 1962) Drawings and photographs of the living parasites were made using phase- contrast ilIumination, and photomicrography employed the use of a Zeiss W.L. research microscope, using Adox KB 14 and 17 and Agfa Isopan IF, 35 mm films. Ali measurements are given in micrometres. Mosquitoes used in transmission experiments were from a local, laboratory-bred colony of Oulex pipiens fatigans. FolIowing the infective blood-meal they were maintained on a 50 % sucrose solution, at a temperature of from 24-26 °0 and a humidity of about 85-95 %. Transmission experiments In March 1974 we obtained a P. marmoratus which was showing unusually abundant haemogregarines in the peripheral blood. Luckily we had, at the same time, three clean P. marmoratus, the blood of which had been consistently nega- tive during a period of about 3 months. Approximately 200 mosquitoes were en- gorged on the infected lizard and, 14 days later, batchesof 20 of these insects were hand-fed to each ofthe clean lizards. Blood films were taken from the experimental animaIs after 8, 15, 20, 25, 28, 29, 30 and 45 days. One of the P. marmoratus (L.2917) was killed and autopsied on the 23rd day after its meal of infected mosquitoes, another (L.2871) on day 30, and the last (L.2918) on day 45. In a separare experiment, similarly infected mosquitoes were fed to two other species of lizards -a Tropidurus torquatu~ (Iguanidae) and an Ameiva ameiva lTeiidae) . R. Figs. 1-5. Schellackia landauae sp.nov., from the lizard Polychrus marmoratus. Developing oocysts as seen in fresh scrapings from the small intestine of an experi- mentally infected lizard. Fif!;. 6. Four freed sporozoites from rttptured oocysts: note variable number of refractile bodies. Bouin-fixed, Giemsa-stained. 228 R.LAINSON,J.J.SHAW AND R.D.WARD RESULTS P. marmoratus (L. 2917): 23-day-old infection No parasites could be found in smears of the liver, spleen, lung, kidney, bone- marrow or brain of the animal killed on the 23rd day. Smears and sections of the small intestine, however, showed enormous numbers of mature and developing schizonts and smaller numbers of immature microgametocytes and macro- gametocytes, alI within the epithelial cells of the gut: no mature oocysts wereseen. As the lizard had never shown coccidial oocysts in its faeces during its captivity, we felt confident that these developmental stages were those of the haemogregarine and that we were probably dealing with a Schellackia species. P. marmoratus (L. 2871): 30-day-old infection Smears and sections of the intestine showed an increased number of mature male and female gametocytes in the epithelial cells and, in addition, occasional mature oocysts in the sub-epithelial tissue: intestinal schizogony remained at a high leveI.. Impression smears of the spleen and liver showed a process of asexual division within the lymphocytes and monocytes, which we interpret as endodyogeny. P. marmoratus (L. 2918): 45-day-old infection Unfortunately we were unable to take blood films from this lizard between day 30 (smears negative) and day 45, when it was killed and examined. On the 45th day, however, sporozoites were present in scanty numbers in the red and white cells of the peripheral blood and in smears of the viscera. Smears and sections of the intestine revealed a massive infection, mainly composed of developing and mature oocysts and innumerable free and intracellular sporozoites in the sub- epithelial tissues. Fresh preparations of scrapings from the gut wall provided large numbers of developing oocysts, typical of Schellackia, as illustrated in Figs. 1-5: from this experiment we could only deduce that the time required for the sporozoites to reach the peripheral blood was between 30 and 45 days. Fig. 7. Diagrammatic representation of the life.cycle of Schellackia landauae sp.nov. (A) Sporozoite in epithelial cell of mosquito stomach, 14 days after infective blood- meal. (B) Sporozoites penetrare epithelial cells of small intestine of lizard, Polychrus marmoratus, after ingestion ofinfected mosquitoes. (C, D) Development ofmicroschi- zonts and micromerozoites. (E, F) Development of macroschizonts and macromero. zoites. (G) Asexual division in monocytes and lymphocytes of spleen and liver, apparently by endodyogeny, producing groups of tachyzoites, and probably iJlitiated by micromerozoites. (H, I) Development ofmicrogametes andfertilization of macrogametes in epithelial. cells of small intestine. (J, K) Entry of fertilized macrogamete into lamina propria and development of oocysts containing eight sporozoites. (L) Liberation of sporozoites from rupturing oocysts: entry of reticulo..endothelial cells and penetration of capillaries. (M, N) Entry of white and red cells of peripheral blood: note rolled-up form in erythrocyte. (O) Infective, diapausing sporozoites in the reticulo.endothelial cells of liver, lung and other viscera. Schellackia landauac sp.nov. 229 ~ Fig. 7. For legend see opposite. 230 R.LAINSON,J.J.SHAW AND R.D.WARD Tropidurus torquatus and Ameiva ameiva N"either of these lizards showed any evidence of infection when they were killed on the 45th day follo,ving their ingestion of the infected mosquitoes. The following description is based on material from both experimental and natural infections in P. marmoratu8. The life-cycle is shown diagrammatical1y in Fig.7. Schellackia landauae sp.nov. The sporozoites The morphology oí the sporozoitevaries considerably, dependingon whether or not it is within a host cell, and on the type oí host cell it eventually occupies. ln the intact oocyst, or freshly emerged(Fig. 4; PIso 5D, E; 6B) The living sporozoite is a slender, curved body measuring approximately 13.0 x 3.0, with one end broader and more acutely pointed than the other: when released from the oocyst it may undergo brief gliding movements. The nucleus of stained speci~ens is often band-form, made up of a small number of densely staining granules and usually placed centrally in the organism: it may sometimes, however, be located at either extrernity.
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