Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2017-05-02
Page range: 477–489
Abstract views: 65
PDF downloaded: 1

Morphology variation of Lutzomyia cruciata eggs (Diptera: Psychodidae: Phlebotominae) in southern Mexico

Instituto de Ecología, A.C., Red Ambiente y Sustentabilidad. Carretera Antigua a Coatepec No. 351, El Haya, CP 91070, Xalapa, Veracruz, México.
El Colegio de la Frontera Sur (ECOSUR), Carretera Antiguo Aeropuerto km 2.5, Tapachula, 30700, Chiapas, México.
El Colegio de la Frontera Sur (ECOSUR), Carretera Antiguo Aeropuerto km 2.5, Tapachula, 30700, Chiapas, México.
Universidad Autónoma de Nuevo León, Facultad de Ciencias Biológicas, Departamento de Zoología de Invertebrados, Laboratorio de Entomología Médica, Ave. Universidad s/n, Apartado Postal 109–F, Ciudad Universitaria, San Nicolás de los Garza, 66451 Nuevo León, México.
The Ohio State University, Ohio Agriculture Research and Development Center 1680 Madison Avenue, 224 Thorne Hall, Wooster OH 44691, Ohio, EEUU.
Instituto de Ecología, A.C., Red Ambiente y Sustentabilidad. Carretera Antigua a Coatepec No. 351, El Haya, CP 91070, Xalapa, Veracruz, México.
intraspecific variation Neotropical region Chiapas Yucatán Veracruz exochorion sculpture pattern Diptera

Abstract

The sand fly Lutzomyia cruciata has been associated with the transmission of Leishmania mexicana to humans in Mexico. This species has a wide distribution in Mexico occupying different microhabitats and environments. In this work comparisons of the egg exochorion of Lu. cruciata from different physiographic areas are presented. Study sites are from different states of southern Mexico. Exochorion analysis was carried out using scanning electron microscopy (SEM). Results show differences in the exochorionic pattern among samples from Veracruz (AVER), Yucatán (HOYU) and Chiapas (TACH). The morphotype “Chiapas” has a polygonal crest pattern, the morphotype “Veracruz” shows parallel and longitudinal crests with some or few connections, and the morphotype “Yucatán” has weak connections between crest ridges. These morphological differences could be the result of local adaptations or evidence of divergence within the nominal unit Lutzomyia cruciata.

References

  1. Alexander, J.B. (1987) Dispersal of phlebotomine sand flies (Diptera: Psychodidae) in a Colombian coffee plantation. Journal of Medical Entomology, 24, 552–558.

    https://doi.org/10.1093/jmedent/24.5.552

    Arrivillaga, J. & Feliciangeli, M.D. (2000) Diferenciación morfológica larval entre poblaciones de Lutzomyia longipalpis (Lutz and Neiva 1912) en Venezuela (Diptera: Psychodidae). Boletín de Entomología Venezolana, 15, 229–234.

    Baiatone, A.R., Barret, T.V. & Scarpassa, V.M. (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

    Barretto, M.P. (1941) Morfologia dos ovos, larvas e pupas de alguns flebótomos de São Paulo. Anais da Faculdade do Medicina da Universidade do São Paulo, 17, 356–427.

    Barth, R. & Muth, H. (1958) Estudos anatômicos e histológicos sobre a subfamília Triatominae (Heteroptera, Reduviidae). VIII parte: Observações sobre a superfície dos ovos das espécies mais importantes. Memorias do Instituto Oswaldo Cruz, 56, 197–208.
    https://doi.org/10.1590/S0074-02761958000100010

    Beament, J.W.L. (1946) The formation and structure of the chorion of the egg in an Hemipteran, Rhodnius prolixus Stål Quart. Quarterly Journal of Microscopical Science, 87, 393–439.

    Cárdenas, E., Munstermann, L.E., Martinez, O., Corredor, D. & Ferro, C. (2001) Genetic variability among populations of Lutzomyia (Psathyromyia) shannoni (Dyar 1929) (Diptera: Psychodidae: Phlebotominae) in Colombia. Memorias do Instituto Oswaldo Cruz, 96, 189–196.

    https://doi.org/10.1590/S0074-02762001000200010

    Castillo, A., Serrano, A.K., Mikery, O.F. & Pérez, J. (2015) Life history of the sand fly vector Lutzomyia cruciata in laboratory conditions. Medical and Veterinary Entomology, 29, 393–402.
    https://doi.org/10.1111/mve.12127

    Chapman, R.F (1998) The insects: structure and function. Cambrige University Press, New York, 959 pp.

    Clements, A.N. (1963) The physiology of mosquitoes. The MacMillan Company, New York, 393 pp.

    Cohnstaedt, L.W., Beati, L., Caceres, A.G., Ferro, C. & Munstermann, L.E. (2011) Phylogenetics of the Phlebotomine sandfly group Verrucarum (Diptera: Psychodidae: Lutzomyia). American Journal of Tropical Medicine and Hygiene, 86, 913–922.
    https://doi.org/10.4269/ajtmh.2011.11-0040

    Cohnstaedt, L.W., Beati, L., Caceres, A.G., Ferro, C. & Munstermann, L.E. (2012) The population structure of Lutzomyia verrucarum (Diptera: Psychodidae), a Bartonella bacilliformis and Leishmania peruviana vector in Peru. Journal of Medical Entomology, 49, 77–84.
    https://doi.org/10.1603/ME11013

    De Almeida, N., Oliveira, R.S., Brazil, B.G. & Soares, M.J. (2004) Pattern of exochorion ornaments on eggs of seven South American species of Lutzomyia sand flies (Diptera: Psychodidae). Journal of Medical Entomology, 41, 819–825.
    https://doi.org/10.1603/0022-2585-41.5.819

    Emmons, L. (1984) Geographic variation in densities and diversities of non-flying mammals in Amazonia. Biotropica, 16, 210−222.
    https://doi.org/10.2307/2388054

    Endris, R.G., Young, D.G. & Perkins, P.V. (1987) Ultrastructure comparison of eggs surface morphology of five Lutzomyia species (Diptera; Psychodidae). Journal of Medical Entomology, 24, 412–415.
    https://doi.org/10.1093/jmedent/24.4.412

    Fausto, A.M., Feliciangeli, M.D., Maroli, M. & Mazzini, M. (2001) Ootaxonomy investigation of five Lutzomyia species (Diptera, Psychodidae) from Venezuela. Memorias do Instituto Oswaldo Cruz, 96, 197–204.
    https://doi.org/10.1590/S0074-02762001000200011

    Feliciangeli, M.D., Castejon, O.C. & Limongi, J. (1993) Egg surface ultrastructure of eight new world phlebotomine sand fly species (Diptera: Psychodidae). Journal of Medical Entomology, 30, 651–656.
    https://doi.org/10.1093/jmedent/30.4.651

    Flores, J.S. & Espejel, I. (1994) Vegetación de la Península de Yucatán. Etnoflora Yucatanense. Fascículo 3. Universidad Autónoma de Yucatán, Mérida, Yucatán, 135 pp.

    Florin, A.D. & Rebollar-Téllez, E.A. (2013) Divergence of Lutzomyia (Psathyromyia) shannoni (Diptera: Psychodidae: Phlebotominae) is indicated by morphometric and molecular analyses when examined between taxa from the southeastern United States and Southern Mexico. Journal of Medical Entomology, 50, 1324–1329.
    https://doi.org/10.1603/ME13085

    Galati, B.A.E. (1995) Phylogenetic systematics of Phlebotominae (Diptera, Psychodidae) with emphasis on American groups. Boletín de Malariología y Saneamiento, 1 (Supplement), 133–142.

    Galati, B.A.E. (2003) Morfologia, Terminologia de adultos e identificação dos Táxons da América. In: Rangel, E. & Lainson, R. (Eds.), Flebotomíneos do Brasil. Ed. Fiocruz, Rio de Janeiro, pp. 23–175.

    García, E. (2004) Modificaciones al Sistema de Clasificación Climática de Köppen. 5ª Edition. Serie de Libros No. 6. Instituto de Geografía, Universidad Nacional Autónoma de México, México City, 90 pp.

    Ghosh, K.N. & Battacharya, A. (1993) A comparison of light microscopic and scanning electron microscopic study on the chorionic sculpturing of sandfly (Phlebotomus argentipes) eggs. Memorias do Instituto Oswaldo Cruz, 88, 355–337.
    https://doi.org/10.1590/S0074-02761993000200026

    Ghosh, K.N. & Mukophadyay, J. (1996) A comparison of chorionic sculpturing of four Indian Phlebotomine sandflies (Diptera: Psychodidae) by scanning electron microscopy. Parasite, 3, 61–67.
    https://doi.org/10.1051/parasite/1996031061

    Gould, S.J. & Johnston, R.F. (1972) Geographic variation. Annual Review of Ecology, Evolution, and Systematics, 3, 457−499.
    https://doi.org/10.1146/annurev.es.03.110172.002325

    Hamarsheh, O., Presber, W.Z., Abdeen, A.L., Salwalhans, G. & Schonion, S. (2007) Genetic structure of Mediterranean populations of the sand fly Phlebotomus papatasi by mitochondrial cytochrome b haplotype analysis. Medical and Veterinary Entomology, 21, 270–277.
    https://doi.org/10.1111/j.1365-2915.2007.00695.x

    INEGI (1988) Carta de vegetación y uso del suelo. Escala 1:1,000,000. Instituto Nacional de Estadística, Geografía e Informática, México City. [map]

    INEGI (1989) Carta climática. Escala 1:1,000,000. Instituto Nacional de Estadística, Geografía e Informática, México City. [map]

    Ibáñez-Bernal, S. (1999) Phlebotominae (Diptera: Psychodidae) de México. I.- Brumptomyia França y Parrot; Lutzomyia França, las especies de L. (Lutzomyia) França y del grupo Verrucarum. Folia Entomológica Mexicana, 107, 61–116.

    Ibáñez-Bernal, S. (2000) Los Phlebotominae (Diptera: Psychodidae) de México. Tesis de Doctorado, Universidad Nacional Autónoma de México, Mexico City, 291 pp.

    Ibáñez-Bernal, S. (2002) Phlebotominae (Diptera: Psychodidae) de México. III. -Las especies de Lutzomyia (Psathyromyia) Barreto, del grupo Aragoi, de L. (Trichopygomyia) Barreto, del grupo Dreisbachi y de L. (Nyssomyia) Barreto. Folia Entomológica Mexicana, 41, 149–183.

    Ibáñez-Bernal, S. (2005a) Phlebotominae (Diptera: Psychodidae) de México. V. Clave ilustrada para la identificación de los machos de Lutzomyia França. Folia Entomologica Mexicana, 44, 49–66.

    Ibáñez-Bernal, S. (2005b) Phlebotominae (Diptera: Psychodidae) de México. VI. Clave ilustrada para la identificación de las hembras de Lutzomyia França. Folia Entomologica Mexicana, 44, 195–212.

    Killick-Kendrick, R. (1990) Phlebotomus vectors of the leishmaniasis: a review. Medical and Veterinary Entomology, 4, 1–24.
    https://doi.org/10.1111/j.1365-2915.1990.tb00255.x

    Killick-Kendrick, R., Leaney, A.J. & Ready, P.D. (1997) The establishment, maintenance and productivity of a laboratory colony of Lutzomyia longipalpis (Diptera Psychodidae). Journal of Medical Entomology, 13, 429–440.
    https://doi.org/10.1093/jmedent/13.4-5.429

    Le Pont, F., Ibáñez-Bernal, S. & Fuentes, C. (2011) Phlébotomes du Nicaragua. 3. Une nouvelle espèce du genre Lutzomyia França, 1924 (Diptera : Psychodidae). Bulletin de la Société entomologique de France, 116, 271–276.

    Méndez-Pérez, C. & Rebollar-Téllez, A. (2012) Análisis morfométrico de poblaciones alopátricas de Lutzomyia olmeca olmeca y Lutzomyia cruciata (Diptera: Psychodidae: Phlebotominae), vectores principales de leishmaniasis cutánea en el sureste de México. Revista Biomédica, 23, 7–21.

    Mikery-Pacheco, O.F., Rojas-León, J.C., Rebollar-Tèllez, E.A. & Castillo-Vera, A. (2015) Sanfly (Diptera: Psycodidae: Phlebotominae) species diversity in an urban area of the municipality of Tapachula, Chiapas, Mexico. Memoria do Instituto Oswaldo Cruz, 110, 142−144.
    https://doi.org/10.1590/0074-02760140351

    Modi, G.B. & Tesh, R.B. (1983) A simple technique for mass rearing Lutzomyia longipalpis and Phlebotomus papatasi (Diptera: Psychodidae) in the laboratory. Journal of Medical Entomology, 20, 568–569.

    http://dx.doi.org/10.1093/jmedent/20.5.568

    Montes de Oca-Aguilar, A.C., Rebollar-Téllez, E.A., Piermarini, P. & Ibáñez-Bernal, S. (2016) Descriptions of the immature stages of Lutzomyia (Tricholateralis) cruciata (Coquillett) (Diptera: Psychodidae, Phlebotominae). Neotropical Entomology, 46, 66–85.
    https://doi.org/10.1007/s13744-016-0439-1

    Morrison, A.C., Ferro, C., Morales, A., Tesh, R.B. & Wilson, M.L. (1993) Dispersal of the sand fly Lutzomyia longipalpis (Diptera: Psychodidae) at an endemic focus of visceral leishmaniasis in Colombia. Journal of Medical Entomology, 30, 427–435.
    https://doi.org/10.1093/jmedent/30.2.427

    Morrone, J.J. (2004) Panbiogeografía, componentes bióticos y zonas de transición. Revista Brasileira de Entomologia, 482, 149–162.
    https://doi.org/10.1590/S0085-56262004000200001

    Morrone, J.J. (2014) Biogeographical regionalization of the Neotropical region. Zootaxa, 3782 (1), 1–110.

    https://doi.org/10.11646/zootaxa.3782.1.1

    Mukhopadhyay, J., Ghosh, K., Ferro, C. & Munstermann, L. (2001) Distribution of phlebotomine sand fly genotypes (Lutzomyia shannoni Diptera: Psychodidae) across a highly heterogeneous landscape. Journal of Medical Entomology, 38, 260–267.
    https://doi.org/10.1603/0022-2585-38.2.260

    Oviedo, M. & Feliciangeli, M.D. (2007) Esculpido exocoriónico de dos poblaciones de Lutzomyia longipalpis s. l. (Diptera: Psychodidae) de Venezuela. Boletín de Malariología y Salud Ambiental, 47, 253–256.

    Orellana, R., Gerald, I. & Espadas, C. (2003) Presente pasado y futuro de los climas de la Península de Yucatán. In: Colunga García, M.P. & Larqué, S.A. (Eds.), Naturaleza y Sociedad en el Área Maya. Academia Mexicana de Ciencias, CYCY, Mexico City, pp. 37–51.

    Pérez, J., Virgen, A., Rojas, J.C., Rebollar-Téllez, E.A., Castillo, A., Infante, F., Mikery, O., Marina, C.F., Ibáñez-Bernal, S. (2014) Species composition and seasonal abundance of sandflies (Diptera: Psychodidae: Phlebotominae) in coffe agroecosystems. Memorias do Instituto Oswaldo Cruz, 109, 80-86.
    https://doi.org/10.1590/0074-0276130224

    Pech-May, A., Escobedo-Ortegón, F.J., Berzunza-Cruz, M. & Rebollar-Téllez, E.A. (2010) Incrimination of four sandfly species previously unrecognized as vectors of Leishmania parasites in Mexico. Medical and Veterinary Entomology, 24, 150–161.

    http: 10.1111/j.1365-2915.2010.00870.x

    Pech-May, A., Marina, C., Vazquez-Dominguez, E., Berzunza-Cruz, M., Rebollar-Téllez, E.A., Nárvaez-Zapata, J.A., Moo-Llanes, D. & Ibáñez-Bernal, S. (2013) Genetic structure and divergence in populations of Lutzomyia cruciata, a phlebotomine sand fly (Diptera: Psychodidae) vector of Leishmania mexicana in southeastern Mexico. Infection, Genetic and Evolution, 16, 254–262.
    https://doi.org/10.1016/j.meegid.2013.02.004

    Pech-May, A., Peraza-Herrera, G., Moo-Llanes, D.A., Escobedo-Ortegón, J., Berzunza-Cruz, M., Becker-Fauser, I., Montes de Oca-Aguilar, A.C. & Rebollar-Téllez, E.A. (2016) Assessing the importance of fourth sandfly species (Diptera: Psychodidae) as vectors of Leishmania mexicana in Campeche, México. Medical and Veterinary Entomology, 30, 310–320.
    https://doi.org/10.1111/mve.12169

    Perez, J.E. & Ogusuku, E. (1997) Chorion patterns on eggs of Lutzomyia sandflies from the Peruvian Andes. Medical and Veterinary Entomology, 11, 127–133.
    https://doi.org/10.1111/j.1365-2915.1997.tb00301.x

    Perkins, V.P. (1982) The Identification and distribution of Phlebotomine sand flies in the United States with notes on the biology of two species from Florida (Diptera: Psychodidae). Abstract of dissertation presented to the graduate council of The University of Florida in Partial Fulfillment of the Requirements for degree of Doctor of Philosophy, Gainesville, Florida, 196 pp.

    Rogo, L.M., Kokwaro, E.D., Mutinga, M.J. & Khamala, C.P. (1992) Differentiation of vector species of phlebotominae (Diptera: Psychodidae) in Kenya by chorionic sculpturing of their eggs. Journal of Medical Entomology, 29, 1042–1044.
    https://doi.org/10.1093/jmedent/29.6.1042

    Rzedowski, J (1978) Vegetación de México. Limusa, México City, 431 pp.

    Sánchez-García, L., Berzunza-Cruz, M., Becker-Fauser, I. & Rebollar-Téllez, E.A. (2010) Sand flies naturally infected by Leishmania (L.) mexicana in the peri-urban area of Chetumal city, Quintana Roo, México. Transactions of the Royal Society of Tropical Medicine and Hygiene, 104, 406–411.
    https://doi.org/10.1016/j.trstmh.2010.01.010

    Sandoval-Ruiz, C., Ibáñez-Bernal, S. & Mendoza-Palmero, F. (2011) Análisis geográfico preliminar de tres especies de Phlebotominae vectores de Leishmaniasis cutánea en México, mediante modelado de nicho ecológico. Memorias de la Reunión Nacional de expertos en Leishmaniasis, Antiguo palacio de Medicina, 24 al 26 de Noviembre, México. [in press]

    Shannon, R. (1939) Methods for collecting and feeding mosquitoes in jungle yellow fever studies. American Journal of Tropical Medicine and Hygiene, 30, 131–138.

    Sherlock, I. (1957) Sobre o Phlebotomus renei Martins, Falcao and Silva, 1956 (Diptera: Psychodidae). Revista Brasileira de Biologia, 17, 547–556.

    Sierra, D., Uribe, S. & Velez, I.D. (1995) Egg surface ultrastructure of New World phlebotomine sandfly Lutzomyia gomezi (Diptera: Psychodidae). Second International Symposium on Phebotomine Sand Flies, Mérida, Venezuela, 96 pp.

    Sierra, D., Vélez, I.D. & Uribe, S. (2000) Identificación de Lutzomyia spp. (Diptera: Psychodidae) grupo verrucarum por medio de microscopia electrónica de sus huevos. Revista de Biologia Tropical, 48, 615–622.

    SMN (2014) Sistema meteorológico nacional, Análisis de reporte anual: Tapachula, Chiapas. Available from: http://smn.cna.gob.mx/climatologia/analisis/reporte/Anual2014.pdf (accessed 5 April 2017)

    Sudia, W. & Chamberlain, R. (1962) Battery light trap, an improved model. Mosquito News, 22, 126–129.

    Theodor, O. (1965) On the classification of American Phlebotominae. Journal of Medical Entomology, 2, 171–197.
    https://doi.org/10.1093/jmedent/2.2.171

    Thorpe, R.S. (1987) Geographic variation: a synthesis of cause, data, pattern and congruence in relation to subespecies, multivariate analysis and phylogenesis. Bollettino di Zoologia, 54, 3–11.
    https://doi.org/10.1080/11250008709355549

    Valderrama, A., Tavares, M.G. & Andrade-Filho, J.D. (2014) Phylogeography of the Lutzomyia gomezi (Diptera: Phlebotominae) on the Panama Isthmus. Parasites and Vectors, 7, 1–9.
    https://doi.org/10.1186/1756-3305-7-9

    Ward, R.D. & Ready, P.A. (1975) Chorionic sculpturing in some sandfly (Diptera, Psychodidae). Journal of Entomology, 50, 127–134.
    https://doi.org/10.1111/j.1365-3032.1975.tb00101.x

    West-Eberhard, M.J. (1989) Phenotypic plasticity and the origins of diversity. Annual Review of Ecology and Systematics, 20, 249–278.
    https://doi.org/10.1146/annurev.es.20.110189.001341

    West-Eberhard, M. J. (2003) Developmental Plasticity and Evolution. New York: Oxford University Press, 816 pp.

    Yammamoto, K., Caceres, A.G., Gomez, E.A., Mimori, T., Iwata, H., Koraneaqa, M., Sakurai, T., Katakura, K., Hashiguchi, Y. & Kato, H. (2013) Genetic diversity of the mitochondrial cytochrome b gene in Lutzomyia spp., with special reference to Lutzomyia peruensis, a main vector of Leishmania (Viannia) peruviana in the Peruvian Andes. Acta Tropica, 126, 156–163.
    https://doi.org/10.1016/j.actatropica.2013.02.007

    Young, D.G. & Duncan, A.M. (1994) Guide to 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 (Gainesville), 54, 1–181.

    http://dx.doi.org/10.1016/0035-9203(95)90687-8

    Young, D.G. & Perkins, P.V. (1984) Phlebotomine sandflies of North America (Diptera: Psychodidae). Journal of the American Mosquito Control Association, 44, 263–304.

    Zimmerman, J.H., Newson, H.D., Hooper, G.R. & Christensen, H.A. (1977) A comparation of the Egg surface structure of six anthropophilic phlebotomine sand flies (Lutzomyia) with scanning electron microscope (Diptera: Psychodidae). Journal of Medical Entomology, 13, 574–579.
    https://doi.org/10.1093/jmedent/13.4-5.574