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Neglected Parasites, with Particular Reference to Members of the Coccidia (Protozoa: Apicomplexa)

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Neglected Parasites, with Particular Reference to Members of the Coccidia (Protozoa: Apicomplexa) ECO 92: Vrotozooíogy In Títe Amazon A protozoologist in Amazónia: Neglected parasites, with particular reference to members of the Coccidia (Protozoa: Apicomplexa) RALPH LAINSON, F. R. S. Departamento de Parasitologia, Instituto Evandro Chagas, Fundação Nacional de Saúde, Caixa Postal 3, Belém, PA 66001, Brasil Gamham's fears might well be extended to a whole range In spite of the vast source of material avaílable of other parasites of threatened host-species. It is a reflec- in Amazónia, the extraordinarily rich variety of tion of our highly biased sense of values that while impas- protozoal parasites in its fauna remains virtu- sioned pleas may be made for the preservation of the Ama- ally neglected. During some 26 years investigat- zonian crocodile, no consideration is given to the impending ing the role of wild animais as reservoirs of doom of ÍLS beautiful trypanosome (Fig. 1) (2). Leishmania, the author has been able to take a While the author's past 26 years in Amazonian Brazil brief but rewarding look at other parasites. have been largely dedicated to studies on the eco- epidemiology of leishmaniasis, they have also provided a This review discusses some of the more interest- unique opportunity to examine a wide variety of wild animais ing ones, in particular some controversial, "ma- for parasites other than Leishmania. Some of the more interest- larial parasites" of lizards; haemogregarines of ing ones, within the subclass Coccidia, are discussed in this re• reptiles and fish; and a variety of intestinal view, and the following classification, based largely on that of Coccidia of birds, reptiles and mammals. Levine et al (3), will help appreciate their taxonomic position (Table 1). Apesar da vasta fonte de material que existe na Amazónia, a riqueza de parasitas protozoários da fauna foi praticamente if-norada. Durante aproximadamente 26 anos, pesquisando o papel de animais silvestres como reservatórios de Leishmania, o autor teve a oportunidade de fazer The Suborder Haemosporina uma breve mas proveitosa pesquisa de outros parasitas. Esta revisão focaliza aiftuns dos mais interessantes, incluindo uma família de "parasitas maláricos" de lagartos: hemonref>arinas de répteis e peixes: e Until 1971 this was divided into three families of blood uma variedade de coccídeos intestinais de aves. répteis e mamíferos. parasites. The Plasmodiidae, containing species of Plasmodium, the "true" malarial parasites of reptiles, birds and animais; the Haemoproteidae, found in similar hosts; he English parasitologist P. C. C. Garnham was once heard to remark that "There is a serious dan- ger that the malarial parasites of man may hecome T extinct". As a leading malariologist of his time, he clearly was not expressing a wish to see the huge loss of human life due to inalaria, he simpiy was voicing the natu• Figure 1. ral concern of a scientist that adequate specimens of the Trypanosoma cecili Lainson, parasites should be preserved before their possible extinc- 1977, from the tion! cayman, Caiman Unfortunately for the human race, eradication of ma• crocodilus crocodilus. lária has yet to be achieved: fortunately for Garnham, a) In an specimens of many malarial parasites are now safely depos- impression smear ited in a Type Collection, bearing his name, in the of kidney; h) In Wellcome Institute of Tropical Medicine, in London (1). the peripheral hlood. Note conspicuous myonemes. Corrcspondcncc to: Ralph Lainson, F.R.S., Departamento de Parasi• Giem.sa's stain. tologia, Instituto Evandro Chagas, Fundação Nacional de Saúde, Caixa Ref. 2. Postal 3, Belém, PA 66001, Brasil Volume 44(2/3) • March/June 1992 Ciência e Cultura (Journal of the Brazilian Associalion for the Advancement of Science) • 81 ECO 92: FrotozooíogtflnT/teAmazon Table 1 — Outline classification of the subclass COCCIDIA ^ ^ :f Kingdom: PROTISTA Haeckel, 1866 Subkingdom; PROTOZOA Goldfuss, 1817 Phylum: APICOMPLEXA Lcvine. 1970 Class; SPOROZOEA Lcuckart, 1879 Subclass: COCCIDIA Lcuckart, 1879 • • I • # Usually with gamonts (Cf & Ç), small and intraccllular: e life-cycle variably wilh asexual and sexual stagcs (i.c. schizogony, gamctogony and sporogony). r Ordcr: AGAMOCOCCIDIIDA Levinc. I >1) • Order: PROTOCOCCIDIIDA Kheisin, 1956 i Ordcr: KUCOCCIDIIDA Lcgcr & Duboscq, 1910 ti • (Wilh schizogony, gamctogony and sporogony) g h i Figure 2. Plasmodium vacuolatum Luinson, Shaw & Landau. 1975 in Subordcr: ADELEINA Lcgcr, 191 I crylhrocyles ofihe lizard Plica umbra. a} younfi Irophozoile: h-f) devel- tí" and Ç assoeiale in pairs: CJ" produeing 1-4 opinií schizonts; íi-h) younf> male and fcmale iiamcíoryles: i-j) mature microgametes: Sporozoitcs in fragile envelope female and male iiamclocytcs. Note prt)minent vacuole containing the malarial pií^ment in ali síai^es of development. Ref. 13. Familics: ADELEIDAE Plasmodium species in mammals of the New World KLOSSIELLIDAE appear to be limited to man and monkeys (5,6,7,8), and this HAEMOGREC.ARINIDAE general opinion has been supported by the results of our LEGERELLIDAE own search for these parasites in blood films from many hundreds of wild mammals of many different species. Subordcr: EIMERIINA Lcgcr, 1911 In sharp contrast, the genus Plasmodium is particularly O* and Ç devcloping scparatcly: C? produeing fcw to well represented in a wide variety of New World lizards, many microgametes: sporozoitcs typieally encloscd in a sporocyst, within oocyst and occasionally snakes (9). The first records of saurian plasmodia in the Américas were those of Aragão & Neiva e.g. Familics:LANKp;STERELLIDAE (10), in 1909, who described P. diplo)>lossi in the legless EIMERIIDAE "glass lizard", Diploglossus fasciatus (Anguidae) from SARCOCYSTIDAE Xerém, near Rio de Janeiro, and P. tropiduri from Tropidurus torquatus (Iguanidae) captured in Minas Gerais. Subordcr: HAEMOSPORINA Danilcwsky, 188.5 Strangely enough, P. diploglossi was apparently not seen Ò' and Ç dcvelop scparatcly: Ó" produeing 8 again until 1968 when we recorded its presence, together flagellatcd microgametes: zygole motile (ookinele): with that of P. tropiduri, in a different lizard, Mahuya sporozoitcs naked. mahouya (Scincidae) in Belém, Pará, North Brazil (11). cg. Familics:PLASIVIODIIDAE P. cnemidophori Carini, 1941 (12) was fir.st discovered HAEMOPROTEIDAE in the little lizard Cnemidophorus lemniscatus from Goiás, LEUCOCYTOZOIDAE Brazil. Interestingly, we have found this parasite to be very GARNIIDAE much more common in the related lizard Ameiva ameiva Taxa di.scussed in this paper are in BOLD TYPE (Teiidae), from Pari-Cachoeira on the Brazil-Colombia bor- der, and Belém (11). and the Leucocytozoidae, seemingly restricted to birds. Finally, our own laboratory described a new plas• In 1971, however, a new group of saurian blood para• modium, P. vacuolatum, found in the silvatic lizard Plica sites which possessed characters precluding their inclusion umhra (Iguanidae) from Belém (13). Among its other char- in any of these families was discovered. A new family, acteristics this little parasite is notable for the conspicuous named the Garniidae in honor of malariologist P. C. C. vacuole containing the pigment granules, in ali stages of its Gamham, was erected for their inclusion (4). The charac• development in the red blood cells (Fig. 2). ters separating the 4 families are given in Table 2. The genus Billhraya Papema & Landau, 1990, was re- cently described in an Australian lizard, Phyllodactylus Family Plasmodiidae: The genera Plasmodium and Billhraya Table 2 — Taxonomic characters separating lamilies of lhe subordcr HAEMOSPORINA". Character Pla.^modiidae Leucocytozoidae li aemoproteidae Garniidae Although we have recorded the presence Schizogony in blood Yes No No Yes of Plasmodium in some Amazonian Wilh malarial pigment Yes No Yes No birds, the subject of avian malária has Gametoeylcs in mature Yes No Yes Yes (Garnia) not been pursued further in our labora- erythrocytcs No (Falli.ua) tory. ' Modificd from Garnham (5). 82 • Ciência e Cultura (Journal of the Brazilian Associatíon for the Advancement of Science) Volume 44(2/3) • IVIarch/June 1992 ECO 92: Vrotozooíogyln^fieAmazm resemblance to those of Leucocytozoon and Akiha (Fig. 3) — a similarity which was enhanced by our failure to demonstrate schizogony of the parasite in the blood of captive lizards examined over periods of several months. For these reasons the para• site was regarded as a member of the Leucocytozoidae (Table 2), previously known only from birds, and given the new generic name oi Saurocytozoon (15). The sporogonic cycle of S. tupinamhi was fol- lowed in experimentally infected mosqui- lOn toes, Culex pipiens fatigans (16): it differed sufficiently from that of Leucocytozoon to invalidate the suggestion that Saurocytozoon is a synonym of the latter parasite (17). A second species, S. mahuyi was subsequently described in another lizard, Mahuya mahouya (18). Family Garniidae: Garnia and Fallisia The genus Garnia — Examination of liz• ards from a locality near Xavantina, Mato Figure 3. Family Grosso, Brazil, in 1967, had revealed an• Leucocytozoidae. Mature 10 other interesting blood parasite in the teiid í>ameiO(yles in leucocyles <>f lhe periplieial hloocl. Ameiva ameiva. Trophozoites, schizonts a.h) /•'entale and male fornis and gametocytes in the mature erythrocytes of Alciba caulleryi af lhe were at first thought to be those of Plas- hird. Gallus domesticas, fram Garnham. ref. 5; c.d) Female moclium, but the use of polarized light and and male i^amelocyte.s of electron microscopy established that in no Saurocytozoon
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