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Revista Pan-Amazônica de Saúde

versión On-line ISSN 2176-6223

Rev Pan-Amaz Saude vol.10  Ananindeua  2019  Epub 09-Dic-2019

http://dx.doi.org/10.5123/s2176-6223201900375 

HISTORICAL ARTICLE

Opening doors: a review of the Protozoa and Insecta taxa published under Wellcome Trust funding at Instituto Evandro Chagas, Belém, Pará State, Brazil

Abrindo portas: uma revisão dos táxons de Protozoa e Insecta publicados, sob o financiamento da Welcome Trust, no Instituto Evandro Chagas, Belém, Pará, Brasil

Jeffrey Jon Shaw (orcid: 0000-0002-7008-1972)1 

1Universidade de São Paulo, Departamento de Parasitologia, São Paulo, São Paulo, Brasil

ABSTRACT

Wellcome Trust and Instituto Evandro Chagas (IEC) joined research efforts during more than 40 years, and many publications have been made about the scientific contributions with the content of this partnership. The aim of the present historical article is to list the new species of Protozoa and Insecta that were named during the presence of Welcome Trust funding at IEC and to briefly mention how their discovery influenced future research and to show how they relate to present trends in the different areas. The result was a total of 119 new species named in conjunction with their hosts and authors, and five that were transferred (comb. nov.); Ralph Lainson authored/co-authored 108, Jeffrey Shaw 60 new species, 56 by Lainson and Shaw, and seven by other colleague authors. Most of the species were discovered in Brazil. The description of these new species has provided a clearer understanding of the taxonomic groups to which they belong and how some are transmitted to man with their resultant pathologies and treatments. And many scientific doors were opened showing the variety of protozoal parasites in Amazonian vertebrates.

Keywords: Protozoa; Parasites; Insecta; Parasite-Host Relation; Taxonomy

RESUMO

A Wellcome Trust e o Instituto Evandro Chagas (IEC) aliaram esforços pela pesquisa durante mais de 40 anos, e muitas publicações foram feitas sobre as contribuições científicas resultantes dessa parceria. O objetivo deste artigo histórico é listar as novas espécies de Protozoa e Insecta que foram nomeadas durante a presença do financiamento da Wellcome Trust no IEC, e mencionar resumidamente como a descoberta das mesmas influenciou futuras pesquisas e mostrar como se relacionam com as atuais tendências nas diferentes áreas. O resultado foram 119 novas espécies nomeadas juntamente com seus autores e hospedeiros e cinco que foram transferidas (comb. nov.); Ralph Lainson foi autor/coautor de 108, Jeffrey Shaw, de 60, Lainson e Shaw, de 56, e outros autores colegas, de sete. A maioria das espécies foram descobertas no Brasil. A descrição dessas novas espécies proporcionou uma compreensão mais clara dos grupos taxonômicos aos quais elas pertencem e como algumas são transmitidas ao homem com suas patologias e tratamentos resultantes. E muitas portas científicas foram abertas, mostrando a variedade de parasitas protozoários nos vertebrados da Amazônia.

Palavras-chave: Protozoa; Parasitos; Insecta; Interações Hospedeiro-Parasita; Taxonomia

INTRODUCTION

An article1 on Wellcome Trust funded research at Instituto Evandro Chagas, in Pará State, Brazil, did not give details of the new organisms that were discovered. A total of 119 new species were named and, due to taxonomic revisions, five species named previously by other authors were transferred (comb. nov.) to newly created genera. These taxa are listed in table 1 together with their hosts and authors. The aim of the present article is to briefly mention how their discovery influenced future research and to show how they relate to present trends in the different areas.

Ralph Lainson was supported for the longest period and his contributions were dominant, being an author/co-author of 108 new species and five new combinations. Jeffrey Shaw authored/co-authored 60 new species and two new combinations. One hundred and one of these new species were discovered in Brazil and two names were given to Leishmania found in Panama. The descriptions of 13 published individually by Ralph Lainson (10) and Jeffrey Shaw (three) were of material that they had collected while respectively working in Belize and Central America.

SPECIES OF PROTOZOA

PROTOZOA: EUCOCCIDIIDA & MICROSPORIDIA

The taxonomic ranks (family, genus, and subgenus) that were created for some of the species are not listed in table 1 and are as follows: the haemosporidian genus Saurocytozoon Lainson & Shaw, 19692 ; the haemosporidian family Garnidae Lainson, Landau & Shaw, 19713 containing the genera Garnia Lainson, Landau & Shaw, 1971, Fallisia Lainson, Landau & Shaw, 19744, and Progarnia Lainson, 19955; two hemogregarine genera Cyrilia Lainson, 19816 and Hemolivia Petit, Landau, Baccam & Lainson, 19907; and the microsporidian genus Alloglugea Paperna & Lainson, 19958. A simple question is why were they found? All are from cold-blooded vertebrates and the majority is from lizards. While searching for lizard Leishmania that to this date have never been found in the Americas, a wealth of parasites was discovered in different blood cells, opening new research areas. However, besides this, it was obvious that an enormous number of parasites was waiting to be discovered. Thus, any available animal was examined for parasites, irrespective of it being a potential reservoir of a human disease.

Their discoveries stimulated others to look for them around the world. Garnia is only known in the Western Hemisphere; Fallisia species have been recorded in the Americas, South East Asia, and Australasia; and Saurocytozoon occurs in both North and South America and in Asia9. Molecular methods are now showing possible evolutionary pathways that reflect the above distributions. The 60 Eimeridae species listed in table 1 were found in either warm or cold blooded vertebrates. A recent paper10 showed that species of Cyclospora, Eimeria, and Isospora from warm blooded vertebrates form a well-supported clade, but organisms identified as Eimeria or Isospora species from cold-blooded vertebrates and marsupials do not fall within this group, suggesting that these are polyphyletic genera. For example, based on 18S rRNA sequences10, two Eimeria species, one from a snake and the other from an anuran, were phylogenetically closer to European Schellackia species within the family Schellackiidae. These observations clearly indicate that future revisions will be required to resolve the polyphyletic genera.

Six species of Sarcocystis were described based on distinctive cyst wall morphology. Except for one, their definitive hosts are unknown. The sexual cycle of Sarcocystis ameivamastigodryasi Lainson & Paperna, 200011 of the teiid lizard, Ameiva ameiva occurs in the intestine of the colubrid snake, Mastigodryas bifossatus. The oocysts are like those of Isospora species having two sporocysts that contain four sporozoites. In the case of the teiid parasite, the oocyst wall ruptures inside the snake's intestine so mature sporocysts are liberated in the faeces. The cystic stage normally occurs in herbivores and the sexual stage in carnivores ranging from canids, corvid birds to snakes. It is possible that some Isospora species could in fact be Sarcocystis species.

PROTOZOA: KINETOPLASTIDA

Given the medical importance of Leishmania species, it is not surprising that the most well-known taxa and taxonomic rank, established in Belém, Pará State, under Wellcome Trust funding, belong to this genus. The creation of the subgenus Leishmania (Viannia) Lainson & Shaw, 198712 was a fundamental step forward in understanding the disease known as leishmaniasis and its phylogeny. Parasites belonging to this subgenus are only found in the Americas, while those of the subgenus Leishmania (Leishmania) are found in the Old World and the Americas. Three previously named organisms, L. braziliensis, L. guyanensis, and L. peruviana were assigned to this subgenus and eight other species were described (Table 1). All but two of these belong to the subgenus L. (Viannia). One of these, L. (L.) amazonensis Lainson & Shaw, 197213, grows profusely in culture and readily infects a range of laboratory animals, producing in hamsters a pathology like diffuse cutaneous leishmaniasis. Because of these attributes this parasite is used extensively in immunological and chemotherapeutic studies. Molecular methods14 have shown that the subgenus L. (Viannia) separated from the basal stock some 80 MYA while the subgenus L. (Leishmania) separation was later being around 50 MYA. There are distinct differences between the immunological response and pathology of the two subgenera in man. Somewhere along the evolutionary line, the subgenus L. (Leishmania) seems to have opted to depress the cell mediated response, while the subgenus L. (Viannia) opted to stimulate it. Perhaps this was due to the very different mammalian hosts in which the two subgenera evolved, one possible being rodents and the other Xenarthra. Today we see this reflected in the extreme immunological differences between diffuse cutaneous leishmaniasis caused by L. (L.) amazonensis and mucocutaneous by L. (V.) braziliensis15.

Leishmania hertigi deanei Lainson & Shaw 197716, later raised to specific status by Lainson and Shaw12 in 1987, is very different from all other Leishmania. The amastigotes are very large and do not appear to be intracellular. Latterly studies have shown that it is phylogenetically outside the genus Leishmania being closer to Endotrypanum. This led to the creation of the genus Porcisia Shaw, Camargo & Teixeira 201617 to accommodate it and the Panamanian porcupine parasite, P. hertigi.

Great advances in our understanding of the taxonomy of Trypanosoma (Schizotrypanum) cruzi were made by Miles et al.18 while working at the Instituto Evandro Chagas that confirmed three genetically distinct lineages that were denoted as Type I, II & III. In the opinion of the author these represent distinct species but have never been named so they do not appear in table 1. Subsequently these lineages have been shown to be distinct by with different molecular markers.

Table 1 - Taxa described under funding of the Wellcome Trust by Ralph Lainson, Jeffrey Shaw and their colleagues while working at the Instituto Evandro Chagas, Belém, Pará, Brazil 

Protozoa Host
Eucoccidiida: Haemosporida: Plasmodiidae
Plasmodium vacuolatum Lainson, Shaw & Landau, 1975 Lizard
Plasmodium neusticuri Lainson & Paperna, 1996 Lizard
Plasmodium kentropyxi Lainson, Landau & Paperna, 2001 Lizard
Plasmodium carmelinoi Lainson, Franco & Matta, 2010 Lizard
Eucoccidiida: Haemosporida: Leucocytozoidae
Saurocytozoan tupinambi Lainson & Shaw, 1969 Lizard
Saurocytozoan mabuyi Lainson, Landau & Shaw, 1974 Lizard
Eucoccidiida: Haemosporida: Haemoproteidae
Polychromophilus deanei Garnham, Lainson & Shaw, 1971 Bat
Haemoproteus peltocephali Lainson & Naiff, 1998 Lizard
Haemoproteus geochelonis Lainson & Naiff, 1998 Lizard
Eucoccidiida: Haemosporida: Garniidae
Garnia gonatodi (Telford, 1970) Lainson, Landau & Shaw, 197l, comb. nov. Lizard
Garnia telfordi Lainson, Landau & Shaw, 1971 Lizard
Garnia utingensis Lainson, Landau & Shaw, 1971 Lizard
Garnia multiformis Lainson, Shaw & Landau, 1975 Lizard
Garnia uranoscodoni Lainson, Shaw & Landau, 1975 Lizard
Garnia morula (Telford, 1970) Lainson, Landau & Shaw, 1971, comb. nov. Lizard
Garnia karyolytica Lainson & Naiff, 1999 Lizard
Fallisia effusa Lainson, Landau & Shaw, 1974 Lizard
Fallisia modesta Lainson, Landau & Shaw, 1974 Lizard
Fallisia audaciosa Lainson, Shaw & Landau, 1975 Lizard
Fallisia simplex Lainson, Shaw & Landau, 1975 Lizard
Progarnia archosauriae Lainson, 1995 Lizard
Eucoccidiida: Adeleina: Haemogregarinidae
Cyrilia lignieresi (Laveran, 1906) Lainson, l992, comb. nov. (Syns Haemogregarina lignieresi Laveran, 1906; H. gomesi Neiva & Pinto, 1926; Cyrilia gomesi Lainson, 1981) Fish
Hemolivia stellata Petit, Landau, Baccam & Lainson, 1990 Anuran
Eucoccidiida: Eimeriina: Lankesterellidae
Lankesterella petiti Lainson & Paperna, 1995 Anuran
Eucoccidiida: Eimeriina: Schellackiidae
Schellackia landauae Lainson, Shaw & Ward, 1976 Lizard
Eucoccidiida: Eimeriina: Eimeridae
Tyzzeria boae Lainson & Paperna, 1994 Snake
Cyclospora niniae Lainson, 1965 Snake
Cyclospora schneideri Lainson, 2005 Snake
Caryospora pseustesi Lainson, Nascimento & Shaw, 1991 Snake
Caryospora micruri Lainson, Nascimento & Shaw, 1991 Snake
Caryospora constanciae Lainson, Nascimento & Shaw, 1991 Snake
Caryospora paraensis Lainson, Nascimento & Shaw, 1991 Snake
Caryospora carajasensis Lainson, Nascimento & Shaw, 1991 Snake
Caryospora epicratesi Lainson, Nascimento & Shaw, 1991 Snake
Isospora albicolis Lainson & Shaw, 1989 Bird
Isospora wilkiei Lainson, 1968 Crocodile
Isospora basilisci Lainson, 1968 Lizard
Isospora tucuruiensis Lainson & Shaw, 1989 Bird
Protozoa Host
Isospora saimiri Lainson & Shaw, 1989 Mammal
Isospora cacici Lainson, 1994 Bird
Isospora thraupis Lainson, 1994 Bird
Isospora capanemaensis Lainson, 2003 Mammal
Isospora rodriguesae Lainson, Da Silva, Franco & De Souza, 2008 Chelonia
Eimeria orthogeomyos Lainson, 1968 Mammal
Eimeria tamanduae Lainson, 1968 Mammal
Eimeria rhynchonycteridis Lainson, 1968 Mammal
Eimeria pseudemydis Lainson, 1968 Turtle
Eimeria bothrops Lainson, 1968 Snake
Eimeria ameivae Lainson, 1968 Lizard
Eimeria crocodyli Lainson, 1968 Crocodile
Eimeria poti Lainson, 1968 Mammal
Eimeria micruri Lainson & Shaw, 1973 Snake
Eimeria liophi Lainson & Shaw, 1973 Snake
Eimeria leimadophi Lainson & Shaw, 1973 Snake
Eimeria cyclopei Lainson & Shaw, 1982 Mammal
Eimeria choloepi Lainson & Shaw, 1982 Mammal
Eimeria trichechi Lainson, Naiff, Best & Shaw, 1983 Mammal
Eimeria philanderi Lainson & Shaw, 1989 Mammal
Eimeria caluromydis Lainson & Shaw, 1989 Mammal
Eimeria vitellini Lainson, Costa & Shaw, 1990 Bird
Eimeria corticulata Lainson & Shaw, 1990 Mammal
Eimeria zygodontomyis Lainson & Shaw, 1990 Mammal
Eimeria lagunculata Lainson, Costa & Shaw, 1990 Chelonia
Eimeria mammiformis Lainson, Costa & Shaw, 1990 Chelonia
Eimeria podocnemis Lainson, Costa & Shaw, 1990 Chelonia
Eimeria carinii Lainson, Costa & Shaw, 1990 Chelonia
Eimeria marajoensis Lainson & Shaw, 1991 Mammal
Eimeria porphyrulae Lainson, 1994 Bird
Eimeria crypturelli Lainson, 1994 Bird
Eimeria bufomarini Paperna & Lainson, 1995 Anuran
Eimeria peltocephali Lainson & Naiff, 1998 Turtle
Eimeria molossi Lainson & Naiff, 1998 Bat
Eimeria bragancaensis Lainson & Naiff, 2000 Bat
Eimeria carmelinoi Lainson, 2002 Lizard
Eimeria damnosa Lainson, Brigido & Silveira, 2005 Mammal
Eimeria lepidosirenis Lainson & Ribeiro, 2006 Fish
Eimeria amazonensis Lainson, Da Silva, Franco & De Souza, 2008 Chelonia
Eimeria carbonaria Lainson, Da Silva, Franco, & De Souza, 2008 Chelonia
Eimeria carajasensis Lainson, Da Silva, Franco & De Souza, 2008 Chelonia
Eimeria wellcomei Lainson, Da Silva, Franco & De Souza, 2008 Chelonia
Acroeimeria paraensis Lainson, 2002 Lizard
Acroeimeria cnemidophori (Carini, 1941) Lainson, 2002, comb. nov. Mammal
Choleoeimeria rochalima (Carini & Pinto, 1926) Lainson & Paperna, 1999, comb. nov. Lizard
Choleoeimeria carinii Lainson & Paperna, 1999 Lizard
Choleoeimeria amphisbaenae Lainson, 2003 Lizard
Eucoccidiida: Eimeriina: Sarcocystidae
Sarcocystis kinosterni Lainson & Shaw, 1972 Mammal
Sarcocystis azevedoi Shaw & Lainson, 1969 Mammal
Sarcocystis marmosae Shaw & Lainson, 1969 Mammal
Sarcocystis oryzomyos Shaw & Lainson, 1969 Mammal
Sarcocystis proechimyos Shaw & Lainson 1969 Mammal
Sarcocystis ameivamastigodryasi Lainson & Paperna, 2000 Lizard/Snake
Protozoa Host
Piroplasmida: Theileriidae
Theileria electrophori Lainson, 2007 Fish
Microspora: Glugeidae
Alloglugea bufonis Paperna & Lainson, 1995 Anuran
Kinetoplastida: Trypanosomatidae
Endotrypanum monterogeii Shaw, 1969 Mammal
Leishmania (Leishmania) amazonensis Lainson & Shaw, 1972 Mammal*
Leishmania (Viannia) panamensis Lainson & Shaw, 1972 Mammal*
Leishmania (Leishmania) aristidesi Lainson & Shaw, 1979 Mammal
Leishmania (Viannia) lainsoni Silveira, Shaw, Braga & Ishikawa, 1987 Mammal*
Leishmania (Viannia) naiffi Lainson & Shaw, 1989 Mammal*
Leishmania (Viannia) shawi Lainson, Braga, de Souza, Póvoa & Ishikawa, 1989 Mammal*
Leishmania (Viannia) lindenbergi Silveira, Ishikawa, de Souza & Lainson, 2002 Mammal*
Leishmania (Viannia) utingensis Braga, Lainson, Ishikawa & Shaw, 2003 Mammal
Porcisia deanei (Lainson & Shaw, 1977) Espinosa et al., 2018 Mammal
Trypanosoma leuwenhoeki Shaw, 1969 Mammal
Trypanosoma preguici Shaw, 1969 Mammal
Trypanosoma plicae Lainson, Shaw & Landau, 1975 Lizard
Trypanosoma cecili Lainson, 1977 Crocodile
Trypanosoma (Megatrypanum) saloboense Lainson, Da Silva & Franco, 2008 Mammal
Insecta
Diptera: Psychodidae: Phlebotominae
Bruptomyia orlandoi Fraiha, Shaw & Lainson, 1970
Psychodopygus wellcomei Fraiha, Shaw & Lainson, 1971
Psychodopygus lainsoni Fraiha & Ward, 1974
Nyssomyia umbratilis (Ward & Fraiha, 1977) Galati, 2003
Psychodopygus llanosmartinsi Fraiha & Ward, 1980
Nyssomyia shawi (Fraiha, Ward & Ready, 1981) Galati, 2003
Nyssomyia richardwardi (Ready & Fraiha, 1981) Galati, 2003
Trichopygomyia ratcliffei (Arias, Ready & Freitas, 1983) Galati, 2003
Psychodopygus leonidasdeanei Fraiha, Ryan, Ward, Lainson & Shaw, 1986
Evandromyia carmelinoi (Ryan, Fraiha, Lainson & Shaw, 1986) Galati, 2003
Trichopygomyia readyi (Ryan, 1986) Galati, 2003

* Infections found in man; † Found infected with Leishmania (Viannia) braziliensis; ‡ Found infected with Leishmania (Viannia) guyanensis.

SPECIES OF INSECTS

INSECTA: DIPTERA: PSYCHODIDAE: PHLEBOTOMINAE

Unravelling the epidemiologies of the different Leishmania species inevitable led to the discovery of new phlebotomine species. It also showed how the epidemiological importance of different groups varies in different biomes. The discovery of Psychodopygus wellcomei Fraiha, Shaw & Lainson 197119 was the first indication of the vectorial importance of this genus for L. (Viannia) species in Amazonia. Six Psychodopygus species are associated with L. (V.) braziliensis and five with L. (V.) naiffi20. It is the predominant genus in south of the Amazon River extending to virgin Atlantic rain forest. In north of the river, L. (V.) guyanensis, transmitted by N. umbratilis, is the dominant leishmania in man. The number of Nyssomyia sand flies is significantly greater in this biome, but there is no significant difference in the variety of species of Nyssomyia and Psychodopygus21.

Continuous environmental variations related to global warming and man's activities modulate the sand fly fauna. Understanding and documenting this is the challenge.

CONCLUSION

Unforeseen benefits have resulted from the description of the species that form the subject of this paper. They range from a clearer understanding of the taxonomic groups to which they belong to how some are transmitted to man with resultant contrasting pathologies and treatments. For example, in 1965 it was accepted that Leishmania braziliensis was the etiological agent of all forms of cutaneous leishmaniasis in Brazil. Studies of the parasites from wild animals, man and sand flies showed that this was wrong. Many scientific doors were opened, giving just a glimpse to the amazing variety of protozoal parasites that occur in Amazonian vertebrates.

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How to cite this article / Como citar este artigo: Shaw JJ. Opening doors: a review of the Protozoa and Insecta taxa published under Wellcome Trust funding at Instituto Evandro Chagas, Belém, Pará State, Brazil. Rev Pan Amaz Saude. 2019;10:e201900375. Doi: http://dx.doi.org/10.5123/S2176-6223201900375

Recibido: 24 de Junio de 2019; Aprobado: 12 de Agosto de 2019

Correspondence / Correspondência: Jeffrey Jon Shaw Universidade de São Paulo, Departamento de Parasitologia Av. Professor Lineu Prestes, 1374. Bairro: Butantã. CEP: 05508-000 - São Paulo, São Paulo, Brasil E-mail: jayusp@hotmail.com

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