Abstract
Nyssomyia umbratilis (Ward & Frahia) is the main vector of Leishmania guyanensis in the Brazilian Amazon region, where it is widely distributed. Studies have hypothesized that this phlebotomine is part of a cryptic species complex, spatially delimited by the Amazonian river systems, and with different transmission potential of L. guyanensis. In the present study, the immature stages of N. umbratilis are described from laboratory-reared specimens originating from the states of Amazonas and Pará, Brazil. Based on scanning electron and optical microscopy examinations, fine morphological structures (eggshell, setae, and mouthparts of larvae and pupae) are presented. A new form of sandfly pupae sexing (non-invasive) is also provided. The correct identification of insect is extremely important for the epidemiology of certain diseases. However, only the morphological characters of adult can be insufficient to separate accurately the closely related species. It is expected that the present description may contribute to solve the taxonomic problem involving N. umbratilis.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abonnenc E (1956) L’oeuf et les formes pré-imaginales de deux Phlébotomes africains: P. antennatus var. occidentalis Theodor, 1933 et P. dubius Parrot, Mornet et Cadenat, 1945. Arch Institut Pasteur d’Algérie 34:518–539
Alencar RB, Barrett TV, Scarpassa VM (2016) Immature stages and larval chaetotaxy of Notofairchildia stenygros (Quate & Alexander) (Diptera: Psychodidae: Bruchomyiinae). Zootaxa 4169(3):457–474. https://doi.org/10.11646/zootaxa.4169.3.3
Arrivillaga J, Navarro JC, Feliciangeli MD (1999) Morfologia y quetotaxia del tagma cefálico larval de Lutzomyia França, 1924 (Diptera: Psychodidae): Proposición de um sistema de nomeclatura. Bol Entomol Venezol 14:1–13
Arias JR, Freitas RA (1977) On the vectors of cutaneous leishmaniasis in the Central Amazon of Brazil. I. Preliminary findings. Acta Amazon 7(2):293–294. https://doi.org/10.1590/1809-43921977072293
Arias JR, Freitas RA (1978) Sobre os vetores de leishmaniose cutânea na Amazônia Central do Brasil. 2: Incidência de flagelados em flebótomos selváticos. Acta Amazon 8(3):387–396. https://doi.org/10.1590/1809-43921978083387
Arias JR, Naiff RD, Miles MS, Sousa AA (1981) The opossum Didelphis marsupialis (Marsupiala Didelphisae) as a reservoir host of Leishmania braziliensis guyanensis in the Amazon basin of Brazil. Trans R Soc Trop Med Hyg 75(4):537–541. https://doi.org/10.1016/0035-9203(81)90194-2
Balbino VQ, Marcondes CB, Alexander B, Luna LKS, Lucena MMM, Mendes ACS, Andrade PP (2001) First report of Lutzomyia (Nyssomyia) umbratilis Ward & Fraiha, 1977 outside of Amazonian region, in Recife, state of Pernambuco, Brazil (Diptera: Psychodidae: Phlebotominae). Mem Inst Oswaldo Cruz 96(3):315–317. https://doi.org/10.1590/S0074-02762001000300005
Bahia AC, Secundino NFC, Miranda JC, Prates DB, Souza APA, Fernandes FF, Barral A, Pimenta PFP (2007) Ultrastructural comparison of external morphology of immature stages of Lutzomyia (Nyssomyia) intermedia and Lutzomyia (Nyssomyia) whitmani (Diptera: Psychodidae), vectors of cutaneous leishmaniasis, by scanning electron microscopy. J Med Entomol 44(6):903–914. https://doi.org/10.1093/jmedent/44.6.903
Brazil BG, Brazil RP (2000) Sexing sand fly pupae (Diptera: Psychodidade: Phlebotominae). Mem Inst Oswaldo Cruz 95(4):471–472. https://doi.org/10.1590/S0074-02762000000400004
Barretto MP (1941) Morfologia dos ovos, larvas e pupas de alguns Flebotomus de São Paulo. Anais da Faculdade de Medicina da Universidade de São Paulo 17:357–427
Carzola D, Oviedo M (2001) Quetotaxia del IV estádio larval de Lutzomyia (Nyssomyia) hernandezi (Diptera: Psychodidae, Phlebotominae). Rev Colomb Entomol 27:153–158
Dujardin JP, Le Pont P, Baylac M (2003) Geographical versus interspecific differentiation of sand flies (Diptera: Psychodidae): a landmark data analysis. B Entomol Res 93:87–90
Emden FI (1957) The taxonomic significance of the characters of immature insects. Annu Rev Entomol 2(1):91–106. https://doi.org/10.1146/annurev.en.02.010157.000515
Endris RG, Young DG, Perkins PV (1987) Ultrastructural comparison of egg surface morphology of five Lutzomyia species (Diptera: Psychodidae). J Med Entomol 24(4):412–415. https://doi.org/10.1093/jmedent/24.4.412
Fausto AM, Maroli M, Mazzini M (1992) Ootaxonomy and eggshell structure of Phlebotomus sandflies. Med Vet Entomol 6(3):201–208. https://doi.org/10.1111/j.1365-2915.1992.tb00607.x
Fausto AM, Feliciangeli MD, Maroli M, Mazzini M (1998) Morphological study of the larval spiracular system in eight Lutzomyia species (Diptera: Psychodidae). Mem Inst Oswaldo Cruz 93(1):71–79. https://doi.org/10.1590/S0074-02761998000100014
Fausto AM, Taddei AR, Mazzini M, Maroli M (1999) Morphology and ultrastructure of spiracles in phlebotomine sanfly larvae. Med Vet Entomol 13(1):101–109. https://doi.org/10.1046/j.1365-2915.1999.00146.x
Fausto AM, Feliciangeli MD, Maroli M, Mazzini M (2001) Ootaxonomic investigation of five Lutzomyia species (Diptera: Psychodidae) from Venezuela. Mem Inst Oswaldo Cruz 96(2):197–204. https://doi.org/10.1590/S0074-02762001000200011
Feliciangeli MD, Castejon OC, Limongi J (1993) Egg surface ultrastructure of eight new world phlebotomine sand flies species (Diptera: Psychodidae). J Med Entomol 30(4):651–656. https://doi.org/10.1093/jmedent/30.4.651
Forattini OP (1973) Entomologia Médica. IV. Psychodidae. Phlebotominae. Leishmanioses. Bartonelose. Ed. Edgar Blucher, São Paulo, p 658
Galati E (2016) Phlebotominae (Diptera, Psychodidae) Classificação, Morfologia, Terminologia e Identificação de Adultos. Apostila. Bioecologia e Identificação de Phlebotominae, vol 1. Universidade de São Paulo, São Paulo, p 131
Ghosh KN, Mukhopadhyay J (1996) A comparison of chorionic sculpturing of four Indian phlebotomine sandiflies (Diptera: Psychodidae) by scanning electronic microscopy. Parasite 3(1):61–67. https://doi.org/10.1051/parasite/1996031061
Hanson WJ (1968) The immature stages of the subfamily Phlebotominae in Panama (Diptera: Psychodidae). PhD. Thesis, Faculty of the Graduate School of the University of Kansas, USA, p 104
Harbach RE, Knight KL (1980) Taxonomists' glossary of mosquito anatomy. Plexus publishing. Inc. Marlton, New Jersey, p 415
Justiniano SCB, Chagas AC, Pessoa FAC, Queiroz RG (2004) Comparative biology of two populations of Lutzomyia umbratilis (Diptera: Psychodidae) of Central Amazonia, Brazil, under laboratory conditions. Braz J Biol 64(2):227–235. https://doi.org/10.1590/S1519-69842004000200007
Killick-Kendrick R, Leaney AJ, Ready PD (1977) The establishment, maintenance and productivity of a laboratory colony of Lutzomyia longipalpis (Diptera: Psychodidae). J Med Entomol 13(4-5):429–440. https://doi.org/10.1093/jmedent/13.4-5.429
Killick-Kendrick M, Killick-Kendrick R (1991) The initial establishment of sandfly colonies. Parassitologia 33:315–320
Lainson R, Shaw JJ, Ward RD, Ready PD, Naiff RD (1979) Leishmaniasis in Brazil: XIII. Isolation of Leishmania from armadillos (Dasypus novemcinctus) and observations on the epidemiology of cutaneous leishmaniasis in north Pará state. Trans Roy Soc Trop Med Hygiene 73(2):239–242. https://doi.org/10.1016/0035-9203(79)90225-6
Lainson R, Shaw JJ, Ready PD, Miles MA, Povoa M (1981) Leishmaniasis in Brazil: XVI. Isolation and identification of Leishmania species from sandflies, wild mammals and man in north Para state, with particular reference to L. braziliensisguyanensis causative agent of “pian-bois”. Trans R Soc Trop Med Hyg 75(4):530–536
Lainson R (1988) Ecological interactions in the transmission of the leishmaniasis. Philos Trans R Soc Lond Serie B 321(1207):389–404. https://doi.org/10.1098/rstb.1988.0099
Leite RAC, Williams P (1996) The first instar larval of Lutzomyia longipalpis (Diptera: Phlebotominae). Mem Inst Oswaldo Cruz 92:197–203
Lane RP, Sawaf B (1986) The immature stage of Phlebotomus langeroni (Diptera: Psychodidae). J Med Entomol 23(3):263–268. https://doi.org/10.1093/jmedent/23.3.263
Ma N, Cai L, Hua B (2009) Comparative morphology of the eggs in some Panorpidae (Mecoptera) and their systematic implication. Syst Biodivers 7(4):403–417. https://doi.org/10.1017/S1477200009990107
Marcondes CB, Santos-Neto LG, Lozovei AL (2001) Ecology of phlebotomine sandflies (Diptera, Psychodidae) in Brazilian Atlantic Forest. Rev Soc Bras Med Trop 34(3):255–260. https://doi.org/10.1590/S0037-86822001000300005
Mukhopadhyay J, Ghosh K (2000) Morphology of larval antennae and mouthparts of four Indian sand flies (Diptera: Psychodidae) by scanning electrón microscopy. Entomol Soc Am 37:575–580
Oca-Aguilar ACM, Rebollar-Téllez E, Ibáñez-Bernal S (2014) Descriptions of the immature stages of Dampfomyia (Coromyia) beltrani (Vargas & Díaz-Nájera) (Diptera: Psychodidae), with notes on morphology and chaetotaxy nomenclature. Zootaxa 3887(3):251–297. https://doi.org/10.11646/zootaxa.3887.3.1
Oca-Aguilar ACM, Rebollar-Téllez E, Ibáñez-Bernal S (2016) The immature stages of Micropygomyia (Coquillettimyia) chiapanensis (Dampf) (Diptera: Psychodidae, Phlebotominae). Zootaxa 4105(5):455–482. https://doi.org/10.11646/zootaxa.4105.5.3
Pessoa FAC, Queiroz RG, Ward RD (2000) Posterior spiracles of fourth instar larvae of four species of phlebotomine sand flies (Diptera: Psychodidae) under scanning electron microscopy. Mem Inst Oswaldo Cruz 95(5):689–691. https://doi.org/10.1590/S0074-02762000000500013
Pessoa FAC, Feitosa MAC, Bermudez EGC, Ríos-Velásquez CM, Ward RD (2008) Immature stages two species of Evandromyia (Aldamyia) and the systematic importance of larval mouthparts within Psychodidae (Diptera, Phlebotominae, Psychodinae). Zootaxa 1740:1–14
Pérez EJ, Ogusuku E (1997) Chorion patterns on eggs of Lutzomyia sandflies from the Peruvian Andes. Med Vet Entomol 11(2):127–133. https://doi.org/10.1111/j.1365-2915.1997.tb00301.x
Le Pont F, Pajot FX (1980) La leishmaniose em Guyane Française. 1. Étude de l'écologie et du taux d'infection naturelle de Lutzomyia (Nyssomyia) umbratilis Ward et Fraiha, 1977 em saison seche. Considérations épidémiologiques. Cahiers ORSTOM, Série Ent Méd et Parasitologie 18:359–382
Pajot FX, Le Pont F, Gentile B, Besnard R (1982) Epidemiology of leishmaniasis in French Guiana. Trans Roy Soc Trop Med Hygiene 76(1):112–113. https://doi.org/10.1016/0035-9203(82)90033-5
Rotureau B (2006) Ecology of the Leishmania species in the guianan ecoregion complex. Am J Trop Med Hyg 74(1):81–96
Satchell GH (1953) On the early stages of Bruchomyia argentina Alexander (Diptera: Psychodidae). Proceedings of the Royal Entomological Society of London, Series A 28:1–5
Scarpassa VM, Alencar RB (2012) Lutzomyia umbratilis, the main vector of Leishmania guyanensis, represents a novel species complex? PLoS One 7(5):e37341. https://doi.org/10.1371/journal.pone.0037341
Scarpassa VM, Alencar RB (2013) Molecular taxonomy of the two Leishmania vectors Lutzomyia umbratilis and Lutzomyia anduzei (Diptera: Psychodidae) from the Brazilian Amazon. Parasit Vectors 6(1):258. https://doi.org/10.1186/1756-3305-6-258
Schaper S, Hernández-Chavarría F (2006) Scanning electron microscopy of the four larval instars of the dengue fever vector Aedes aegypti (Diptera: Culicidae). Rev Biol Trop 54(3):847–852
Stork NE (1980) A scanning electron microscope study of tarsal adhesive setae in the Coleoptera. Zool J Linnean Soc 68(3):173–306. https://doi.org/10.1111/j.1096-3642.1980.tb01121.x
Trouillet J (1979) Sergentomyia (Rondanomyia) ingrami Newstead, 1914, Sergentomyia (Rondanomyia) dureni Parrot, 1934 et Sergentomyia hamoni Abonnenc, 1958. Annales de Parasitologie 54(3):353–373. https://doi.org/10.1051/parasite/1979543353
Young DG, Duncan MA (1994) Guide of the identification and geographic distribution of Lutzomyia sand flies in Mexico, the West Indies, Central and South America (Diptera: Psychodidae). Memoirs of the American Entomological Institute 54:1–881
Ward RD (1976a) A revised numerical chaetotaxy for neotropical phlebotomine sandfly larvae (Diptera: Psychodidae). Syst Entomol 1(1):89–94. https://doi.org/10.1111/j.1365-3113.1976.tb00035.x
Ward RD (1976b) The immature stages of some phlebotomine sandflies from Brazil (Diptera: Psychodidae). Syst Entomol 1(3):227–240. https://doi.org/10.1111/j.1365-3113.1976.tb00043.x
Ward RD, Fraiha H (1977) Lutzomyia umbratilis, a new species of sand fly from Brazil (Diptera: Psychodidae). J Med Entomol 14(3):313–317. https://doi.org/10.1093/jmedent/14.3.313
Ward RD, Ready P (1975) Chorionic sculpturing of some sandfly eggs (Diptera: Psychodidae). J Ent A 50:127–134
Zimmerman JH, Newson HD, Hooper GR, Christensen HA (1977) A comparison of the egg surface structure of six antropophilic phlebotomine sand flies (Lutzomyia) with the scanning electron microscope (Diptera: Psychodidae). J Med Entomol 13(4-5):574–579. https://doi.org/10.1093/jmedent/13.4-5.574
Acknowledgments
We offer our deepest thanks to the Instituto Nacional de Pesquisas da Amazônia that provided technical support for the development and implementation of this study; to Mr. Wilson Meirelles and Mr. Jaqueline from Laboratório Temático de Microscopia at Instituto Nacional de Pesquisas da Amazônia (INPA), in Manaus, Brazil; and to Dr. José Antônio Picanço Diniz Júnior from Instituto Evandro Chagas, in Belém, Brazil, for allowing the use of the scanning electron microscope.
Funding
This study was funded by the MCTIC/INPA, by the National Council of Scientific and Technological Development (CNPq) grants, process numbers 409058/2006-8 to Toby Vincent Barrett and 575482/2008-7 to Vera Margarete Scarpassa, by the Foundation of Research Support of the State of Amazonas (FAPEAM), process numbers 1501/2008 and 3111/2012 to Vera Margarete Scarpassa.
Author information
Authors and Affiliations
Corresponding author
Additional information
Edited by Andre VL Freitas – Unicamp
Rights and permissions
About this article
Cite this article
Alencar, R.B., Justiniano, S.C.B. & Scarpassa, V.M. Morphological Description of the Immature Stages of Nyssomyia umbratilis (Ward & Frahia) (Diptera: Psychodidae: Phlebotominae), the Main Vector of Leishmania guyanensis Floch (Kinetoplastida: Trypanosomatidae) in the Brazilian Amazon Region. Neotrop Entomol 47, 668–680 (2018). https://doi.org/10.1007/s13744-018-0587-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13744-018-0587-6