Rev. Inst. Med. top. São Paulo UDC 616.936 23(l) :12-17, ianeiro-fevereiro, l98I

MALARIA INFECTION IN ANOLIS LIZARDS ON MARTINIQUE. LESSER ANTITLES

Stephen C. AYALA (1) and Paul E HERTZ (2)

SUMMARY

Plasmodia (Protozoa: Haemosporidiidae) identified as Plasmodium azurophilum Telford 1975 were found in 11 of 89 Anolis roquet from Martinique in the southern Lesser Antilles. Ten lizards frorn intermediate elevations had parâsites in their ery- throcytes, whereas the single infected lizard from a higher elevation rain forest site had parasites only in its leucocytes. Two parasite species could be involved: a garnia-group (pigmentless) plasmodium in the erythrocytes, and a fallisia-group (leu- cocyte invading) species. If this is the case, then a fallisia-group species is widespre- ad in the Caribbean region as part of the P. azurophilum complex. Otherwise, if looth stages are part of a single species, the fallisia-group species from other regions in the Neotropios might be expected to show erythrocyte phases at some stage of their life cycle.

INTRODUCTION

Some workers on malaria in South and Cen- western Caribbean islands 1,2,e (Table I). \Me tral American reptiles have preferred to retain report here the finding of P. azurophilum in all the 39 currenfly accepted Neotropical para- anoles of a completely different phylogenetic site species in the single genus Plasmodium 1.2, and geographic origin Anolis roquet on the while others have proposed using several differ- island of Martinique (FiSs.- 1-3). This finding ent genera: Plasmodium only for pigmented considerably extends the known distribution of plasmodia using erythrocytes as host cells; Gar- malaria in rffest Indean reptiles, and raises se- nia for non-pigmented parasites in erythrocy- verâl'questiöns about its systematics, origin and tes; and Fallisia for plasmodia found in leuco- dispersal. cyte host cells ó,7. The description of Plasmo- dium azurophilum in anole lizards on the Grea- MATERIALS AND METHODS ter Antilles Islands, inhabiting both erythrocy- (PEH) tes and leucocytes e is an obstacle to those In July 1.975, one of us collected se- prefering to use the second alternative. Our veral series of A. roquet as part of a study of geographical 4. observation on apparently the same parasite in its variation and local adaptation Methanol-fixed prepared the Southern Lesser Antilles do not solve the blood smears were fro.m lizards problem, but they help to bring it into clearer from four sites in northern Marti- focus. nique (Fig. 3): Morne Calebasse (650 meters elevation, elfin rain forest), Petíte Savane (500 Plasmodium azurophilum Telford 1g?5 and m, roadside vegetation), Habitation Eden (350 P. floridense Thompson & Huff 1944 have been m, banana grove) and Habitation Ajoupa (175 found infecting Anolis lizards on several of the m, loanana grove). Animals from the three

(1) Microbiology Ðept., Universidad de1 Vall.e Medical School; and Tulane University International Center for Medical Re- search; Apartado .A.éreo 5390. Cali, COLOMBIA (2) Museum of Comparative Zoolory, Harvard University, Cambridge. Present ad.dress: Dept. of Biological Sclences. Barnard College, Columbia University. New york 1002?, U.S.A.

T2

AYALA, S. C. & HERTZ, P. E. - Malaria infection in Anolis lizards on Martinique, Lesser Antilles. Rev, Insú. Med. trop. São Paulo 23:12-U, 1981.

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Fig. 2 - Plâsmodium azurophilm: known dis- tribution of infections in anole lizards of the caribbean islands (shaded). The dotted tine abo- ve Maftinique indicates the northern limit of fhe distribution of the roquet species group of South American origin, ând the southern limit of the bimæulatus species group of anoles de- rived from populations on the GÌeater Antiltes. Fig. 3 - Collection sites for Anolis roqueú on Martinique: Morne Calebasse (6b0 méters eleva- tion), Petíte Savane (500 m), Habitation Eden (350 m), and Habitation Ajoupa (U5 m). LE LORRAI NE

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cocytes were found during more than 20 hours modium) modesúum and to other leucocyte- of searching the blood smears of 10 different inhabiting plasmodia on the South American infected lizards. mainland 6,7.

Plasmodia in the single infected anole from DISCUSSION Morne Calebasse inhabited a wide variety of mononuclear and polymorphonuclear leucocytes. The malarial parasite from Greater Antiltes The infection apparently stimulated a marked anoles named Plasmodium azurophilum by TEL- production of these cell types, since they were FORD e thus also infects anoles on Martinique. far more numerous than is normally the case The picture is complicated by the virtually com- in peripheral blood. Despite â seârch of more plete separation of erythrocyte and leucocyte than 10 hours. not a single infected erythrocyte forms in different lizards, although Telforcl \ryas found, although leucocytes harboring all noted this same situation for the other anole stages. of the para,site were seen about once in hosts. In fact, were it not for Telford's thorough every 5 to 10 consecutive 1000 X microscope description, our plasmodia would unhesitatingly fields, and multiply-infected leucocytes were have been identified as two distinct species: a common. These parasites appear identical to pigmentless (garnia group) species inhabiting those described as the leucocyte phase of P. azlu- erythrocytes, and a leucocyte-inhabiting (falli. rophilum in anoles of Hi,spaniola and Jamaicae. sia group) species similar to those known from They are also very similar to Fallisia (:Plas- several Brazilian lizards6,7. t4

AYALA, S. Ç. & H'E,PúTZ, P. E. Malaria infection in Ànolis lizards Mart¡n¡que, Lesser 'Rev. - on Antilles. Inst. Med. úrop. São Paulo 23:12-17,1981.

Additional material must be studied to test geographic origins2,11,12. It occurs in anoles of Telford's belief that P. azurophilum is not ac- both the South American-derived alpha lineage tually a composite species. If it turns out that (4. roquet, A. cybotes, A..krugi), and the Meso two distinct parasites are involved, then a falli- American-derived beta lineage (4. grahami, A. sia group species similar to those known from lineatopus)., Perhaps it can infect almost ar¡y northeastern Brazil is widespread in the Carib- anole population living in regions suitable for bean region. the insect vector species. A careful reading of the P. azurophilum des- Infected lizards sureþ carry their parasites cription suggests that two distinct species could with then when they colonize new islands. The be involved. The total number of naturally in- bimaculatus species group of anoles living on fected lizards with plasmodia in their leucocy- the northern lêsset Antilles (St. Croix south tes was small: three A. lineaúopus from Jamai- through Dominica) are in fact derived from ca and five A. cybotes from Haiti (Table I). No- stocks on Puerto Rico in the Greater Antilles s, ne were found in the single infections in A, gra- where P. azurophilum is known .to occur. hami and A. krugi. In addition, they were found However, A. roquet and all the other anole spe- in two experimentally infected A. cybotes: the cies on the islands. south of Martinique. are de- hosî ceil type(s) in the first doner was not rived from a differenL stock.of colonists from stated, but in the second case there were no the adjacent South Amerióah mainland s. Thus, plasmodia found in the erythrocytes of the the presence of P, azurophilum on Martinique donor host, and only leucocyte stages developed can not be enplained by a simple southward in the recipient.' dispersal of infected lizards from the Greater Antilles, unless it was brought in and establish- fn on the other hand, P. azurophilum does ed bimaculaúus group lizards whose own effort prove to be a species capable of infecting 'single at colonization later failed tt. both white and red blood cells at different. as yet undescribed phases of its life cycle, then If P. azurophilum is truly a unique species we should probably look for similar "erythrocy- of Caribbean origin, it may be that a represen- te phases" at some stâge of the infection cycle tative of the bimaculatus species group did once of the other fallisia group species. inhabit Martinique, from which it was later displaced by A. roquet, while leaving behind a A remarkable proliferation of host leucocy. malarial infection period tes as a consequence of plasmodial infection as a reminder of the of encounter. Nevertheless, factors has been seen on other occasions with leuco- two other need also be probable cyte-invadlng parasites. TELFORDe noted it in considered: 1) the ease with which (including malaria-infected one of his two experimentally infected A. cybo- flies DÍptêra) be wind-dispersed between is- úes-, and we (Ayala & Guerrero, unpublished) ',rnight' Iands, and 2) the effect animal sa'w,':Aj sithilar'reaction in an A. frenaúus from on dispersal of the much increased central Panama carrying an undescribed plas- size of the island banks (and hence, reduced distance between islands) modia in its leucocytes. Whatever the mecha- as recently as 15,000 years ago Pleis- nism, the result is a striking increase in the during the tocene sea appropriate host cells. level lowerings. Two other circumstances suggest further roquet is a widespread ecological ge- ^Anolis study A. roquet neralist, the only anole on the island of Marti- of and its infections on Marti- nique would be worthwhile. Phlebotomine nique. It has differentiated into six recogniza- If sandflies 1, ble subspecies 'which tend to occupy different are involved as insect vectors the situation climatic habitats on the islands. HERTZ¿ iden- could be convenient to study, since these insects are not generally tified physiological differences between the abundant on the Caribbean islands only a different subespecies. Anolis roquet summus, - single species having the form in which been reported so far from Martinique, and it we found the infections, (V/ILLIAMS occurs continuously throughout apparently feeds on reptiles & the mountains 13, COELHO and other reports . of northern Martinique in dense rain forest and cited thereinl in disturbed habitats. Finally, Anolis roquet on Martinique is also the only reported lizard host of Leishmania (,,Leish- Plasmodium azurophilum, like P. floriden- mania henrici") in New World reptiles ¡. This se, infects anoles of quite different genetic and report has never been followed up, although it

16 AYAI,A, S. C. & HERTZ, P. E. Mala¡ia infection in Anotis lizatds on Martinique, Lesser Antilles. Rev. Inst. Med.. trop. São Paulo 23:12-l?,1981. -

now seems li,keþ that these parasites, assuming REFERENCES that they were really Trypanosomatids, were 1. AY'ALA, S. C. ptasmodia of pâlæiúic probably monoxenous flagellates from ingested - Reptiles. In Protozoa. J. p. Kreier, ed. New york, Academic press, insects rather than true Leishmania. 3: 26?-309, 19??. 2. ÂYALA, S. C. - Checklist, host index, and annotated RESUMEN biblio$aphy of plasmodium in reptiles. J. protozool. 25: 87-100, 19?8. Infección malárica en saurios del genero Anolis 3. GORMAN, c. & ATKINS, L. - The zoogeography of en la isla Martinique, Antillas menores. Lesse¡ Antillian Anolis lizards _ an arìalysis based upon chtomosomes and lâctic dehydrogenases. Bull, Museum Comparative Zool. (Harvard. En 11 de 89 Anolis University) l3g: roquet de la isla antillâ- 53-80, 1969. na de Martinique, fueron encontrados parási- 4. HERTZ, P. E. Altitudinal tos maláricos identificados como Plasmodium - vâtiation in thermoregula_ tory strategies, physiological ecolog.y, and azurophilum Telford 1975. Diez lagartos captu- morphology ot some West Indian anoles. lDoctoral d.issertation], rados a 350 y 500 metros de elevación presen- Harvard University, 19?2, 290 pp. taron plasmodios en sus glóbulos rojos, mien- 5. LAINSON, R,.; LANDAU, I. & SIIAW, _ positivo J. J. Further tras el único animal encontrado a 650 parasites of the fa"rnity Garniidae. Coccidiida: HaÆmos- metros en selva montano.pluvial tenía parásitos poridüdae) in Btazilian lizards. Fallisia effusa gen. abundantes pero exclusivamente en los leuco- nov., sp. nov.,. and Fâllisia modesta gen. nov., sp. nov. Paræitology 68: 11?-125, 19?4. citos. Es posible que se trate de dos especies distintas de plasmodios: una eue infecta eritro- 6. LAINSON, R,.; SHAW, J. J. A¿ LANDAU, r. _ Some citos sin producir pigmento malárico (del gru- blood parasites of the Brazilian lizards püca umbra ând par¿sitology po y que Untanosodon supetciliosa. ?0: 119-141, "garnia"), la otra reside en leucocitos 19?6. (del grupo "fallisia"). En este caso, un plasmo- 7. LAZELI,, ,t. (Sauria: dio representante del grupo fallisia se encuentra - The anoles Iguânidae) of the Lesser Antilles. Bull. Museum ámpliamente distribuido en islas del Caribe, Comparaúive z¡ool, (:H:ar- co. vard University) 148: 1-11b, l9?2. nocido hasta ahora como "la fase leucocitaria" de P. azurophilum. Si por eI contrario las dos 8. LEGER,, M. Infection sanguine par Leptomonas chez un saurien. - formas son realmente C. R. Séanc Soc. Biol. (pads) 81: ??2-??4. fases de una sola espe- 1918. cie que infecta ambos tipos de células, enton- 9. TELFORD, S. ces debemos buscar en las otras especies del R. - Saurian malaria in the Caribbean: grupo fallisia para Plasmodium azüophilum, sp. nov., a malarial parasite averiguar si ellas tambien with schizogony and gametogony in both presentan red and. white formas eritrocÍticas en alguna fase blood cells. Inú, J. parasitol. 5: 388,894, 19?5. de su ciclo normal. 10. ROGIER, E. & LANDAU, I. Description - de Schelra_ ckia golvani, n. sp (Lankesterellidae), parasite de lé_ zards ACKNOWLEDGEMEN'fS de Guadeloupe. Bull. Museum NaúI. Hist. Naú. (Paris) (Zoologie) 194: 9t-9?, 19?5. lf . WILLIAMS, E. E. We thank P.G. Haneline, A.S. Rand and Fan- - The ecology of co{onizâtion as seen in the zoogeography of anoline ny Carvajal for preparing, requesting and tran6- lizards on small islânds. Quart, Rev, Biol. 44: 345.889, 1969. porting, and preliminary stu{y of the blood sli- 12. WILLIAMS,. E. des. The work was made possible by grants E. - West Indian anoles: a taxonomic and evolutionary summary. I Introduction from the National Science Foundation (GB - and spe. cies list. Breviora, Museum Comp¿rative Zool. (Harvard 3?731X to Dr. Ernest E. Ivilliams and DEB University) 440: 1-21, 19?6. 75-16334 to P.E. Hertz), the Richmond and An- 13. WILLIAMS, P. & COELHO, M. de V. Taxonomv and derson Funds of Harvard University and the Ex- - transmission of Leishmania. Adv. parasitol. 16r L-42, plorer's Club of New York (to p.E. Hertz), and 1979. the U.S. Public Health Service (NIH AI-12511 ro S.C. A5tala). Recebido para publicação em 29/4/I9gO

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