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Home , Caryospora (alveolate), Cyrilia, Draco maculatus, Eimeriorina, Fallisia, Frenkelia

ECO 92: Vrotozooíogy In Títe Amazon

A protozoologist in Amazónia: Neglected parasites, with particular reference to members of the (: )

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 -. 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 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). , 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 , 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 ; haemogregarines of ing ones, within the subclass Coccidia, are discussed in this re• and fish; and a variety of intestinal view, and the following classification, based largely on that of Coccidia of , reptiles and . 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 uma variedade de coccídeos intestinais de aves. répteis e mamíferos. parasites. The , containing species of , the "true" malarial parasites of reptiles, birds and animais; the , 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 due to inalaria, he simpiy was voicing the natu• Figure 1. ral concern of a scientist that adequate specimens of the 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 ; h) In Wellcome Institute of Tropical , 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 : PROTISTA Haeckel, 1866 Subkingdom; PROTOZOA Goldfuss, 1817 : APICOMPLEXA Lcvine. 1970 ; 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 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 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 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 (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 "glass lizard", Diploglossus fasciatus (Anguidae) from Xerém, near Rio de Janeiro, and P. tropiduri from Tropidurus torquatus () 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 much more common in the related lizard Ameiva ameiva Taxa di.scussed in this paper are in BOLD TYPE (), 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 () 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 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 of the latter parasite (17). A second species, S. mahuyi was subsequently described in another lizard, Mahuya mahouya (18).

Family Garniidae: Garnia and

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. , 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 established that in no Saurocytozoon tupinambi stage of development did the organism pro- Laínson & Shaw. 1969 in the duce malarial pigment (19,20). By defini- lizard. Tupinambus nigropunc- tatus. Ref. 15. tion, therefore, the parasite could not be in- Figure 4. Garnia telfordi cluded in either the Plasmodiidae or the Lainson. Landau & Shaw. Haemoproteidae, and the presence of a 1971. in the teiid lizard schizogonic cycle in the blood precluded its Ameiva ameiva. a.h} Youní^ and f^rowiní> trophozoites; inclusion in the Leucocytozoidae. •4V e) Younii amoehoid .schizoni: The subsequent finding of similar d) Douhle of pigmentless parasites in other species of liz• d erythroeyte with a younj> female i^ametocyte and a ards led US to erect a fourth family within sehizont: e) Multiple infection the Suborder Haemosporina, to which we t of schizont.s: f) Mature gave the name Garniidae (4). The type ge• .sehizont with separated merozoites: Í^) Mature female nus received the name of Garnia and the í>ametoeyte and .sehizont: type species became Garnia f^onatodes h) Mature male s>ametoeyte and (previously described as a species of Plas- youníí female: i) E.\flaí>ellatínií modium in the lizard Gonatodes, by Telford male ^amelocyte. Ref. 4. in 1970). The parasite of Ameiva was named Garnia telfordi (Fig. 4) as a tribute marmoratus (Gekkonidae) (14), and representatives of the to Dr. Sam Telford, the American parasitologist who has genus have yet to be recorded in the Américas. contributed much to our knowiedge of saurian parasites. The genus is characterized by schizogony and gametogony Family Leucocytozoidae: The genera in the mature red blood cells, with no production of ma• Leucocytozoon, Akiha and Saurocytozoon larial pigment.

In 1967 we noted the frequent presence of large male and The genus Fallisia — During these studies an extraordi- female gametocytes in lymphocytes, and occasionally im- nary new haemosporidian was discovered in the teiid lizard mature erythrocytes, in the peripheral blood of the lizard Neu.sticurus hicarinalu.s from various localities in Pará. Al- Tupinamhus nii^ropunctatus (Teiidae). They bore a striking though clearly related to Garnia, it was found to undergo

Volume 44(2/3) • March/June 1992 Ciência e Cultura (Journal of the Brazilian Association for ttie Advancement of Science) • 83 ECO 92: Vrotozooíogy In Títe Amazm both schizogony and gametogony in the thrombocytes and, more rarely, the lymphocytes. The membrane of the infected thrombocyte becomes remarkably thickened, giving it a cyst-hke appearance (Fig. 5). There is no deveiopment in the red biood- cells, and for this reason the parasite Figure 5. Fallisia was piaced in a second genus within effusa Luinson. the Garniidae, named Fallisia in Landau & Shaw. 1974 in thromt>i>cytes honor of the Canadian parasitologist of lhe lizciid Murray Faliis who worked exten- Neusticurus siveiy on other members of the Hae- bicarinatus. a.h) mosporina. The parasite of Neus- Uninfecled thiomho- cytes: c) Young ticurus was given the specific name : d-g) of F. ejfusa, in view of its exuberant Developing schiznnis: deveiopment in the saurian host (19). h) Mature, ruptured scliizoni: i-n) The new genera were not ac- Developing and cepted by some American workers mature feniale and male gumetocytes: o) (9,21,22). While acknowledging the Tlivomhocyte with a lack of pigment, and other biological male gametocyte. peculiarities which were not consist- young schizonts and ent with the existing defmition of the trophozoiíes. Note frequency of multiple family Plasmodiidae and the genus infection of lhe Plasmodium, they preferred to modify thromhocyte and these definitions in order to include modification of its the new parasites. Our opinion has re- ivall lo give a cyst- like appearance. mained, however, that... "Attempts to Giemsas stain. consign ali these parasites to a single Ref. 19. 10 genus result in the forcing of square

( Table 3 — Subordcr HAEMOSPORINA: Family GARNIIDAE)' pegs into round boles, with the repeated necessity of redefining the families for the inclusion of an Differentiated from the families Plasmodiidae and Haemoproteidae hy the ah- sence of malarial pigment. Separated from the Leucocvlozoidae (al.w without • organism which could more conveniently and ment) hy lhe presence of a .schizogony cycle in the penpheral hlood. properly be piaced in a separate group..." (18). Genus Garnia Genus Fallisia Latterly, Telford (23,24), who was strongly G. telfordi Lainson, Landau & Shaw F. effusa Lamson, Landau & Shaw opposed to this view, relented somewhat and 1971: in Ameiva ameiva (Teiidac) 1974: in (Teii- agreed that Fallisia and Garnia should be sepa• dae). TYPE SPECIES rated from the genus Plasmodium. He suggested, G. utingensis LL&S 1971: in Anolis F. modesta LL&S 1974: in Tropidu- however, that they might be used at generic and rus torquatus (Iguanidae) punctatus (Iguanidae) subgeneric leveis, respectively, within the family G. multiformis Lainson, Shaw & Lan• F. audaciosa Lainson, Shaw & Lan• Plasmodiidae: e.g. Fallisia ejfusa and Plasmodium dau 1975: in Plica umhra (Iguanidae) dau 1975: in Plica umhra (Iguanidae) (Garnia) gonalodi. Furthermore, it was sug• G. uranoscodoni LS&L 1975: in Ura- F. simple.x LS&L 1975: in Plica um• noscodon superciUosa (Iguanidae) hra gested, modification of the defmition of the fam• ily now permitted the inclusion of Saurocytozoon G. gonalodi (Telford 1970) LL&S 1971: F. copemani Paperna & Landau in Gonatodes humeralis (Sphaerodac- 1990: in Carlia rhomhoidalis (Scinci- in the Plasmodiidae. Most European workers, tylidae). TYPE SPECIES dae) however, have preferred to retain the family G. morula (Telford 1970) LL&S F. siamen.se (Telford 1986) Paperna Garniidae and its two genera Garnia and Fallisia 1971: in Mahuya mahouya (Scinci- & Landau 1990: in maculatus (1,20,25,26), with increasing support for this (Agamidac) dac) coming from recent ultrastructure studies of these G. azurophilum (Telford 1975) F. {Plasmodioide.s) neotropicalis parasites (20). The suggestion that Saurocytozoon Garnham & Duggan 1986: in Anolis Gabaldon, Ulloa & Zerpa 1985: in lineatopis (iguanidae) various Vcne/.uclan birds gametocytes are those of a Plasmodium species G. lainsoni (Telford 1978) Garnham (27) has yet to be substantiated. & Duggan 1986: in Phylodactylus Species of Fallisia have now been described ventralis (Gekkonidae) from lizards of the Old World, in Thailand (24) G. marginata (Telford 1979) G & D and Austrália (25). Even more interesting is the 1986: in Anolis frenatus (Iguanidae) report of another Fallisia species in birds from G. scorzai (Telford 1978) G & D 1986: in P. ventralis (Gekkonidae) Venezuela (28). A number of parasites previously described as Plasmodium species have since been

84 • Ciência e Cultura (Journal of the Brazilian Association for the Advancement of Science) Volume 44(2/3) • March/June 1992 ECO 92: Vrotozooíogy In Tfie Atnazon

transferred to the genera Garnia and Fallisia (1,4,25), and a large phyllostomids, which we ignored. Only 10 small, hst of the recognized species of these parasites is given in long-tongued bats suspected to be Glossophaga were avail- Table 3. able, and we slipped in a single small short-tongued Myotis nigricans for luck. Family Haemoproteidae: , Lucky it proved to be, for not only was it the only in- Polychwmophilus and other genera fected bat but it was the only one infested with the ectoparasitic fly Basília, specimens of which we had fortu- The genus — Haemoproteids have an nately preserved. Histological sections of these provided ample distribution in birds, reptiles and mammals. We, beautiful specimens of mature oocysts of the bat's parasite, however, have concerned ourselves only with Polychrom• containing large numbers of sporozoites. Garnham retumed ophilus, one of three genera of the family, and infecting to London a happy and contented man, and the elusive bats of both the Old and the New World. While our obser- parasite was subsequently named Polychromophilus deanei vations on this organism have been of modest proportions, in honor of our old friends who had innocently started the they do serve to illustrate the stubbom persistence of some whole affair (31). parasitologists in achieving their goal! In 1938 Maria and Leonidas Deane found the gameto- cytes of a malarial parasite in the red blood cells of The suborder Adeleina Glossophaga soricina, a small nectar-feeding bat, caught in (as defined in Table 1) a banana plantation in Piratuba, Pará. They made drawings of the parasite, but the specimens were lost and it was only Family Haemogregarinidae: , described 23 years later (29), without, however, receiving a , , Karyolysis and Hemoliria name. Previous records of similar parasites from bats in the Ali these parasites are heteroxenous. That is, they have part Américas are few and far between (30), and the descrip- of their life cycle in one host and the rest in one or more tions very meagre. Gamham, with his passionate interest in others. Characteristically they undergo schizogony in the the Haemoproteidae, for this reason nursed a determination, host, ultimately producing gametocytes which verging on obsession, to rediscover the parasite of circulate in the red and/or white cells of the blood of a va- Glossophaga and compare it with parasites of Old World riety of fish, amphibia. reptiles, birds and mammals. The bats. It came as rather a surprise. however, when he advised sporogony cycle takes place in haemotophagous inverte- US that he was coming to Belém for just that purpose, arriv- brates, such as mosquitoes and other dipterans, mites, ing from London in October, 1969. Ali we had to do, he ex- and leeches. plained, was to take him to the banana plantation in Our knowledge of the complete life-cycle and mode of Piratuba, catch the bats and find the parasite! Anyone familiar with the bewildering network of rivers and streams of the Amazon Region will appreciate the task IN LEECH IN FISH that confronted us, and this was further complicated by a mysterious that assailed our distinguished visitor shortly after his arrival, and the cause of which we never did discover. Gamham, confined to bed for nearly two weeks, prob- ably suffered more from sheer frustration than he did from his illness, as he saw his chances of finding his precious parasite slipping from his grasp. In the meantime, however, we had talks with representatives of Petrobrás the Brazilian State oil company in Belém, who were operating in an area quite close to Piratuba and offered to take us as near as possible in their cruiser. The rest of the joumey would be made by outboard motor in a small dinghy which could penetrate the smaller streams. Garnham, still unwell and clearly shaky on his legs, insisted on accompanying us. Needless to say, the area had undergone great changes Figure 6. Cyrilia lignieresi (Lareran. 1906) Lainson. 1981: 1992. during the 31 years that had elapsed since the Deanes had Life cycle in lhe fish Synbranchus marmoratus and lhe leech Hae- worked there, and it proved impossible to pinpoint the ex- menteria lutzi. A} Parasites enrer eiyrhrocyres; B-Hj Snccessivc gen- act locality. We chose some capture-sites on the river eiations of schizonls in eryrhrocytes: l-K) Development of micro- banks, however, put up our mist-nets and took our collec- gametocytes (Kj and maciogametocyies (L): M.N) Rclease of gametocytes in liinten of leech iníestine; O) Association of female and tion of bats back to the cruiser for examination. male gametocytes on surface of iníestine epithelium: P.Q) Male Gamham was unswervingly in favour of dealing only gametocyte produces 4 microgametes. one of which fertilizes the fe• with the small bats which probably were Glossophaga spe• male gametocyte: R-U) Zygote micleiís divides to give an oocyst con• taining fremi 20-30 naked sporozoites. Ref. 33. cies, but to his chagrin most of the catch was made up of

Volume 44(2/3) • March/June 1992 Ciência e Cultura (Journal of the Brazilian Association for tfie Advancement of Science) • 85 ECO 92: Vrotozoology In Tfte Amazm. transmission of many of these parasites is incomplete. In- name of Haemogregarina lignieresi. The French worker fection of insectivorous is generally thought to thought that the host was probably Anguilla vulgaris (the take place after the ingestion of the host, and true eel of the Old World), but as the family Anguillidae that of some (e.g. frogs and toads) may follow has no representative in the neotropics he was clearly deal- the eating of and/or leeches. Haemogregarines ing with S. marmoratus, as later indicated by Leger & of purely aquatic vertebrates, such as fishes, are beheved to Leger (39) in their list of haemogregarines of fish. The cor- be largely transmitted by leeches, but it is possible that rect name of the parasite, in spite of Laveran's very inad- parasitic copepods or isopods may be involved. Although equate description, should therefore be Cyrilia lignieresi most workers have favoured the view that transmission of (Laveran, 1906) nov. comb. (syns., Haemogregarina lignieresi the haemogregarines of aquatic animais is by the bite of the Laveran, 1906; H. gomesi Neiva & Pinto, 1926; Cyrilia gomesi leech (32,33,34), the possibility that it may also take place Lainson, 1981). when the leech is eaten has also to be considered. Finally, a It may well be that other species of Cyrilia will be dis- third host may be introduced into the life cycle of some closed when more details are available on the sporogony of haemogregarines (35). Thus, some Hepatozoon species may parasites previously considered as species of Haemo• inhabit the blood-cells of both lizards and snakes which to- gregarina, particularly those of fish. Species of the two gether provide gametocytes for a vector, such as the mos• genera, at present adequately identified by morphology of quito, in which resulting sporogony produces large numbers their oocysts, are given in Table 4. of sporozoites. Other lizards become infected by eating Very recently Siddall & Desser (34) revealed a hitherto these mosquitoes, while certain snakes also become in• unknown developmental stage of H. halli, a haemo• fected by preying on the lizards. gregarine of , in the leech Placohdella ornata. After It must be remembered that the generalized term formation of the octozoic oocysts in the intestinal caeca, "haemogregarine" is applied to the blood stages of a variety the released sporozoites migrate to the anterior somites of of coccidia, not only within the the leech where they undergo suborder Adeleina but also in the asexual division, each producing Table 4 — Family HAEMOGREGARINIDAE suborder Eimeriina (discussed be- up to 250 merozoites. These mi• low). The term is derived from Species of Haemogregarina and Cyrilia as identified hy grate to the proboscis, from the morphology of their oocysts in the invertebrate host the strange gregarine-like, gliding (vector) where they are inoculated into movements the parasites may subsequent hosts following make when they emerge from the In or turtles: oocysts with 8 sporozoites the bite of the leech. The whole blood cells. Due to the very simi• Haemogregarina stepanowi Danilewsky. 1885 Haemogregarina nicoriae Castellani & Willey. 1904 process, from the initial infec- lar morphology of these blood Haemogregarina halli Paterson & Desser, 1976 tion of the leech to transmission, forms, much confusion has arisen Haemogregarina choudhuryi Ray & Bhattacharjee. 1984 takes several months. Paperna in the literature regarding the ge- (40) described extraintestinal neric nature of many haemo• In fishes: oocysts with many sporozoites "oocysts" of Haemogregarina CvnV/a/(.?/;!>;•«/(Laveran. 1906) Lainson, 1981: 1992 gregarines described purely from CxriUa imcinata (Khan. 1978) Lainson, 1981 species in leeches, which con- blood films. There has been, and tained 40 or more unfortunately still is, a tendency "sporozoites". Siddall & Desser to name these as species of Haemogregarina, when a great (34) considered these not to be oocysts, but to represent a many quite probably belong to other genera. The only safe schizogonic stage similar to that they described for H. method of identifying these organisms is by study of their balli. complete life-cycle, and in particular that part in the in• Whether or not a similar stage occurs in the life-cycle vertebrate vectors. A good example is to be found among of Cyrilia remains to be ascertained. If it does exist, the the haemogregarines of fish. present author would have missed seeing it because his ex- perimentally infected leeches were not examined over a The genera Haemogregarina and Cyrilia — In 1926 sufficiently long period. Neiva & Pinto (36) referred to a haemogregarine in the red blood cells of the "swamp eel", Synbranchus marmoratus The genus — During a visit to the author's (Synbranchidae), as Haemogregarina gomesi, based on the laboratory, in 1986, Dr. Gilles Petit worked on the life-cy• morphology of the blood forms. Lainson (33) studied the cle of a haemogregarine commonly found in the toad Bufo development of the parasite in the leech Haementeria lutzi, marinus, and showed its vector to be the Amblyomma which commonly feeds on this fish, and showed it to pro- rotondatum (41). Among the peculiarities shown by this duce oocysts containing from 20-30 sporozoites (Fig. 6). As parasite were schizogony and cyst formation in the erythro- the oocysts of Haemogregarina species contain only 8 cytes, as well as in cells of the reticulo-epithelial system; sporozoites (Table 4), he removed the parasite of S. sporogony inside the sessile digestive cells of the intestinal marmoratus from that genus and placed it in a new one, caeca of the tick, with the formation of a star-shaped Cyrilia. oocyst; the formation, in these oocysts, of 100-150 division Recently (37) the author's attention has been drawn to products, referred to as "sporokinetes"; and the migration the fact that a very brief description of Cyrilia gomesi had of these bodies into further cells of the digestive tract, been given by Laveran (38), as early as 1906, under the where each parasite produced a "sporocyst" containing

86 • Ciência e Cultura (Journal of the Brazilian Association for tfie Advancement of Science) Volume 44(2/3) • Marcfi/June 1992 ECO 92: Frotozooíogy In Tfie Kmazm

gony" (schizogony), with the production of Figure 7. Sciíellackia landauae Lainsoii. Slum- & Wnid. 1976, in "meronts" giving rise to "merozoites", llw lizLinl Pulychrus marmo- even though this "...contravenes the con- ratus aHíl llw niD.squiio Culex ventional notion of infectivity of sporo• pipiens faíigans. A) Sparozoiíe wiííiin epiílwliíil ccll <>f miisquiio zoites and the restriction of merogony to slomach. 14 days afiei hUxul- the vertebrate host". It is noteworthy that mcal 1)11 iiifcctcil lizani: B) Afler these stages of H. halli do have the typical, ÍHí^cslií)/! of injccicd mosquilo non-cystic appearance of schizonts whereas by úiiolhcr lizard. ilic pai asile peiíelralcs llic cclis iif llw iiiws- those of Hemolivia are very clearly cystic, liiial cpillieliiim: CD) Dc\cli>p- with a thick wall. iiieiil of niicroscliizíiiils prodiw- in<^ niicromerozoilcs: E.í-'} De- velopmeiil of macroschizonls and macrimierozoiícs: 11.li Pro- The Suborder Eimeriina ducíion of micr<>í>amelo(yies (as defíned in Table 1) and macri>í>aniet()cyles: ferlili- zalion: J.K) Zxí^oles niptiire inío própria and prodnce íran- Family Lankesterellidae: sieni íMHysIs canlainiiií; H spino- and zoiles; L-N) Oiwysl.s soon rup- I ////•('. and spin-azoiíes enler red and wliile cells of lhe capillar- These parasites are also heteroxenous ies: Gj Exlra-inteslinal asexual di- haemogregarines, of amphibians, reptiles vision (endodyo)>eny'.') in lhe vís• and birds. Unlike members of the suborder cera oj lhe lizard. of tincerlain .v/ij- Ij nificunce: O) Diapausin!> sporo- Adeleina, however, they have ali stages of zoiles accunuilaling in lelicido- their life-cycle in the vertebrate host, in the endolheliul cells of lhe vise era. tissues of which they ultimately produce Ref. 43. oocysts containing from 8 to very many naked sporozoites. On rupture of these 8-24 "sporozoites". ITiose sporocysts formed in the sessile di- oocysts, within the host tissues, the sporozoites invade the gestive cells are voided into the lúmen of the gut and expelled blood cells, where they await ingestion by the haema- with the faeces: those in the fixed cells remain in the tick. tophagous invertebrate vector. Within these vectors the Transmission of this extraordinary haemogregarine is sporozoites emerge from the blood cells and penetrate the considered to be affected in a variety of ways. An adult cells of the intestinal epithelium, where they remain quies- toad may become infected after ingesting (a) an infected cent within a . tick, (b) material contaminated by sporocysts voided in the Passive transmission to a new host takes place when faeces of ticks and (r) larval arthropods or small vertebrates the infected vector is eaten, the sporozoites invading the tis• that have ingested the sporocysts. Finally, toads may be• sues and establishing themselves in the intestinal wall come infected at the tadpole (larval) stage, after ingesting sporocysts con- I. S. botivaJU taminating the aquatic environment. Taxonomically Hemolivia is closest to the genus Karyolysis, a haemogregarine of lacertid lizards, and the vectors of which are parasitic Figure 8. ín(rcasin^> involvc- mites (42). Kaiyolysis also produces menf of the intestinal epithe• sporokinetes, but these enter the lium nf liw vertebrate host in foitr species of Schellackia. of the mite where the sporocysts are Possihle evolution of the formed. On hatching, therefore, the "hií>her" coccidia, throw^h a mite larvae carry fully formed sporo• i^enns snch as Ty-zeria. when the developmeni of a resistam cysts containing from 20-30 sporo• oocyst passiny, out with the fae- zoites. This and other differences in ees replaces a non-resisiant their life-cycles clearly separate the one which ruptures in the host genera Kaiyolysis and Hemolivia. and liherates the sporozoites into the hlood; hl = invasion of Based on their observations on hlood cells hy sporozoites in the development of Haemogregarina the lamina própria: ep = intes• Tyzze/Ua up. halli in the leech (34), Siddall & tinal epithelium: fe = feniliza- 8 tion of macro^^ametocxle: Ip = Desser presented powerful arguments lamina própria: In — ;-inl lúmen: to suggest that the above-mentioned mi = microí^ametocytes: no = postsporogonic division of certain non-resistani oocysts: ro = re- sistant iXHvst: sc = schizoi^ony. adeleid haemogregarines in their vec• Rei. 43. tors should be regarded as "mero-

Volume 44(2/3) • March/June 1992 Ciência e Cultura (Journal of the Brazilian Assocíation for ttie Advancement of Science) • 87 ECO 92: Prcftozooíb^iflnTíteAtnazan

Tyzzeria) or (predominantly) one. two, four or many sporocysts, each of which contains one to many sporozoites, again depending on the genus. Trans• mission is by the ingestion of oocysts contaminating the externai environment. The family contains 17 recognized genera, the best known of which are and . In discussing the former, Levine (44) calculated that species of this parasite had been described in a mere 1.2% of the world's , and in only about 5.7% of its mammals. He estimated that if ali the chordates were to be examined, we might expect to fmd 34,000 species of Eimeria and that 3,500 might Figure 9. species of snakes from Amazoniaii Brazil. a) C. be in mammals. The overall estimate of Eimeria spe• pseustesi Lainson et al. from Pseusíes s. sulphureus (Coluhridae): hj C. cies in ali their different hosts could reach the stag- jararacae Carini, from (Viperidaej: cfj C. micruri and C. gering total of about 45,000! Most eimeriids do not constanciae Lainson et al. from Micrurus s. spixii (Elapidae): d.g) C. paraensis and C. carajasensis Lainson et al. from Oxyrhopus petola digitalis harm their hosts, but some do and can (Coluhridae): e) C. epicratesi Lainson et al. from Epicrates c. cenchria cause heavy losses in a variety of domestic animais. (Boidae). Ref 43. Although few infect man (e.g. Isospora and Crypto- sporidium), the advent of AIDS and the frequency of (Schellackia), or endothelial cells of capillaries and the fulminating with these parasites in the immuno- lymphoid- cells of a variety of organs (Lank- suppressed patient has shown that human infection with esterella). Here the parasites undergo schizogony, game- these two coccidia is much more common than we previ- togony and sporogony, producing oocysts which are of a ously supposed. transient nature and soon rupture, within the tissues of the vertebrate host. The released sporozoites invade the blood- The genus Caryospora — This eimeriid parasitizes a vari• stream and once more circulate in the red and/or white ety of predatory snakes, and raptorial birds of the orders blood-cells. (hawks, eagles and vultures) and Strigi- Schellackia species are distinguished by their small formes (). Rare records exist of infection in 2 species oocysts, which contain only 8 naked sporozoites, usually of lizards, a turtle, and a single (9). locahzed in the lamina própria of the intestine. They have In these hosts the parasites undergo the characteristic been described from a variety of hzards and, more rarely, eimeriid schizogony and gametogony within the cells of the in toads. Lankesterella produces larger oocysts containing small intestine, ultimately producing resistant oocysts large numbers of naked sporozoites, localized in various or• which are voided, unsporulated, in the faeces. Sporulation, gans other than the intestine. outside the host, produces a single sporocyst containing 8 Of particular interest among members of the Lank- sporozoites and a variable amount of residuum (Fig. 9). esterellidae studied in the author's laboratory has been Typically, the sporocyst prominent Stieda and sub- Schellackia landauae (43), the life cycle of which (Fig. 7) Stieda bodies at one ex- was studied in the iguanid lizard Polychrus marmoratus. tremity of the sporocyst, In comparing the gametogony and sporogony of some the composite structure species of Schellackia one sees an increasing involvement looking much like a of the intestinal epithelium of the vertebrate host, suggest- "stopper" in a bottle. It is ing a possible evolution of the so-called "higher coccidia" at this point that the 10 (Fig. 8). The genus , for example, also possesses sporozoites emerge when oocysts with 8 naked sporozoites, but these have now de- the oocysts (or liberated veloped a resistam oocyst wall and are expelled into the sporocysts) are ingested lúmen of the intestine, from where they now pass out with by a new host. the faeces. In this way the necessity of a blood-sucking vec• The demonstration of tor has been eliminated, and direct transmission now takes the heteroxenous life-cy- place by the ingestion of oocysts contaminating the envi- cles of both Toxoplasma ronment. and (see be- low), and the virtual re- Family Eímeríídae: , Tyzzeria, striction of Caryospora to Caryospora, Isospora, Eimeria and other genera. predatory snakes and birds, raised the suspicion Figure 10. Isospora species from hirds of Amazonian Brazil. a) I. These coccidia are monoxenous parasites (one host) of ver- that this coccidian, too, albicolis and h) I. tucuruiensis. tebrates and , typically producing resistant might have secondary Lainson & Shaw. 1989. hothfrom oocysts which are voided in the faeces. Depending on the hosts in its life-cycle. It Turdus albicolis (Turdidae). Ref. 5J. genus, these oocysts may contain naked sporozoites (e.g. has now been shown

88 • Ciência e Cultura (Journal of the Brazilian Association for the Advancement of Science) Volume 44(2/3) • March/June 1992 ECO 92: Vrotozootogy In Títe Amazon

the host tissues hefore expulsion in the faeces were clearly Sarco- cystis species (e.g. '"Isospora" higemina of the and the ). Secondly, it was found (50) that after feeding oocysts of I.felis and /. rivolta, from the faeces of , to mice, rats and hamsters, the sporozoites released in the gut made their way, and persisted in, the mesenteric lymph-nodes and other organs. When such tissues were fed to new-born kittens, these subsequently passed oocysts of the two coccidia. It remains likely, therefore, that the life-cy• cle of other species of Isospora Figure 11. Isospora belli Wenyon. 1923 in the dianhoeaic faeces of an AIDS patient. a) may be similarly more compli- Unspoiulaled oocyst: h) Mature oocyst. with sporocysts seen end-on. Original. cated than has been realized (see Figure 12. Eimeria species of chelonids from Amazonian Brazil. a-c) E. lagunculata. E. mammiformis and E. podocnemis Lainson et al, 1990 ali from the river turtle. Podocnemis expansa. , below). d) E. carinii Lainson et al. 1990 from the ("jahoti"). Geochelone denticulata. Ref 54. During our studies in Amazó• nia, one new species of Isospora (45,46,47) that at least some Caiyospora species may un- was described from the "squirrel monkey", Saimiri s. dergo a second cycle of development in the connective tis- sciureus (Primates: Cebidae) and two from the "white- sue of experimentally fed with oocysts. Dormant throated ", Turdus alhicollis (Passeriformes: Turdidae) sporozoites, within "caryocysts" in the tissues of these sec- (51). Ironically, the type locality of the three parasites, the ondary hosts serve as an alternative source of infection for Island of Tocantins, now lays beneath the waters of the res- further snakes or birds. ervoir formed when the new Tucuruí hydroelectric dam Six new species of Caiyospora were recently discov- abrupdy flooded some 2,430 km^ of Amazonian forest. ered by the author (48) in 4 different species of snakes in In conclusion, /. belli (Fig. 11) was isolated from the Pará, bringing the worldwide total of species in reptiles to diarrhoeaic stools of 1 out of 10 AIDS patients examined in 28 (48,49). It is certain that many more species remain to Belém (52). be described among snakes that commonly prey on rodents. What exactly is the host-specificity for these species The genus Eimeria — Species of this extremely common remains doubtful, and cross-infection experiments with coccidian are found in ali classes of vertebrates but very Caiyospora from different genera would give a lot of rarely in invertebrates. Among the latter, 4 species have useful Information. been recorded in the centipedes Mecistocephalus, Himan- tarium, Geophilus and Lithobius (Chilopoda) and 2 in the The genus Isospora — Although the type species, Isospora millipedes Tachypodoiulus and Stigmatogaster (Diplo- rara Schneider, 1881 was described from the slug Limax poda). Doubtful species are registered in the "acom worm", (Mollusca: Gastropoda), no further species have, to the au• Glossobalanus (Hemichordata), the Perichaeta thor's knowledge, been described in invertebrates. On the spp. (Oligochaeta), and of a gyrinid beetle (Cole- other hand, Levine (9) listed 247 species from vertebrates, optera) (9). including amphibia, reptiles, birds and mammals (including To date, only monoxenous life cycles are known for man). This bizarre situation clearly indicates a closer look the genus Eimeria. The parasite usually inhabits the at Limax to substantiate Schneider's rather inadequate de- epithelial cells of the intestine, sometimes the gall bladder scription of /. rara. and bile ducts. Successive cycles of schizogony are fol- Classically the genus Isospora (like Eimeria) has been lowed by gametogony of the typical eimeriid type (Table regarded as an essentially monoxenous coccidian, with 1), and the production of oocysts. Maturation of the oocyst schizogony and gametogony in the intestinal epithelium, to give 4 sporocysts, each containing 2 sporozoites (Fig. and producing oocysts which pass out with the faeces. 12), is usually exogenous and transmission to the new host These mature outside the host, producing an oocyst with 2 depends on the ingestion of mature oocysts. Unlike sporocysts, each of which contains 4 sporozoites (Fig. 10). Isospora, host specificity of Eimeria species is relatively Infection was considered to be acquired solely by the inges- strictly maintained, at least within host genera. tion of the mature oocyst in contaminated food or water. With such a wealth of Eimeria species already re• Following the elucidation of the life-cycle of Sarco- corded in an immense variety of hosts, it was no great sur- cystis (below), the genus Isospora came under closer scru- prise that we were able to record 16 new ones from Amazo• tiny. In the first place, a number of so-called Isospora spe• nian animais; these included the following: cies described as producing oocysts which matured within In snakes — Eimeria micruri, in Micrurus filiformis Volume 44(2/3) • March/June 1992 Ciência e Cultura (Journal of the Brazilian Association for tfie Advancement of Science) • 89 ECO 92: Vrotozooíogy In Tfte Amazon

(Elapidae); E. Uophi. in Liophis cohella and E. leimadophi Sarcocystis, and probably those of , will only in- in Leimadophis poecilogyrus (Colubridae) (53). fect the intermediate hosts and not the definitive hosts.

In chelonids — E. lagunculata. E. mammiformis and The genus Sarcocystis — Typically with elongate E. podocnemis, ali in the river turtle Podocnemis expansa cysts in the skeletal or cardiac muscle: bradyzoites are (Chelonia: Pelomedusidae) (Fig. 12); E. carinii in the tor- elongate. toise Geochelone denticulata (Chelonia: Testudinidae) Our own studies on Sarcocystis have been limited to (54). the description of the following new species, based on the morphology of the sarcocysts in the intermediate hosts: S. In birds — E. vitellini. in the toucan Rhamphastos v. oryzomyos and S. azevedoi, both in the "rice rat", Oiyzomys vitellinus (: Rhamphastidae) (55). capito (Rodentia: Cricetidae); S. proechimyos in the "spiny rat", Proechimys guyannensis (Rodentia: Echimyidae); S. In mammals — E. cyclopei in the "silky anteater", marmosae in the opossum, Marmosa murina (Marsupialia: Cyclopes didactylus; E. corticulata and E. marajoensis in Didelphidae); and S. kinosterni in the tortoise, Kinosternon the "lesser anteater". Tamanduá tetradactyla (: scorpioides (Reptilia: Chelonia) (Fig. 13) (60,61,62). Myrmecophagidae); E. choloepi in the "two-toed sloth". As yet, we have no Information on the definitive hosts Choloepus didactylus (Xenarthra: Bradypodidae); E. of these parasites, but from the observations of other au- philanderi in the "4-eyed opossum", Philander opossum, thors (63,64), it is highly likely that they will prove to be and E. caluromydis in the "wooly opossum", Caluwmys p. snakes, for those of rodents and . That of S. philander (Marsupialia: Didelphidae); E. zygodontomyis in kinosterni is more difficult to suggest, although large the "cane-", Zygodontomys lasiurus (Rodentia: snakes (e.g. Boidae) and crocodiles are quite capable of Cricetidae); and E. thchechi in the manatee, Trichechus preying on small chelonids such as Kinosternon. The author immgids (Sirenia) (51,56-59). has noted the frequent presence of mature sporocysts in the tissues and faeces of the cayman Caiman C. crocodilus, which are suspiciously similar to those of Sarcocystis, and Family Sarcocystidae: subfamilies it is hoped that future transmission experiments will be pos- Sarcocystinae and Toxoplasmatinae sible to elucidate the life cycle of S. kinosterni.

This family contains coccidia of particular medicai and veterinary importance, such as Toxoplasma, Sarcocystis and . Ali members are heteroxenous, with gametogony in the intestinal cells of the definitive host. Resulting oocysts may sporulate outside or inside the host: those maturing inside are usually passed as freed, mature sporocysts. The oocysts contain 2 sporocysts, each con- taining 4 sporozoites. An asexual cycle takes place in in- termediate hosts which have ingested oocysts/sporocysts, with the production of "tissue cysts" containing infective zoites in their muscular organs and/or nervous tissue. Fur- ther definitive hosts become infected when they ingest these tissue cysts.

Subfamily Sarcocystinae: Sarcocystis. Frenkelia, Arthrocystis

The two-host life cycle involves a prey (the intermediate host) and a predator (the definitive host). Asexual multiplication takes place in the intermediate host, with last generation schizonts ("sarcocysts") produc- ing metrocytes ("mother cells") which in tum give rise to large numbers of bradyzoites. These are the infective forms for the definitive host, when it ingests the tissues of its prey. In the definitive host the bradyzoites enter the epithelial cells of the intestine where they develop directly into male and female gametocytes. Fertilization leads to Figure 13. Sarcocystis kinosterni Lainson & Shcnv. 1972 in the tortoise the production of delicate oocysts which mature in the ("miiçuã" I Kinosternon scorpioides. a,hl Histological sections showing tissue cysts ("sarcocysts") in . a) Low power view: h) lamina própria. Here they usually rupture and release the high power riew showing metrocytes (m) giring rise to bradyzoites (hr): sporocysts which pass into the lúmen of the gut and are c.d) Giemsa-stained smears of crushed tissue cyst. showing bradyzoites expelled, fuUy mature, in the faeces. The sporocysts of and a cluster of metrocytes at still higher magnification. Ref. 61.62.

90 • Ciência e Cultura (Journal of the Brazilian Associatíon for ffie Advancement of Science) Volume 44(2/3) . Marcfi/June 1992 ECO 92: Vrotozoohgy In Tfie Amazm

The genus Frenkelia is distin• ed that the coccidial parasites guished from Sarcocystis by its referred to as Isospora felis, I. "sarcocysts" being in the cen• vulpina and /. ohioensis pro- tral nervous system, and by duced tissue cysts, containing their rounded or lobular shape. only one or two zoites, in the Frenkelia induces host-cell nu• tissues of rodents fed with ma• cleus hypertrophy, whereas ture oocysts. It was further Sarcocystis does not. shown that these tissue cysts Arthrocystis has its sar• were infective only to the de• cocysts in striated muscle, like finitive hosts (felids and can- those of Sarcocystis, but they ids), and for this reason Frenkel are peculiarly jointed, like a (66) removed these isosporids piece of bamboo, and the bra• from the genus Isospora and dyzoites are spherical. A para• gave them the new name of site of the Indian jungle fowl, Cystoisospora. its definitive host is as yet un• Levine (9) does not accept known (9). the name, however, and consid- ers it as a synonym of Isospora. Subfamily The arguments in favour of us- Toxoplasmatinae: ing the new names of Ham• Toxoplasma, Besnoitia, mondia and Cystoisospora , seem acceptable enough to the Cystoisospora and present author, who would pre- fer to see their use for the same These parasites undergo schiz- reasons he has given for retain- ogony in the intestine prior to Figure 14. a) Virífin. piimary forest in tlie Carajás liills. Pará. ing the generic names Garnia Brazil: hi Total clestrmiion of primary forest seen in many ár• and Fallisia (page 7). gametogony; the oocysts ma• eas of Pará. Orií>inal. ture outside the host; and the tissue cysts have no The genus Neospora — Dubey metrocytes, only bradyzoites. (The complete life cycle of and co-workers (67) gave this name to a Toxoplasma-Uke Neospora is as yet unknown). parasite producing a fatal disease in , and subsequently found associated with disease of new-born , horses The genus Toxoplasma — Tissue cysts are formed in both and . They differentiated it from Toxoplasma by its the intermediate host and the definitive hosts (Felidae). thicker tissue-cyst wall, slender bradyzoites, larger number They develop in a wide variety of cells, have a thin wall, of in the tachyzoite, and the failure of serum from and have the host outside the cyst. Tachyzoites infected animais to react with Toxoplasma and vice versa. (rapidly dividing asexual stages of the acute phase of infec- The two organisms are best distinguished by the indirect tion), bradyzoites (in the tissue cysts) and sporozoites (in fluorescent antibody and immunoperoxidase tests. The de• the oocysts) are ali infective to the intermediate host and finitive host and sporogonic stages of the parasite are as yet the definitive host. unknown.

The genus Besnoitia — This coccidian differs from Toxoplasma in the following features. The tissue cysts de• Pathogenicity of parasites velop principally in fibroblasts, and only in the intermedi• of the Sarcocystidae ate host; the host cell nucleus is within the tissue cyst and undergoes marked hypertrophy; sporulated oocysts are not The importance of Toxoplasma as a for man and infective to the definitive hosts (Felidae). The infectivity of a wide range of domestic animais (intermediate hosts) is tachyzoites and bradyzoites is variable, according to the well known: that of other members of the family less so. Besnoitia species. Sarcocystis species in the intermediate hosts may be a cause of , poor milk production, weight loss, re- The genus Hammondia — Frenkel & Dubey (65) gave this tarded growth and even death, in a number of different name to a parasite {H. hammondi) producing tissue cysts farm animais. The one species, S. hominis, for which man predominantly in skeletal muscle, rarely the . They is the definitive host may cause him náusea, stomach pains separated it from Toxoplasma mainly because the tissue and diarrhoea. cysts infect only the definitive hosts (Felidae), and the Besnoitia hesnoiti is a serious pathogen of cattle (inter• sporozoites (from oocysts) only the intermediate hosts (ro- mediate hosts) in and Israel, where it is known to dents). Levine (9), however, regards Hammondia as a synonym give rise to fever, hair loss and skin changes, diarrhoea and of Toxoplasma. sometimes death. The genus Cystoisospora — Frenkel and co-workers show- Neospora infection in dogs, sheep, cattle and equines

Volume 44(2/3) . March/June 1992 Ciência e Cultura (Journal of the Brazilian Association for tfie Advancement of Science) • 91 ECO 92: Frotozooíqgy In Tfie Amazon may cause abortion following transplacental transmission, 12. Carini A 1941 Sobre um plasmodio endoglobular e uma eimeria do encephalomyelitis, , and a fatal, generalized in- lagarto Cnemidophorus lemniscatus lemniscatus. Arch Biol São Paulo 25: 205-206 fection similar to acute . 13. Lainson R. JJ Shaw, I Landau 1975 Some blood parasites of the In Belém we have not worked specifically on this group Brazilian lizards Plica umhra and Uranoscodon superciliosa of coccidia, although an isolation of Toxoplasma was made (Iguanidae). 70: 119-141 from the peripheral blood of a febrile patient (68), and it 14. Papema I. I Landau 1990 Billhraya australis n.gen. n.sp. from the South Australian gecko Phyllodactyhis marmoratus. Ann Parasitol was found that domestic pigeons in the city commonly Hum Comp 65: 170-176 harbored tissue cysts of this parasite in the brain (69). 15. Lainson R, JJ Shaw 1969 A new haemosporidian of lizards, Saurocytozoon lupinamhi gen.nov., sp.nov., in Tupinamhus nigropunctatus (Teiidae). Parasitology 59: 159-162 16. Landau I, R Lainson. Y Boulard, JC Michel, JJ Shaw 1973 Concluding remarks Développment chez Culex pipiens de Saurocytozoon tupinamhi (Sporozoaire. Leucocytozoidae). parasite de lézards brésiliens. C R In this brief review I have been able to discuss only some Acad Sei Paris 276: 2449-2452 17. Hsu CK, GR Campbell. ND Levine 1973 A checklist of the species of the protozoological findings made during a very superfi• of the genus Leucocytozoon. J Protozool 20: 195-203 cial examination of Amazonian animais. Control of man's 18. Lainson R. I Landau. JJ Shaw 1974 Observations on non-pigmented devastation in Amazónia permitting (Fig. 14), a great haemosporidia of Brazilian lizards, including a new species of Saurocytozoon in Mahuxa mahouxa (Scincidae). Parasitology 69: number of other parasites clearly remain to be discovered 215-223 and described in the extraordinarily rich fauna of this re- 19. Lainson R, I Landau, JJ Shaw 1974 Further parasites of the family gion, and a vast area of research is indicated to elucidate Garniidae (Coccidiida: Haemosporidiidae) in Brazilian lizards. their life cycles. Fallisia effusa gen.nov.. sp.nov. and Fallisia modesta gen.nov., sp.nov. Parasilology 68: 117-125 It is a sad fact, however, that in this era of dispropor- 20. Boulard Y. I Landau, D Baccam. G Petit. R Lainson 1987 Observa• tionate concentration on the molecular biology of a mere tions ultrastructurales sur les formes sanguines des Garniidés handful of protozoal . support for studies on the {Garnia gonatodi. G. uranoscodoni et Fallisia effusa) parasites de biology, morphology and of the parasitic Proto- lézards Sud-Américains. Europ J Protistol 23: 66-75 21. Telford SR 1973 Saurian malarial parasites from Guyana: their ef- zoa, as a whole, has dwindled alarmingly. To such an ex- fect upon the validity of the family Garniidae and the genus Garnia, tent. indeed, that in the near future we are likely to face an with description of two new species. Int J Parasitol 3: 829-842 acute shortage of protozoologists capable of recognizing 22. Ayala SC 1978 Checklist. host index. and annoted bibliography of them under the . • Plasmodium from reptiles. J Protozool 25: 87-100 23. Telford SR 1988 A contribution to the systematics of the reptilian malária parasites, family Plasmodiidae (Apicomplexa: References and notes Haemosporina). Buli Florida State Mus Biol Sei 34: 65-96 24. Telford SR 1986 Fallisia parasites (Haemosporidia: Plasmodiidae) from the flying lizard. Draco maculatus () in Thailand. J 1. Gamham PCC. AJ Duggan 1986 Catalogue of the Cainham collec- Parasitol 72: 766-769 tion of malaiial parasites and other haemosporidia. William 25. Papema I, I Landau 1990 Fallisia copemani n.sp (Haemosporidia: Clowes Limited, Beccles and London: a Wellcome Trust Publica- Garniidae) from the Australian Carlia rhomhoidalis. Ann tion Parasitol Hum Comp 65: 16-21 2. Lainson R 1977 Trypanosoma cecili n.sp.. a parasite of the South 26. Euzeby J 1989-1990 Protozoologie Médicale Comparée. Vols 3 & American cayman, Caiman crocodilus crocodiliis (Linnaeus, 1758) 4: Collection Fondation Mareei Mérieux. France (Crocodilia: Alligatoridae). In Festschrift in honor of CA. Hoare. 27. Telford SR 1978 Intralymphocytic schizonts associated with an ini- FRS. Protozoology 3: 87-93: a London Scholl of Hygiene & Tropi• tial infection of Saurocytozoon lupinambi in Tupinamhus tegui.vin. cal Medicine publication Int J Parasitol 8: 133-138 3. Levine ND. JO Corliss, FEG Cox. G Deroux. J Grain, BM Honigberg, 28. Gabaldon A, G Ulloa. N Zerpa 1985 Fallisia (Plasmodioides) GF Leedale, AR Loeblich. J Lom. D Lynn. EG Mermfeld. FC Page. neotropicalis subgen. nov., sp.nov.. from Venezuela. Parasitol 90: G Poljansky. V Sprague. J Vavra. FG Wallace 1980 A newly re- 217-225 vised classification of the Protozoa. J Protozool 27: 37-58 29. Deane LM. MP Deane 1961 Sobre dois hemocitozoários 4. Lainson R. I Landau. JJ Shaw 1971 On a new Family of non- encontrados em mamíferos silvestres da Região Amazônica. Rer pigmented parasites in the blood of reptiles: Garniidae fam.nov.. Inst Med Trop São Paulo 3: 107-110 (Coccidiida: Haemosporidiidae). Some species of the new genus 30. Wood SR 1952 blood parasite records from SW United Garnia. Int J Parasitol 1: 241-250 States and México. J Parasitol 38: 85-86 5. Gamham PCC 1966 Malarial parasites and other Haemosporidia. 31. Gamham PCC. R Lainson. JJ Shaw 1971 A contribution to the study Blackwell Scientific Publications. Oxford of the haematozoon parasites of bats. A new mammalian 6. Coatney GR. WE Collins. M Warren. PG Contacos 1971 The pri- haemoproteid. Polychromophilus deanei n.sp. Mem Inst Oswaldo mate matarias. US Government Printing Office. Washington Cruz 69: 119-125 7. Killick-Kendrick R 1978 Taxonomy. zoogeography and evolution, 32. Reichenow E 1910 Haenwgregarina stepanowi. Die p 1-52. In Rodent Malária. R Killick-Kendrick. W Peters, eds. Aca- Entwicklungsgeschichte einer Hâmogregarine. Arch Protistenk 20: demic Press, London/NY 251-350 8. Deane LM. JA Ferreira. M Okumura. MO Ferreira 1969 Malária 33. Lainson R 1981 On Cvri/ío .«omí-í/(Neiva & Pinto. 1926) gen.nov. parasites of Brazilian monkeys. Rer Inst Med Trop São Paulo 11: (Haemogregarinidae) and Trypanosoma hourouli Neiva & Pinto, in 71-86 the fish Synhranchus marmoratus: simultaneous transmission by the 9. Levine N 1988 The protozoan phylum Apicomple.xa Vol II. CRC leech Haemenleria lutzi. In Parasitological Topics. EU Canning, ed. Press. Boca Raton. Florida Society of Protozoologists Special Publication 1: 150-158 10. Aragão HB. A Neiva 1909 A contribution to the study of the 34. Siddall ME. SS Desser 1991 Merogonic development of Haemo- intraglobular parasites of the lizards. Two new species of gregarina halli (Apicomplexa: Adeleina: Haemogregarinidae) in Plasmodium. PI diploglossi. n.sp. and PI. tropiduri, n.sp. Mem Inst the leech Placohdella ornata (Glossiphoniidae). its transmission to a Oswaldo Cruz 1: 44-50 chelonian intermediate host and phylogenetic implications. / 11. Lainson R, JJ Shaw 1969 New host records for Plasmodium Parasitol 11: 426-436 diploglossi. P. tropiduri Aragão and Neiva, 1909. and P. 35. Landau I, JC Michel, AG Chabaud. ER Brygoo 1972 Cycle cnemidophori Carini, 1941. Parasilology 59: 163-170

92 . Ciência e Cultura (Journal of the Brazilian Association for tfie Advancement of Science) Volume 44(2/3) • March/June 1992 ECO 92: Vrotozooío^yln^fie Amazon

biologique ã'Hepatozoon domerguei: discussion sur les caracteres denticulata (Linn) from Amazonian Brazil (Reptilia: Chelonia). fondamentaux d'un cycle de Coccidie. Z Parasitenk 38: 250-270 Mem Inst Oswaldo Cruz 85: 383-390 36. Neiva A, C Pinto 1926 Contribuição para estudo dos hematozoários 55. Lainson R, AM Costa, JJ Shaw 1990 Eimeria Vitellini n.sp. do Brasil. Ann Fac Med São Paulo 1: 79-82 (Apicomplexa; Eimeriidae) from the Brazilian toucan, Rhamphastos 37. Siddall ME 1991 Personal communication vitellinus vitellinus Lichtenstein (Aves: Piciformes: Rhamphastidae). 38. Laveran MA 1906 Sur une hémogregarine de Tanguille. C R Soe Mem Inst Oswaldo Cruz 85: 199-202 Bio/ 60: 457-458 56. Lainson R, JJ Shaw 1982 Coccidia of Brazilian edentates: Eimeria 39. Leger A, M Legar 1920 Hémogregarine d'un poisson marin, cyc/opei n.sp. from the silky anteater, Cyclopes didactylus (Linn) (Diagramma mediterraneum). C R Soe Biol 83: 1275-1277 and Eimeria choloepi n.sp. from the two-toed sloth, Choloepus 40. Papema I 1989 Developmental cycle of chelonian haemogregarines didactylus (Linn). Syst Parasitol 4: 269-278 in leeches with extra-intestinal multiple sporozoite oocysts and a 57. Lainson R, JJ Shaw 1990 Coccidia of Brazilian mammals: Eimeria note on the blood stages in the chelonian hosts. Dis Aquat Oig 7: corticulata n.sp. (Apicomplexa: Eimeriidae) from the anteater 149-153 Tamanduá tetradactyla (Xenarthra; Myrmecophagidae) and 41. Petit G, I Landau, D Baccam. R Lainson 1990 Description et cycle Eimeria zygodontomyis n.sp. from the cane mouse Zygodontomys biologique d'HemoIivia stellara n.g., n.sp., hémogregarine de lasiurus (Rodentia: Cricatidaa). / Protozool 37: 51-54 crapauds brésiliens. Ann Parasito! Hum Comp 65: 3-15 58. Lainson R, JJ Shaw 1991 Coccidia of Brazilian mammals: Eimeria 42. Reichenow E 1921 Die Hâmococcidien der Eidechsen. marajoensis n.sp. (Apicomplexa: Eimeriidae) from the anteater. Vorbemerkungen und I. Theil. Die Entwicklungsgeschichte von Tamanduá tetradactxla (Xenarthra: Myrmecophagidae). / Pro• . Arch Protistenk 42: 179-291 tozool 38: 28-30 43. Lainson R, JJ Shaw, RD Ward 1976 Schellackia landauae sp.nov. 59. Lainson R, RD Naiff, RC Best, JJ Shaw 1983 Eimeria trichechi nsp. (: Lankesterellidae) in the Brazilian lizard Polychrus from the Amazonian manatee, Trichechus inunguis (Mammalia: marmoratus (Iguanidae): experimental transmission by Culex Sirenia). Syst Parasitol 5: 287-289 pipiens fatigans. Parasitology 72: 225-243 60. Shaw JJ, R Lainson 1969 Sarcocystis of rodents and marsupials in 44. Levine ND 1973 Introduction, history, and taxonomy, p 1-22. In Brazil. Parasitology 59: 233-244' The Coceidia. DM Hammond, PL Long, eds. University Park Press, 61. Lainson R, JJ Shaw 1971 Sa;rocw;5 ^?raf/7/i n.sp. from the Brazil• Butterworths, Baltimore London ian tortoise Kinosternon scorpioides. J Protozool 18: 365-372 45. Cawthorn RJ, PHG Stockdale 1982 The developmental cycle of 62. Lainson R, JJ Shaw 1972 Sarcocystis in tortoises: a replacement Caryospora hubonis Cawthorn and Stockdale 1981 (Protozoa: name, Sarcocystis kinosterni, for the homonym Sarcocystis gracilis Eimeriidae) in the great horned , Bubo rirginianus (Gmelin). Lainson & Shaw, 1971. / Protozool 19: 212 CanJZool 60: 152-157 63. Rzepczyk CM 1974 Evidence of a rat-snake life cycle for 46. Wacha RS, JL Christiansen 1982 Development of Caryospora Sarcocystis. Int J Parasitol 4: 447-449 bigenetiea n.sp. (Apicomplexa: Eimeriidae) in rattlesnakes and 64. Matuschka F-R 1986 Sarcocystis clethrionomyelaphis n.sp. from laboratory mice. / Protozool 29: lll-XTi snakes of the genus Elaphe and different voles of the Family 47. Upton SJ, WL Current, JV Ernst, SM Bamard 1984 Extraintestinal Arvicolidae. / Parasitol 72: 226-231 development of Caryospora simplex (Apicomplexa: Eimeriidae) in 65. Frenkel JK, JP Dubey 1975 Hammondia hammondi gen.nov., experimentally infected mice. Mus musculus. J Protozool 31: 392- sp.nov., from domestic cats, a new coccidian related to Toxoplasma 398 and Sarcocystis. Zeitschrift Parasitenk 46: 3-12 48. Lainson R, FP Nascimento, JJ Shaw 1991 Some new species of 66. Frenkel JK 1977 Besnoitia wallacei of cats and rodents: with a re- Caryospora (Apicomplexa: Eimeriidae) from Brazilian snakes, and classification of other cyst-forming isosporid coccidia. J Parasitol a re-description of C. jararacae Carini, 1939. Mem Inst Oswaldo 63: 611-628 Cruz 86: 349-364 67. Dubey JP, JL Carpenter, CA Speer, MJ Topper, A Uggla 1988 49. Upton SJ, PS Freed. MG Freed 1989 Two new species of coccidia Newly recognized fatal protozoan disease of dogs. / Am Vet Med (Apicomplexa: Eimeriorina) from Peruvian reptiles. Trans Am Assoe 192: 1269-1285 Mierosc Soe 108: 96-100 68. Noura F, R Lainson, JJ Shaw 1968 Toxoplasmose em Belém, Pará, 50. Frenkel JK, JP Dubey 1972 Rodents as vectors for felina coccidia, Brasil: isolamento de Toxoplasma do sangue periférico de paciente Isospora felis and Isospora rivolta. J Infect Dis 125: 69-72 febril. Rev Serv Espec Saúde Públ 14: 39-45 51. Lainson R, JJ Shaw 1989 Two new species of f/mér/a and three 69. Lainson R 1968 Unpublished observations new species of Isospora (Apicomplexa: Eimeriidae) from Brazilian 70. Acknowledgements. The author owes an immense debt of gratitude to mammals and birds. Buli Mus Natn Hist Nat Paris 11: 349-365 the Wellcome Trust, London who have financed his studies over 52. Lainson R 1990 Unpublished observations such a long period, and to a succession of Directors of the Instituto 53. Lainson R, JJ Shaw 1973 Coccidia of Brazilian snakes: Isospora Evandro Chagas who have given unstinted support. Professor PCC deeipiens. Eimeria micruri, E. liophi and £. leimadophi spp.n., with Gamham has remained a constant and unwavering source of inspi- redescriptions of Caryospora hrasiliensis Carini, 1932 and Eimeria ration and encouragement throughout. I am grateful to the editors poecilogyri Carini, 1933. / Protozool 20: 358-362 and publishers of the following journals and text-books, who al- 54. Lainson R. AM Costa, JJ Shaw 1990 £/mena species (Apicomplexa: lowed me to reproduce previously published illustrations: Blackwell Eimeriidae) of Podoenemis expansa (Schweigger) and Geoehelone Scientific Publications. Oxford; Bulletin du Muséum National

Volume 44(2/3) • March/June 1992 Ciência e Cultura (Journal of the Brazilian Association for the Advancement of Science) • 93