Morphometric variability of anopheles pseudopunctipennis (Diptera: Culicidae) from different ecoregions of Argentina and Bolivia.
Species of Anopheles Meigen reported to be important malaria vectors include An. (Nyssorhynchus) albimanus Wiedeman, An. (Nyssorhynchus) aquasalis Curry, An. (Nyssorhynchus) darlingi Root and An. (Anopheles) pseudopunctipennis Theobald (Forattini 1962). Some species of the Nyssorhynchus subgenus involved in malaria transmission share the same geographical distribution and posses a high degree of morphological similarity (Faran 1980). For example, An. (Nyssorhynchus) evansae Brethes was misidentified as An. (Nyssorhynchus) benarrochi Gabaldon, Cova Garcia and Lopez and, furthermore, An. benarrochi females were misidentified as An. (Nyssorhynchus) oswaldoi Peryassu, confirmed later as An. benarrochi species (Quinones et al. 2001; Calle et al. 2002).
The present study was focused on An. pseudopunctipennis, a species with a wide distribution that has distinctive populations defined by allozymes and restriction fragment length polymorphisms (RFLPs) (Estrada-Franco et al. 1993). A more extensive study revealed the existence of three clusters within An. pseudopunctipennis: one comprising specimens from the United States, Mexico and Guatemala, a second cluster including samples from Colombia, Ecuador, Peru, Chile and Argentina, and a third cluster comprising Grenada specimens (Manguin et al. 1995). Rueda et al. (2004), describing the neotype of An. pseudopunctipennis, suggested the need for morphological, molecular and biochemical studies for a better definition of the species limit.
Within the morphological context, morphometry (Rohlf & Marcus 1993; Adams et al. 2004) appears as an important taxonomic tool for species discrimination and species variations (Dujardin et al. 1997, 1998; Calle et al. 2002; Jaramillo et al. 2002; Monroy et al. 2003; Belen et al. 2004; Lehmann et al. 2005; Yurtas et al. 2005; Feliciangeli et al. 2007). Delgado & Rubio-Palis (1993) examined the morphometric variation of Anopheles (Nyssorhynchus) nuneztovari Gabaldon and detected variability within Venezuelan populations. Later, Rubio-Palis (1998, 2000), using measurements of larval and adult characters of An. darlingi populations from Venezuela, confirmed the separation of this species from Anopheles (Nyssorhynchus) marajoara Galvao and Damasceno, Anopheles (Nyssorhynchus) braziliensis (Chagas) and Anopheles (Nyssorhynchus) argyritarsis Robineau-Desvoidy, and found biological and morphological variations of this species, suggesting it may represent a species complex. Most of these studies were focused on the molecular or morphological characterization of Anopheles species to probe similarity or variability between them or within each, sharing the same geographical areas, and trying to differentiate these populations and their implications as malaria vectors.
In the present paper we used cladistics and morphometric analysis to test whether either ecoregional characterization or geographical distance has a greater effect in differentiating An. pseudopunctipennis populations found in the Transitional and Yungas ecoregions of Argentina and Convergence ecoregion of Bolivia.
MATERIALS AND METHODS
Sample Area Characterization
Adult mosquitoes were collected in 15 localities, 13 in Argentina and two in Bolivia. In Argentina, Jujuy and Salta localities were from
the Yungas ecoregion, while the Tucuman localities were from the transitional area between Yungas and Chaco ecoregiones (Cabrera & Willink 1973; Dinerstein et al. 1995). Parque Nacional Carrasco (Cochabamba, Bolivia) is in the convergence of three ecoregions: Cloud Forests (Yungas), Dry Forests (Dry Chaco) and Tropical Amazon Rainforest (The Nature Conservancy 2008). In Taruma (Santa Cruz, Bolivia), the ecoregion is called Transitional Amazon Forest of Chiquitana (IBIF 2006) (Fig. 1).
The Yungas has a large geographical distribution in South America, from Venezuela through northwestern Argentina. It is frequently fragmented by either natural events (flooding rivers) or human activities (agriculture, pastures and wood production). The typical piedmont vegetation consists of two types of vegetation with a north-south orientation in response to temperature gradient: one is the forest of "palo blanco" (Calycophyllum multiflorum Griseb. (Castelo)) and "palo amarillo" (Phyllostylon rhamnoides (J. Poiss.) Taub.), and the second is the forest of "tipa" (Tipuana tipu (Benth.) Kuntze) and "pacara" (Enterolobium contortisiliquum (Vell.) Morong.). Both vegetation types are under anthropic pressure, that in the impoverished south is nearly completely destroyed, and that in the north is more diverse (Prado 1995; Brown et al. 2001).
The Chaco ecoregion extends from southern Bolivia through western Paraguay, southern Brazil and north-central Argentina. It is composed of deciduous xeric forests with grasses, cacti and terrestrial bromeliads, and, also, the savannas and the halophytic steppes (Cabrera & Willink 1973; Cabrera 1976; Dinerstein et al. 1995). In western Chaco province, there is a transitional area (with the Yungas) (Ayarde 1995). The Chaco province is threatened by cattle grazing, seasonal fires and the conversion of natural habitats for agriculture (Dinerstein et al. 1995).
[FIGURE 1 OMITTED]
Parque Nacional Carrasco near Cochabamba, Bolivia lies in the Sub-Andean range. This park has vegetation typical of the semihumid Puna, the perennial wet to semi-wet forest, the Amazonic Sub-Andean forest, the pre-Andean forest, the inter-Andean dry forest and the Tucumanian-Bolivian subtropical mountainous forest, also known as Yungas. The main problems in this area are deforestation to allow cultivation, commercialization of tree species of economic value, and highway construction (boliviaenlared.com 2005-2006).
At Taruma (Santa Cruz Department in eastern Bolivia), the climate in the region largely determines the predominant vegetation known as the Transitional Amazon Forest of Chiquitana (IBIF 2006). This is a characteristic forest with Amazonian humid weather alternating with Chaco dry weather. Thus two well-marked seasons exist, a dry and a wet one. During the wet season (Apr-Nov) most of the rainfall occurs, and during the dry season (May-Jul) rainfall decreases considerably. In recent years the environment has changed and the weather has become drier. The forest is mostly dry tropical, with some interspersed savanna. To the north is the humid part of the forest and the savannas. The pastures present the most important problem because of soil degradation, but recently sustainable agriculture has started to be used in an effort to try to conserve the environment (IBIF 2006).
In Argentina, the adult specimens were collected as described by Dantur et al. (2003, 2005, 2009). In Bolivia, specimens were collected individually as larvae and reared to adults. They were subsequently sacrificed and identified using the taxonomic key of Wilkerson & Strickman (1990). To carry out the morphometric measurements (in mm), the specimens were mounted on entomological pins, labeled, and examined with a stereoscopic microscope.
One hundred and seventy-three An. pseudopunctipennis female specimens were analyzed: 24 from Salta (localities: Parque Nacional El Rey, El oculto and Aguas Blancas), 41 from Jujuy (INTA Yuto and Lagunita Yuto), 51 from Tu cuman (Iltico, Dique El Molino, Quebrada de Lules, Potrero Las Tablas, El Cadillal, Arroyo Molle Yaco, Arroyo Hornillo and La Sala) and 57 from Bolivia (Parque Nacional Carrasco and Taruma) (Table 1). The following characters were measured: length of proboscis and length of palpomeres 1-5, pale and dark scale spots on the costal vein. For wing spots, we adopted the nomenclature proposed by Wilkerson & Peyton (1990): length of the basal pale (BP), sectoral dark (SD), subcostal pale (SCP), preapical dark (PD), preapical pale (PP).
Cladistics. Parsimony analysis was conducted with the software TNT 1.0 (Goloboff et al. 2005), which allows the use of continuous characters to obtain a phylogenetic hypothesis. Once the confidence intervals were calculated (CI = Mean [+ or -] [Z.sub.[alpha]/2] xS/[square root]N) with [alpha] = 0.05 (Norman & Streiner 1996) for each locality of An. pseudopunctipennis (Table 2), the algorithm proposed by Goloboff et al. (2006) was used, where the morphometric characters were treated as additive, and the ranges were optimized directly on the most parsimonious cladograms. The neotype redescription of An. pseudopunctipennis was used (Rueda et al. 2004) as the outgroup and for rooting cladograms. Finally, the exact algorithm of implicit enumeration for the search of the most parsimonious solution was followed.
Morphometrics: The logarithmic transformation ([Log.sub.10] (X + 1)) was carried out on the complete data set to minimize intrapopulation variation due to static allometry. Subsequently, the size effects were corrected following Klingenberg (1996) based on the common model of linear growth (Common Principal Components Analysis or CPCA). The CPC scores were considered as an estimate of within-group variation and were used as variables in a canonical discriminate analysis (CDA) except for CPC1, which is an estimate of the common allometric pattern (Klingenberg 1996; Dujardin 2000). The variables were introduced in the PAD 0.81 program (Dujardin 2006) to carry out a Discriminant Analysis (DA). The results were graphically represented in a scatter plot using the first two canonical discriminant functions as axes. To examine the morphological similarity between the populations, the Mahalanobis distances obtained in CDA and the Cluster Analysis with Unweighted Pair Group Method Analysis (UPGMA) NEIGHBOR 3.6 (Felsenstein 2004) were used, and the resulting dendrogam was visualized in TREEVIEW 1.6.6 (Page 2001). To test for significant differences among populations, size variables were analyzed with the Kruskal-Wallis test ([alpha] = 0.05).
In the cladistic analysis six equally parsimonious trees were obtained of 4,608 steps in length, with consistency and retention indices of 0.91 and 0.82, respectively. The strict consensus of these trees (Fig. 2) depicts the Bolivian populations (Taruma and Parque Nacional Carrasco) as more basal (ancestral), sister of the node that includes all the Argentinean populations (Salta, Jujuy and Tucuman) consisting of a polytomy that includes 7/8 of the Tucuman localities (Arroyo Mole Yaco, El Cadillal, Quebrada de Lules, El Molino, Iltico, Arroyo Hornillo and La Sala), a clade that includes a mixture of Jujuy (INTA Yuto and Lagunita Yuto) and Tucuman (Potrero Las Tablas) localities and finally a clade that contains the Salta localities (El Oculto, Parque Nacional El Rey and Aguas Blancas).
[FIGURE 2 OMITTED]
The node that separates Argentinean and Bolivian populations is supported by the following synapomorphies: length of palpomere 1 (character 0: 0.109-0.116 [right arrow] 0.127), length of palpomere 5 (character 4: 0.208-0.222 [right arrow] 0.237-0.253), length of the basal pale (character 5: 0.092-0.093 [right arrow] 0.018-0.033) and proboscis length (character 10: 1.905-1.958 1.990-2.195). The Salta clade (El Oculto+Parque Nacional El Rey+Aguas Blancas) is characterized by the length of palpomere 1 (character 0: 0.127 [right arrow] 0.245-0.255), and Parque Nacional El Rey and Aguas Blancas clustered together by the length of the basal pale spot (character 5: 0.033 [right arrow] 0.063). The clade comprising Potrero Las Tablas, INTA Yuto and Lagunita Yuto populations is supported by the length of the basal pale spot (character 5: 0.022-0.033 [right arrow] 0.090-0.091). Populations of An. pseudopunctipennis in some localities can be defined by autapomorphies: Aguas Blancas by the length of the basal pale spot (character 5: 0.063 [right arrow] 0.106), Potrero Las Tablas by the length of palpomere 1 (character 0: 0.127 [right arrow] 0.0148-0.206), Iltico by the length of palpomere 1 (character 0: 0.127 [right arrow] 0.129-0.159), Quebrada de Lules by the length of sector dark spot (character 7: 0,388-0,443 [right arrow] 0.506) and Lagunita Yuto by proboscis length (character 10: 2.303-0.2305 [right arrow] 2.181-2.277).
In contrast, the DA factorial map, starting from the first nine conformation components (representing 98% of the variation of the conformation), showed partial separation of the Salta population and overlap between Tucuman and Jujuy, Cochabamba and Santa Cruz populations (Fig. 3A). The reclassification of the five populations was as follows: Salta 23l24 (95%) and Jujuy 35l41 (85%) and Cochabamba 27l31 (87%), and it was reduced in Tucuman 38l51 (74%) and Santa Cruz 17l26 (65%).
The cluster analysis UPGMA (Fig. 3B) shows the differentiation of Salta from the other four. Tucuman population differs from the cluster formed by Cochabamba, Santa Cruz and Jujuy. The size variable (Fig. 3C) showed significant differences (p < 0.05), from the smallest to the largest, for three groups of populations: Cochabamba, < Salta, Tucuman and Santa Cruz < Jujuy.
The geographical distribution of An. pseudopunctipennis is a sympatric with other species, such as An. abimanus and An. argyritarsis; but each of these species occupies a somewhat different typical environment.
As reported by Patz et al. (2000) and Alencar et al. (2009), it is known that environmental changes will modify vector-borne disease transmission patterns. Accordingly in Argentina, Burgos et al. (1994) reported that malaria and An. pseudopunctipennis distributions acquire different patterns when moving from the foothills to the central region of the country where climatic conditions are more favorable for the development of both. Curto et al. (2003) disagreed with these authors, and asserted that An. pseudopunctipennis and malaria distribution would change in relation to modifications in the climatic conditions and eventually would be restricted to the extreme northwest of the country.
[FIGURE 3 OMITTED]
Environmental changes will directly affect vector populations by causing modification within each population of traits including morphological characters that evolve under ecological pressure (Rundle & Nosil 2005; Alencar et al. 2009). Different studies have concluded that morphometry is useful because it is focused on morphological traits and modifications in them, and is a good tool for the discrimination of vector species as well as for studies of intraspecific population variability (Dujardin et al. 1997, 1998; Rubio-Palis 1998; Calle et al. 2002: Yurtas et al. 2005). Just as in Haemagogus capricornii Lutz and Haemagogus janthinomys Dyar populations in Brazil, the molecular and morphological diversity of An. pseudopunctipennis populations can be expected to evolve under different types of ecological pressure (ecoregional characteristics) (McKinnon et al. 2004; Alencar et al. 2009).
There are several works dealing with An. pseudopunctipennis populations in America. By analyses of specimens from various localities, Estrada-Franco et al. (1993) and Manguin et al. (1995) recognized the existence of three An. pseudopunctipennis population groups: one from the southern USA, Mexico and Guatemala, another from South America through Central America including Belize, and a third on Grenada Island. Previous to the present study, there had been no examination of external morphological characters of An. pseudopunctipennis populations in relation to ecoregional characteristics. This is the first report that deals with the morphological traits of specimens that have been affected by the ecological conditions that characterize each ecoregion.
In view of the risk of malaria re-emergence in the extreme northwest of Argentina, where until now only a few cases were reported, the behavior of this species becomes very important. Because there is active transmission of the disease in certain areas of Bolivia near Argentina, the need to differentiate between the various An. pseudopunctipennis populations in relation to transmission patterns is critical. The cladistic analyses described here accurately differentiated between Argentinean and Bolivian populations by proboscis and palpomere lengths. Similarly, Manguin et al. (1999) found that proboscis length and the forefemur differentiated populations of An. darlingi.
Morphometric analyses did not reveal any population differentiation of An. pseudopunctipennis based on geographical distances. Bolivian and Tucuman populations should be the most differentiated, but the results of the Discriminant Analysis showed that Salta populations have the least overlap. The UPGMA separated the Salta group of specimens from the remaining four population groups, and PCA detected the greatest difference between Jujuy and Cochabamba.
We conclude that the methods used were useful for the analysis of An. pseudopunctipennis populations, allowing us (1) to differentiate between two An. pseudopunctipennis populations (Bolivian and Argentinean), and (2) to discover that the characteristics of the ecoregion, i.e., the local environment, cause such differentiation between populations to occur. Finally, it is necessary to consider the effect of the changing global weather and in particular, the consequent increase in average global temperatures and accumulated rainfall (Magnuson 2001; Moreno 2006; Alencar et al. 2009) that will affect not only malaria transmission patterns, but also cause the vector populations involved to evolve further (Mc Michael 2001; Alencar et al. 2009). For this reason it is necessary to acquire further knowledge about the possible existence of An. pseudopunctipennis populations in the extreme south of South America.
The authors thank Nery Vianconi and Enrique Laci, Technicians of the National Coordination of Vectors Control, Ministry of Health of the Argentina, for their field assistance. This work was supported by Grants (PICT 01-04347; PICT 02- 12605) from Agencia Nacional de Promotion Cientifica y Tecnologica (FONCyT), Consejo Nacional de Investigaciones Cientificas Tecnicas (CONICET), Consejo de Investigaciones de la Universidad Nacional de Tucuman (CIUNT) and Coordinacion Nacional de Control de Vectores (Ministerio de Salud de la Nacion). The samples from Bolivia were collected by G. N. Fritz and R. Rodriguez, supported in part by the United States National Institutes of Health, Grant R01 AI 31034.
ADAMS, D. C., ROLHF, F. J., AND SLICE, D. E. 2004. Geometric morphometrics: Ten years of progress following the 'revolution'. Ital. J. Zool. 71: 5-16.
ALENCAR, J., RODRIGUEZ-FERNANDEZ, J., DEGALLIER, N., BRISOLA MARCONDES, C., MARTINS COSTA, J., AND GUIMARAES, A. E. 2009. Multivariate Discrimination between two cryptic Haemagogus species associated with the transmission of Yellow Fever Virus in the Americas. J. Am. Mosquito Control Assoc. 25: 18-24.
AYARDE, H. 1995. Estructura de un sector de selva pedemontana, Reserva Fiscal Parque La Florida, Tucuman, Argentina, pp. 69-78 In A. D. Brown and H. R. Grau [eds.], Investigation, Conservation y Desarrollo en las selvas subtropicales de montana, Laboratorio de Investigaciones Ecologicas de las Yungas, Universidad Nacional de Tucuman, Tucuman, Argentina.
BELEN, A., ALTEN, B., AND AYTEKIN, A. M. 2004. Altitudinal variation in morphometric and molecular characteristics of phlebotomus papatasi populations. Med. Vet. Entomol. 18: 343-350.
BOLIVIAENLARED.COM. 2005-2006. Biologia: Ecologia: Areas protegidas: Parque Carrasco. http://www.boliviaenlared.com/html/parque-carrasco.html [Accessed 20 May 2008]
BROWN, A. D., GRAU, H. R., MALIZIA, L., AND GRAU, A. 2001. Los Bosques Nublados de la Argentina, pp. 623-659 In M. Kappelle and A. D. Brown [eds.], Bosques Nublados de Latinoamerica, Editorial IN-Bio, Costa Rica.
BURGOS, J. J., CURTO DE CASAS, S. I., CARCAVALLO, R. U., AND GALINDEZ-GIRON, G. I. 1994. Global climate change influence in the distribution of some pathogenic complexes (malaria and chagas disease) in Argentina. Entomologia y Vectores 1: 69-78.
CABRERA, A. L. 1976. Regiones fitogeograficas argentinas. Enciclopedia Argentina de Agricultura y Jardineria, Vol. II, ACME, Buenos Aires, Argentina, 85 pp.
CABRERA, A. L., AND WILLINK, A. 1973. Biogeografia de America Latina. Monografia 13, Serie de Biologia, OEA, Washington, D.C.
CALLE, D. A., QUINONEZ, M., ERAZO, H., AND JARAMILLO, N. 2002. Morphometric discrimination of females of five species of Anopheles of the Subgenus Nyssorhynchus from Southern and Northwest Colombia. Memorias do Instituto Oswaldo Cruz 97: 1191-1195.
COLLINS, F. H., AND PASKEWITZ, S. M. 1995. Malaria: Current and future prospects for control. Annu. Rev. Entomol. 40: 195-219.
CURTO, S. I., CARBAJO, A. E., AND BOFFI, R. 2003. Aplicacion de Sistemas de Information Geografica en Epidemiologia. Caso de estudio: Malaria en la Argentina (1902-2000). GAEA, Sociedad Argentina de Estudios Geograficos, 2003: 239-248.
DANTUR JURI, M. J., ZAIDENBERG, M., AND ALMIRON, W. R. 2003. Fluctuacion estacional de Anopheles (Anopheles) pseudopunctipennis (Diptera: Culicidae) en un area paludica de Salta, Argentina. Entomologia y Vectores 10: 457-468.
DANTUR JURI, M. J., ZAIDENBERG, M., AND ALMIRON, W. R. 2005. Distribucion espacial de Anopheles pseudopunctipennis en las Yungas de Salta, Argentina. Revista de Saude Publica 39: 565-70.
DANTUR JURI, M. J., ZAIDENBERG, M., CLAPS, G. L., SANTANA, M., AND ALMIRON, W. R. 2009. Malaria transmission in two localities in north-western Argentina. Malaria J. 8: 18.
DELGADO, N., AND RUBIO-PALIS, Y. 1993. Identification of Anopheles (Nyssorhynchus) (Diptera: Culicidae) occurring in Western Venezuela. Mosquito Systematics 25: 222-230.
DINERSTEIN, E., OLSON, D. M., GRAHAM, D. J., WEBSTER, A. L., PRIMM, S. A., BOOKINBER, M. P., AND LEDEC, G. 1995. Una evaluation del estado de conservacion de las ecoregiones terrestres de America Latina y el Caribe. World Bank, Washington, D.C.
DUJARDIN, J. P. 2000. Introduccion a la Morfometria, con Enfasis en Triatominae y Phlebotominae. Institut de Recherches pour le Developpement (IRD), Montpellier--France. http://www.mpl.ird.fr/morphometrics/ [Accessed 15 March 2008]
DUJARDIN, J. P. 2006. PAD (Analisis Discriminante y Permutaciones) version 0.81. Institut de Recherches pour le Developpement (IRD), Montpellier--France. http://www.mpl.ird.fr/morphometrics/ [Accessed 15 March 2008]
DUJARDIN, J. P., BERMUDEZ, H., CASINI, C., SCHOFIELD, C. J., AND TIBAYRENC, M. 1997. Metric differences between sylvatic and domestic Triatoma infestans (Hemiptera: Reduviidae) in Bolivia. J. Med. Entomol. 34: 544-551.
DUJARDIN, J. P., FORGUES, G., TORREZ, M., MARTINEZ, E., CORDOBA, C., AND GIANELLA, A. 1998. Morphometrics of domestic panstrongylus rufotuberculatus in Bolivia. Ann. Trop. Med. Parasit. 92: 219-228.
ESTRADA-FRANCO, J. G., LANZARO, G. C., MA, M. C., WALKER-ABBEY, A., ROMANS, P., GALVAN-SANCHEZ, C., CESPEDES, J. L., VARGAS-SAGARNAGA, R., LAUGHINGHOUSE, A., COLUMBUS, I., AND GWADZ, R. W. 1993. Characterization of Anopheles pseudopunctipennis sensu lato from three countries of Neotropical America from variation in allozymes and ribosomal DNA. Am. J. Trop. Med. Hyg. 49: 735-745.
FARAN, M. 1980. Mosquito Studies (Diptera: Culicidae) XXXIV. A revision of the Albimanus Section of the subgenus Nyssorhynchus of Anopheles. Contributions of the American Entomol. Institute 15: 1-214.
FELICIANGELI M. D., SANCHEZ-MARTIN, M., MARRERO, R., DAVIES, C., AND DUJARDIN, J. P. 2007. Morphometric evidence for a possible role of Rhodnius prolixus from palm trees in house re-infestation in the State of Barinas (Venezuela). Acta Tropica 101: 169-177.
FELSENSTEIN, J. 2004. NEIGHBOR-Neighbor-Joining and UPGMA methods. http://evolution.gs.washington.edu/phylip/ [Accessed 15 March 2008]
FORATTINI, O. P. 1962. Entomologia Medica. Vol. 1. Parte general, Diptera Anophelini. Facultade de Higiene y Saude Publica, Sao Paulo. 662 pp.
GOLOBOFF, P. A., FARRIS, J. S., AND NIXON, K. 2005. Tree Analysis Using New Technology (TNT). Version 1.0. http://www.zmuc.dk/public/phylogeny/tnt [Accessed 15 March 2008]
GOLOBOFF, P. A., MATTONI, C. I., AND QUINTEROS, A. S. 2006. Continuous characters analyzed as such. Cladistics 22: 1-13.
INSTITUTO BOLIVIANO DE INVESTIGACIONES FORESTALES (IBIF). 2006. Estaciones de campo: La Chonta. http://www.ibifbolivia.org.bo/ESP/estaciones_de_campo/la_chonta.htm [Accessed 20 May 2008]
JARAMILLO, N., CASTILLO, D., AND WOLFF, M. 2002. Geometric morphometric differences between pan strongylus geniculatus from field and laboratory. Memorias do Instituto Oswaldo Cruz 97: 667-673.
KLINGENBERG, C. P. 1996. Multivariate allometry, pp. 23-49 In L. F. Marcus, M. Corti, A. Loy, G. J. Naylor and D. E. Slice [eds.], Advances in Morphometrics. Proc. NATO-ASI on Morphometrics. Plenum Pres, New York.
LEHMANN, P., ORDONEZ, R., OJEDA-BARANDA, R., MENDEZ DE LIRA, J., HIDALGO-SOSA, L., MONROY, C., AND RANSEY, J. M. 2005. Morphometric analysis of Triatoma dimidiata populations (Reduviidae: Triatominae) from Mexico and Northern Guatemala. Memorias do Instituto Oswaldo Cruz 100: 477-482.
MAGNUSON, J. 2001. 150-year global ice record reveals major warming trend. Inter-Am. Inst. Glob. Change Res. 24: 22-25.
MANGUIN, S., ROBERTS, D., PEYTON, E. L., FERNANDEZ-SALAS, I., BARRETO, M., FERNANDEZ-LOAYZA, R., SPINOLA, R. E., MARTINEZ-GRANAOU, R., AND RODRIGUEZ, M. H. 1995. Biochemical systematic and population genetic structure of Anopheles pseudopunctipennis, vector of malaria in Central and South America. Am. J. Trop. Med. Hyg. 53: 362-377.
MANGUIN, S., WILKERSON R. C., CONN, J. E. RUBIO-PALIS, Y., DANOFF-BURG, J., AND ROBERTS, D. 1999. Population structure of the primary malaria vector in South America, Anopheles darlingi, using isoenzyme, random amplified polymorphic DNA, internal transcribed spacer 2, and morphologic markers. Am. J. Trop. Med. Hyg. 60: 364-376.
MCKINNON, J. S., MORI, S., BLACKMAN, B. K., DAVID, L., KINGSLEY, D. M., JAMIESON, L., CHOU J., AND SCHLUTER, D. 2004. Evidence for ecology's role in speciation. Nature 429: 294-298.
MCMICHAEL, A. J. 2001. Global environmental change as "risk factor": can epidemiology cope? Am. J. Public Health 91: 1172-1174.
MONROY, C. BUSTAMANTE, D. M., RODAS, A., ROSALES, MEJIA, M., AND TABARU, Y. 2003. Geographic distribution and morphometric differentiation of Triatoma nitida Usinger 1939 (Hemiptera: Reduviidae: Triatominae) in Guatemala. Memorias do Instituto Oswaldo Cruz 98: 37-43.
MORENO, A. R. 2006. Climate change and human health in Latin America: drivers, effects, and policies. Region. Environ. Change 6: 157-164.
NORMAN, G. R., AND STRINER, D. L. 1996. Bioestadistica. Rubes Editorial Harcourt SL, ed. Madrid: Harcourt Brace de Espana, S.A., pp. 150-162.
PAGE, R. 2001. TreeView--Tree drawing software for Apple Macintosh and Microsoft Windows. http://taxonomy.zoology.gla.avc.uk/rod/rod.html [Accessed 20 March 2008].
PATZ, J. A., GRACZYK, T. K., GELLER, N., AND VITTOR, A. Y. 2000. Effects of environmental change on emerging parasitic diseases. Int. J. Parasitol. 30: 1395-1405.
PRADO, D. E. 1995. Selva pedemontana: contexto regional y lista floristica de un ecosistema en peligro, pp. 19-52 In A. D. Brown and H. R. Grau [eds.], Investigacion, Conservacion y Desarrollo en las selvas subtropicales de montana, Laboratorio de Investigaciones Ecologicas de las Yungas, Universidad Nacional de Tucuman, Tucuman, Argentina.
QUINONES M. L., HARBACH R. E., CALLE, D. A., RUIZ, F., ERAZO, H. F., AND LINTON, Y. M. 2001. Variante morfologica de hembras de Anopheles benarrochi (Diptera: Culicidae) en Putumayo, Colombia. Biomedica 21: 351-359.
ROLHF, F. J., AND MARCUS, L. F. 1993. A revolution in morphometrics. Trends Ecol. Evol. 8: 129-132.
RUBIO-PALIS, Y. 1998. Caracterizacion morfometrica de poblaciones de Anopheles (Nyssorhynchus) darlingi del sur de Venezuela. Boletin Entomologia Venezolana 13: 141-172.
RUBIO-PALIS, Y. 2000. Anopheles (Nyssorhynchus) de Venezuela: Taxonomia, bionomia, ecologia e importancia medica. Escuela de Malariologia y Saneamiento Ambiental "Dr. Arnoldo Gabaldon" y el Proyecto Control de Enfermedades Endemicas. Maracay, Venezuela. 120pp.
RUEDA, L. M., PEYTON, E. L., AND MANGUIN, S. 2004. Anopheles (Anopheles) pseudopunctipennis Theobald (Diptera: Culicidae): Neotype designation and description. J. Med. Entomol. 41: 12-22.
RUNDLE, H. D., AND NOSIL, P. 2005. Ecological speciation. Ecol. Letters 8: 336-352.
SALLUM, M. A. M., SHULTZ, T. R., AND WILKERSON, R. C. 2000. Phylogeny of Anophelinae (Diptera: Culicidae) based on morphological characters. Ann. Entomol. Soc. Am. 93: 745-775.
THE NATURE CONSERVANCY. 2008. Bolivia: Places we protect: Amboro and Carrasco National Park. http://www.nature.org/wherewework/southamerica/bolivia/work/art10696.html [Accessed 20 May 2008]
WILKERSON, R. C., AND PEYTON, E. L. 1990. Standardized nomenclature for costal wing spots of the genus Anopheles and other spotted-wing mosquitoes (Diptera: Culicidae). J. Med. Entomol. 27: 207-224.
WILKERSON, R. C., AND STRICKMAN, D. 1990. Illustrated key to the female anopheline mosquitoes of Central America and Mexico. J. Amer. Mosquito Control Assoc. 6: 7-34.
YURTAS, H., ALTEN, B., AND AYTEKIN, A. M. 2005. Variability in natural populations of Anopheles sacharovi (Diptera: Culicidae) from southeast Anatolia, revealed by morphometric and allozymic analysis. J. Vector Ecol. 30: 206-212.
MARIA J. DANTUR JURI (1), JONATHAN LIRIA (2), JUAN C. NAVARRO (3), ROBERTO RODRIGUEZ (4) AND GARY N. FRITZ (5)
(1) Instituto Superior de Entomologia "Dr. Abraham Willink", Facultad de Ciencias Naturales e Instituto Miguel Lillo, Universidad Nacional de Tucuman, Miguel Lillo 205, T4001MVB, Tucuman, Argentina
(2) Departamento de Biologia, Facyt, Universidad de Carabobo, Valencia edo. Carabobo, C. postal 2005, Venezuela
(3) Laboratorio de Biologia de Vectores, Instituto de Zoologia Tropical, Universidad Central de Venezuela, Apdo. 47058 Caracas 1041-A, DC
(4) Ministerio de Salud y Prevision Social, Laboratorio de Entomologia Medica, Escuela Tecnica de Salud Boliviano Japonesa, Avenida Ancieto Arce No. 440, Cochabamba, Bolivia
(5) Department of Biological Sciences, Eastern Illinois University, 600 Lincoln Ave., Charleston, IL 61920, USA
TABLE 1. ANOPHELES PSEUDOPUNCTIPENNIS COLLECTION LOCALITIES IN ARGENTINA AND BOLIVIA. Localities Dates Geographical coordinates Argentina Tucuman Province Iltico 13/12/2000 27[degrees]20'05"S 65[degrees]38'55"W El Molino 14/12/1999 27[degrees]19'48"S 65[degrees]42'W Quebrada de Lules 12/12/1998 26[degrees]50'S 65[degrees]40'W Potrero Las Tablas 19/04/1999 26[degrees]51'S 65[degrees]27'W El Cadillal 08/04/2000 26[degrees]36'36"S 65[degrees]12'W Arroyo Molle Yaco 30/04/1999 26[degrees]17'00"S 65[degrees]16'45"W Arroyo Hornillos 22/04/1999 26[degrees]13'S 65[degrees]25'48"W La Sala 29/04/1999 26[degrees]45'S 65[degrees]23'W Salta Province Parque Nacional El Rey 22/02/2000 24[degrees]42'S 64[degrees]37'48"W El Oculto 05/01/2002 23[degrees]06'S 51[degrees]48'W Aguas Blancas 07/01/2002 22[degrees]43'48"S 64[degrees]21'36"W Jujuy Province INTA Yuto 26/10/2005 23[degrees]37'60"S 64[degrees]28'W Lagunita Yuto 26/10/2005 23[degrees]38'22"S 64[degrees]27'11'W Bolivia Cochabamba Department Parque Nacional Carrasco 03/01/1995 16[degrees]58'60"S 65[degrees]7'60"W Santa Cruz Department Taruma 09/12/1991 18[degrees]33'S 63[degrees]4'60"W Localities N (1) Collectors (2) Argentina Tucuman Province Iltico 10 LMA El Molino 10 LMA Quebrada de Lules 1 LMA Potrero Las Tablas 10 LMA and MJDJ El Cadillal 4 LMA, MJDJ and GM Arroyo Molle Yaco 3 LMA Arroyo Hornillos 5 LMA La Sala 10 LMA and MJDJ Salta Province Parque Nacional El Rey 4 LMA El Oculto 10 MJDN, NV and EL Aguas Blancas 10 MJDJ, NV and EL Jujuy Province INTA Yuto 30 MJDJ, NV and EL Lagunita Yuto 11 MJDJ, NV and EL Bolivia Cochabamba Department Parque Nacional Carrasco 31 GNF and RR Santa Cruz Department Taruma 26 GNF and JEC (1) N: number of specimens. (2) LMA: Lucrecia Monica Augier, MJDJ: Maria Julia Dantur Juri, GM: Gustavo Molina, NV: Neri Vianconi, EL: Enrique Laci, GNF: Gary Fritz, RR: Roberto Rodriguez and JEC: Jan E. Conn. TABLE 2. MORPHOMETRICS CONFIDENCE INTERVALS (95% CI) FOR MEASUREMENTS OF PALPOMERES AND BASAL PALE OF AN. PSEUDOPUCTIPENNIS COLLECTED FROM LOCALITIES IN ARGENTINA AND BOLIVIA. Palpomere 1 Palpomere 2 Parque Nacional El Rey 0.178 0.277 0.335 0.562 El Oculto 0.245 0.255 0.445 0.495 Aguas Blancas 0.255 0.281 0.414 0.475 Potrero Las Tablas 0.148 0.206 0.518 0.616 El Molino 0.122 0.146 0.513 0.599 Iltico 0.129 0.159 0.457 0.549 Arroyo Molle Yaco 0.127 0.193 0.372 0.504 El Cadillal 0.030 0.147 0.146 0.726 Quebrada de Lules 0.101 -- 0.506 -- Arroyo Hornillo 0.126 -- 0.435 0.596 La Sala 0.123 0.150 0.516 0.612 INTA Yuto 0.126 0.139 0.508 0.560 Lagunita Yuto 0.103 0.127 0.485 0.530 Parque Nacional Carrasco 0.099 0.116 0.451 0.498 Taruma 0.100 0.109 0.439 0.480 Grenada -- -- 0.200 0.330 Palpomere 3 Palpomere 4 Parque Nacional El Rey 0.688 0.905 0.275 0.382 El Oculto 0.740 0.837 0.379 0.430 Aguas Blancas 0.730 0.823 0.349 0.414 Potrero Las Tablas 0.822 0.936 0.381 0.473 El Molino 0.808 0.906 0.394 0.480 Iltico 0.751 0.877 0.358 0.440 Arroyo Molle Yaco 0.680 0.887 0.355 0.454 El Cadillal 0.155 0.907 0.075 0.506 Quebrada de Lules 0.758 -- 0.379 -- Arroyo Hornillo 0.658 0.859 0.305 0.494 La Sala 0.850 0.955 0.400 0.469 INTA Yuto 0.869 0.889 0.430 0.453 Lagunita Yuto 0.815 0.876 0.400 0.436 Parque Nacional Carrasco 0.680 0.730 0.348 0.376 Taruma 0.658 0.705 0.335 0.364 Grenada 0.320 0.410 0.150 0.220 Palpomere 5 Basal Pale Parque Nacional El Rey 0.228 0.290 0.063 -- El Oculto 0.244 0.267 0.033 -- Aguas Blancas 0.242 0.274 0.106 -- Potrero Las Tablas 0.226 0.319 0.090 0.151 El Molino 0.238 0.273 0.022 -- Iltico 0.232 0.304 0.018 -- Arroyo Molle Yaco 0.237 0.303 0.000 -- El Cadillal 0.053 0.276 0.000 -- Quebrada de Lules 0.253 -- 0.000 -- Arroyo Hornillo 0.189 0.327 0.000 -- La Sala 0.233 0.293 0.000 -- INTA Yuto 0.258 0.293 0.091 0.120 Lagunita Yuto 0.259 0.283 0.071 0.094 Parque Nacional Carrasco 0.208 0.231 0.093 0.107 Taruma 0.204 0.222 0.092 0.102 Grenada 0.080 0.130 -- -- Sector Dark Subcostal Pale Parque Nacional El Rey 2.238 2.640 0.332 0.578 El Oculto 2.155 2.496 0.344 0.419 Aguas Blancas 2.350 2.538 0.351 0.478 Potrero Las Tablas 2.629 3.156 0.325 0.416 El Molino 2.463 2.718 0.374 0.425 Iltico 2.243 2.625 0.342 0.467 Arroyo Molle Yaco 1.736 2.308 0.302 0.389 El Cadillal 1.822 2.725 0.289 0.443 Quebrada de Lules 2.401 -- 0.506 -- Arroyo Hornillo 2.407 2.768 0.339 0.450 La Sala 2.544 2.840 0.334 0.441 INTA Yuto 2.662 2.759 0.384 0.425 Lagunita Yuto 2.543 2.719 0.388 0.430 Parque Nacional Carrasco 2.175 2.274 0.387 0.421 Taruma 2.066 2.246 0.371 0.413 Grenada -- -- 0.070 0.100 Pre-apical Dark Pre-apical Pale Parque Nacional El Rey 0.711 0.919 0.233 0.323 El Oculto 0.805 0.934 0.283 0.344 Aguas Blancas 0.728 0.971 0.289 0.353 Potrero Las Tablas 0.922 1.101 0.254 0.313 El Molino 0.873 0.992 0.267 0.355 Iltico 0.804 0.975 0.272 0.344 Arroyo Molle Yaco 0.549 0.940 0.203 0.269 El Cadillal 0.610 1.038 0.241 0.290 Quebrada de Lules 0.708 -- 0.303 -- Arroyo Hornillo 0.837 1.064 0.208 0.267 La Sala 0.785 1.010 0.238 0.318 INTA Yuto 0.992 1.042 0.262 0.284 Lagunita Yuto 0.929 1.010 0.250 0.301 Parque Nacional Carrasco 0.787 0.832 0.256 0.282 Taruma 0.744 0.824 0.246 0.277 Grenada 0.190 0.250 0.050 0.100 Proboscis Length Parque Nacional El Rey 2.119 2.670 El Oculto 2.046 2.246 Aguas Blancas 1.965 2.195 Potrero Las Tablas 2.303 2.533 El Molino 2.317 2.471 Iltico 2.165 2.420 Arroyo Molle Yaco 1.990 2.273 El Cadillal 0.526 2.710 Quebrada de Lules 2.249 -- Arroyo Hornillo 2.292 2.450 La Sala 2.352 2.607 INTA Yuto 2.305 2.369 Lagunita Yuto 2.181 2.277 Parque Nacional Carrasco 1.905 1.994 Taruma 1.825 1.958 Grenada 0.970 1.130
|Printer friendly Cite/link Email Feedback|
|Author:||Juri, Maria J. Dantur; Liria, Jonathan; Navarro, Juan C.; Rodriguez, Roberto; Fritz, Gary N.|
|Date:||Sep 1, 2011|
|Previous Article:||Influence of saccharum officinarum (poales: poaceae) variety on the reproductive behavior of Diatraea flavipennella (Lepidoptera: Crambidae) and on...|
|Next Article:||A description of the first instar of Matus ovatus (Coleoptera: Dytiscidae).|