Pupal shape and size dimorphism in Aedes albopictus (Skuse, 1894) (Diptera: Culicidae)

Main Article Content

Elvira Sanchez
Daniel Castillo
Jonathan Liria


Aedes albopictus (Skuse, 1894) is a culicid mosquito associated with the transmission of pathogens causative for dengue, yellow fever, chikungunya, Mayaro and other diseases. Several recent studies have proposed that demographic surveys of dengue vector pupae are more useful than traditional larval indices for estimating populations. Geometric morphometrics is a tool for describing phenotypic variation that has been validated for characterizing sexual dimorphism. We undertook to apply this method to describe sexual and morphological dimorphism in A. albopictus pupae. Two-dimensional co-ordinates were digitalized from 60 specimens in two stages using 10 landmarks in pupae and 14 in wings.  Configuration matrices were aligned by generalized procrustes analysis to extract matrix configurations and centroid size (CS).  A discriminant analysis (DA) was used to test group (female or male) membership significance, and non-parametric ANOVA was used for CS differences. We found significant differences (Kruskal-Wallis P < 0.01) among pupal cephalothorax CS and adult wings; female pupae and adults were larger than males. The DA for cephalothorax and wing specimens showed significant differences (Hotelling P < 0.0001) between females and males. Through cross-validation, females and males were correctly classified with greater than 90% accuracy using the conformation characteristics described. Our study is the first description of phenotypic variation of pupal shape and size in A. albopictus laboratory colonies, and the results can be used as an additional tool in dengue entomological survey programs. More studies are necessary to confirm the variation between natural and laboratory populations. 

Article Details

How to Cite
Sanchez, E., Castillo, D. and Liria, J. 2017. Pupal shape and size dimorphism in Aedes albopictus (Skuse, 1894) (Diptera: Culicidae). Journal of Threatened Taxa. 9, 6 (Jun. 2017), 10314–10319. DOI:https://doi.org/10.11609/jott.3059.9.6.10314-10319.
Author Biographies

Elvira Sanchez, Centro de Estudios en Zoología Aplicada, Laboratorio Museo de Zoología, Departamento de Biología, Facultad Experimental de Ciencias y Tecnología, Universidad de Carabobo, Valencia 2005, Carabobo, Venezuela.

Mrs. Elvira Sánchez is a graduate of the BS Biology program of the Biology Departament, University of Carabobo. Actually is a Lecturer-Researcher of Biology Departament, University of Carabobo. Her research interest is on mosquitoes ecology and taxonomy.

Daniel Castillo, Departamento de Biología, Facultad Experimental de Ciencias y Tecnología, Universidad de Carabobo, Valencia 2005, Carabobo, Venezuela.

Mr. Daniel Castillo is a graduate of the BS Biology program of the Biology Departament, University of Carabobo.

Jonathan Liria, Universidad Regional Amazónica IKIAM, 7 Km vía Muyuna 150150, Napo, Ecuador.

Dr. Jonathan Liria is a Lecturer-Researcher at the Ikiam University. His research interests are medical entomology, geometric morphometrics, and Culicidae systematics and biogeography.


Adams, D.C., J. Rolhf & D.E. Slice (2004). Geometric morphometrics: Ten years of progress following the ‘revolution’. Italian Journal of Zoology 71: 5–16; http://doi.org/10.1080/11250000409356545

Armbruster, P. & R. Hutchinson (2002). Pupal Mass and Wing Length as Indicators of Fecundity in Aedes albopictus and Aedes geniculatus (Diptera: Culicidae). Journal of Medical Entomology 39(4): 699–704; http://doi.org/10.1603/0022-2585-39.4.699

Barrera, R. (2009). Simplified Pupal Surveys of Aedes aegypti (L.) for Entomologic Surveillance and Dengue Control. American Journal of Tropical Medicine and Hygiene 81(1): 100–107.

Barrera, R., M. Amador & G.C. Clark (2006). Use of the pupal survey technique for measuring Aedes aegypti (Diptera: Culicidae) productivity in Puerto Rico. American Journal of Tropical Medicine and Hygiene 74(2): 290–302.

Belen, A., B. Alten & A.M. Aytekin (2004). Altitudinal variation in morphometric and molecular characteristics of Phlebotomus papatasi populations. Medical and Veterinay Entomology 18: 343–350; http://doi.org/10.1111/j.0269-283X.2004.00514.x

Benedict, M.Q., R.S. Levine, W.A. Hawley & L.P. Lounibos (2007). Spread of the tiger: Global risk of invasion by the mosquito Aedes albopictus. Vector-borne and Zoonotic Diseases 7: 76–85; http://doi.org/10.1089/vbz.2006.0562

Bookstein, F.L. (1991). Morphometric Tools for Landmark Data: Geometry and Biology. EEUU, Cambridge.

Bueno, R. & R. Jiménez (2012). Implicaciones sanitarias del establecimiento y expansión en España del mosquito Aedes albopictus. Revista Española de Salud Pública 86: 319–330.

Calle, D.A., M. Quiñónez, H. Erazo & N. Jaramillo (2008). Discriminación por morfometría geométrica de once especies de Anopheles (Nyssorhynchus) presentes en Colombia. Biomedica 28: 371–385.

Cantrell, W. (1939). Relation of size to sex in pupae of Aedes aegypti (L.), A. triseriatus (Say) and A. vexans (Meig.). Journal of Parasitology 24(4): 448–449.

Carreira, V., I. Soto, J. Mensch & J. Fanara (2011). Genetic basis of wing morphogenesis in Drosophila: sexual dimorphism and non-allometric effects of shape variation. BMC Developmental Biology 11: 32; http://doi.org/10.1186/1471-213X-11-32

Castro, A., S. Davidson, C. Azevedo, M. Bicudo de Paula & R. Marques (1994). Duration of larval and pupal development stages of Aedes albopictus in natural and artificial containers. Revista de Saúde Pública 29(1): 15–19.

Consoli, A.G. & R.L. de Oliveira (1994). Principais Mosquitos de Importância Sanitária no Brasil. Fiocruz, Rio de Janeiro, 228pp.

Couret, J., E. Doton & M.Q. Benedict (2014). Temperature, larval diet, and density effects on development rate and survival of Aedes aegypti (Diptera: Culicidae). PLoS One 9(2): e87468; http://doi.org/10.1371/journal.pone.0087468

Devicari, M., A.R. Lopes & L. Suesdek (2011). Wing sexual dimorphism in Aedes scapularis (Diptera: Culicidae). Biota Neotropica 11(2): 165–169; http://doi.org/10.1590/S1676-06032011000200016

Dujardin, J.P. (2008). Morphometrics applied to medical entomology. Infection, Genetics and Evolution 8: 875–890; http://doi.org/10.1016/j.meegid.2008.07.011

Focks, D.A. (2003). A Review of Entomological Sampling Methods and Indicators for Dengue Vectors. Gainsville, World Health Organization, 40pp.

Gratz, N.G. (2004). Critical review of the vector status of Aedes albopictus. Medical and Veterinary Entomology 18: 215–227.Â

Gunz, P. & P. Mitteroecker (2013). Semilandmarks: a method for quantifying curves and surfaces. Italian Journal of Zoology 24: 103–109.

Hammer, Ø. & D.A.T. Harper (2011). PAST: Palaeontological Statistics, versión 2.10. Available in: http:// folk.uio.no/ohammer/past.

Haramis, L.D. (1985). Larval nutrition, adult body size, and the biology of Aedes triseriatus, pp. 431–437. In: Lounibos, L.P., J.R. Rey, J.H. Frank (eds.). Ecology of Mosquitoes: Proceedings of a Workshop. Florida Medical Entomology Laboratory, Vero Beach, FL.

Harrison, B. (2005). Easily seen characters to identify the pupa of Aedes albopictus in the united states. Journal of the American Mosquito Control Association 21(4): 451–454.

Hayes, R.O. (1953). Studies on the artificial insemination of the mosquito Aedes aegypti (L.). Mosquito News 13(2): 145-152.

Hernandez, M., M. Piña, A. Soto-Vivas, M.A. Rangel & J. Liria (2015). Primer registro de Aedes albopictus (Skuse, 1894) (Diptera: Culicidae) en el Estado Carabobo, Venezuela. Salus 19: 39–41.

Jirakanjanakit, N., W.A.T. Leemingsa, S. Thongrungkiat, S. Apiwathnasorn, C. Singhaniyom, C. Bellec & J.P. Dujardin (2007). Influence of larval density or food variation on the geometry of the wing of Aedes (Stegomyia) aegypti. Tropical Medicine and International Health 12(11): 1354–1360.

Klingenberg, C.P. (2011). MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11: 353–357; http://doi.org/10.1111/j.1755-0998.2010.02924.x

Lounibos, L.P. (1994). Geographical and developmental components of adult size of neotropical Anopheles (Nyssorhynchus). Ecological Entomology 19: 138–146.

Massad, E., F.A.B. Coutinho, M.N. Burattini & L.F. Lopez (2001). The risk of yellow fever in a dengue-infested area. Transactions of the Royal Society of Tropical Medicine and Hygiene 9: 370–374.

Mikery-Pacheco, O., K. Serrano-Domínguez, P. Marcelín-Chong & D. Sánchez-Guillén (2015). Efficiency of the separation of Aedes (Stegomyia) albopictus (Diptera: Culicidae) male and female pupae using a sieving device. Acta Zoológica Mexicana 31(1): 113–115.

Moorefield, H.M. (1951). Sexual dimorphism in mosquito pupae. Mosquito News 11: 175-177.

Morales-Vargas, E.R., P. Ya-Umphan, N. Phumala-Morales, N. Komalamisra & J.P. Dujardin (2010). Climate associated size and shape changes in Aedes aegypti (Diptera: Culicidae) populations from Thailand. Infection, Genetics and Evolution 10: 580–585; http://doi.org/10.1016/j.meegid.2010.01.004

Muñoz, M. & J.C. Navarro (2012). Virus Mayaro: un arbovirus reemergente en Venezuela y Latinoamérica. Biomédica 32: 286–302; http://doi.org/10.7705/biomedica.v32i2.647

Nasci, R.S. & C.J. Mitchell (1994). Larval diet, adult size, and susceptibility of Aedes aegypti (Diptera: Culicidae) to infection with Ross River virus. Journal of Medical Entomology 31: 123–126.

Nuñez-Rodríguez, J.A. & J. Liria (2017). Geometric morphometrics sexual dimorphism in three forensically-important species of Blow Fly (Diptera: Calliphoridae). Life: The Excitement of Biology 4(4): 272–284; http://doi.org/10.9784/LEB4(4)NunezRodriguez.01

Oliveira, P., E. Carvalho & L. Suesdek (2012). Temporal variation of wing geometry in Aedes albopictus. Memórias do Instituto Oswaldo Cruz 107(8): 1030–1034; http://doi.org/10.1590/S0074-02762012000800011

Penn, G.H. (1949). The pupae of mosquitoes of New Guinea. Pacific Science 3(1): 1–85.

Reiter, P. (1998). Aedes albopictus and the world trade in used tires, 1988-1995: the shape of things to come? Journal of the American Mosquito Control Association 14: 83–94.

Rohlf, J. (2008). tpsDig, Program for Digitalizing morphologic landmark and outlines for Geometric Morphometric Analyses, ver. 2.11. Department of Ecology and Evolution, State University of New York at Stony Brook. Available from: http://life.bio.sunysb.edu/morph/index.html

Rohlf, J. (2016). tpsRelw, Program provides a low dimensional approximation (via a principal components analysis) to the tangent space approximation of shape space, ver. 1.62. Department of Ecology and Evolution, State University of New York, Stony Brook. Available from: http://life.bio.sunysb.edu/morph/index.html

Rohlf, J. & L. Marcus (1993). A revolution in morphometrics. Trends in Ecology and Evolution 8: 129–132; http://doi.org/10.1016/0169-5347(93)90024-J

Rúa-Uribe, G., C. Suárez-Acosta & R. Rojo (2012). Implicaciones epidemiológicas de Aedes albopictus (Skuse) en Colombia. Revista Facultad Nacional de Salud Pública 30(3): 328–337.

Sheets, H.D. (2010). MakeFan, a tool for drawing alignment “fans†at equal angular spacing. Available from: http://www3.canisius.edu/~sheets/imp7.htm

Vargas, M. (1968). Sexual dimorphism of larvae and pupa of Aedes aegypti (Linn.). Mosquito News 28(3): 374–379.

Vásquez, M. & J. Liria (2012). Morfometría geométrica alar para la

identificación de Chrysomya albicep sy C. megacephala (Diptera: Calliphoridae) de Venezuela. Revista de Biología Tropical 60(3): 1-10; http://doi.org/10.15517/rbt.v60i3.1776

Virginio, F., P. Oliveira & L. Suesdek (2015). Wing sexual dimorphism of pathogen-vector culicids. Parasite and Vectors 8(1): 159–167; http://doi.org/10.1186/s13071-015-0769-6

Webster, M. & H.D. Sheets (2010). A practical introduction to landmark-based geometric morphometrics. pp. 163–188. In: Alroy, J. & G. Hunt (eds.). Quantitative Methods in Paleobiology. Paleontological Society Papers. Volume 16.

Xue, R.D., D.R. Barnard & G.C. Muller (2010). Effects of body size and nutritional regimen on survival in adult Aedes albopictus (Diptera: Culicidae). Journal of Medical Entomology 47(5): 778–782; http://doi.org/10.1603/ME09222