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259–268 (2011) Tropical Biomedicine 28(2): 259–268 (2011) Morphometric and meristic characterization of Phlebotomus argentipes species complex in northern Sri Lanka: evidence for the presence of potential leishmaniasis vectors in the country Gajapathy, K.*, Jude, P.J. and Surendran, S.N. Department of Zoology, Faculty of Science, University of Jaffna, Jaffna 40000 * Corresponding author email: [email protected] or [email protected] Received 20 September 2010, received in revised form 6 January 2011; accepted 14 January 2011 Abstract. The transmission of cutaneous leishmaniasis (CL) is of public health concern in Sri Lanka. The parasite Leishmania donovani is reported to be the causative agent for CL in Sri Lanka. However there is no report on the vector of CL in the country. Phlebotomus argentipes sensu lato is the well known vector of L. donovani which causes visceral leishmaniasis (VL) in the nearby South India. The taxon Ph. argentipes previously reported to occur as a species complex comprising of two morphospecies namely A and B. The taxonomy of the Argentipes complex was reassessed recently and reported to have three species viz. Phlebotomus glaucus, Ph. argentipes sensu stricto and Ph. annandalei. A study was carried out in Jaffna mainland, where three CL patients have been recorded, and two associated islands in northern Sri Lanka to record the presence of the members of the Argentipes complex. Sandflies were collected using human landing and cattle baited collections. Collected samples were analyzed based on reported morphometric and meristic characteristics. The study revealed the presence of all three members of the complex in which Ph. glaucus and Ph. argentipes s.s. are reported for the first time in Sri Lanka. INTRODUCTION as the parasite responsible for CL in Sri Lanka (Karunaweera et al., 2003). However in India, Leishmaniasis was considered as an exotic L. donovani is associated with VL and the disease for decades in Sri Lanka (Navaratna vector is Phlebotomus (Euphlebotomus) et al., 2007) until the first autochthonous case argentipes Annandale & Brunette, 1908 of cutaneous leishmaniasis (CL) which was (Diptera, Psychodidae) (Ilango, 2000). identified in 1992 (Athukoralle et al., 1992). Phlebotomus argentipes s.l. (sensu lato) Since then, the number of cases identified has is suspected as a potential vector of CL in Sri increased dramatically. More than 400 cases Lanka. It shows geographic variation which were identified for CL from 2001 to 2005 is associated with several morphological (Siriwardana et al., 2007). Around 2000 cases characteristics (Lane, 1988). The best have been reported in the last eight years described of these is the difference in the from different parts of the country including length of the sensilla chaetica (s. chaetica, the northern Jaffna Peninsula where three CL previously known as the antennal ascoids; patients have been recorded (Siriwardana Ilango, 2000) on antennal flagellomere II et al., 2010). The first case of visceral (Ilango et al., 1994; Ilango, 2000). The leishmaniasis (VL) was identified from North morphology of s. chaetica has previously Central Province of the country in 2006 been used to differentiate sandfly species (Abeygunasekara et al., 2007). Leishmania (Lane & Fritz, 1986). The length of the s. donovani zymodeme MON -37 is identified chaetica appears to correlate with VL 259 distribution; sandflies from VL-endemic areas Leishmaniasis is emerging as an in India have short s. chaetica (less than half important vector-borne disease in Sri Lanka the length of the flagellomere which they are (Nawaratna et al., 2007). One of the options attached to) whereas sandflies from non- to control the disease transmission is to endemic areas have longer s. chaetica. implement an optimum vector control Sympatric populations have also been measure. The perfect identification of vectors recorded in India (Ilango et al., 1994). As a and establishment of their bionomics are result of this and other studies (such as important for a successful vector control variation in cuticular hydrocarbons, programme when the vector taxon exists as Kamhawi et al., 1992), it has been suggested a species complex. Presence of two or more that Ph. argentipes s.l. exists as a species sibling species in a particular area would complex. conceal the real transmission pattern of the Previously the species complex was disease and lead to inaccurate assessment described to be composed of two in the vector control programme. morphospecies, viz. A and B based on the With this background and considering length ratio of s. chaetica and second the recent taxonomic reassessment, the antennal flagellomere (Ilango, 2000). The morphometric characters of the Ph. populations with long s. chaetica in the argentipes sandflies from northern Sri Lanka second antennal flagellomere (more than were studied and the results are reported in 50% of the length of the flagellomere II) were this article. referred as morphospecies A and those with short s. chaetica (less than 50% of the length of the flagellomere II) as morphospecies MATERIALS AND METHODS B (Ilango, 2000). The presence of morphospecies B is associated with CL Sandfly collection endemic areas in India (Ilango, 2000). Phlebotomine sandflies were collected Although presence of Ph. argentipes s.l. using human landings catches (HLC) and was reported for many years in Sri Lanka cattle baited collection (CBC) techniques. (Carter & Antonipulle, 1949; Lewis, 1978; Samplings were done with a mouth aspirator Lane et al., 1990), the absence of any form of from 1900 – 0100 hrs during the period leishmaniasis was related to the zoophagic between January and April 2010 from three nature of the sandfly populations in the locations namely Delft island (9 º 28’ 60 N 79º country. However Surendran et al. (2005a) 40’ 0” E), Pungudutheevu (9º 34’ 60” N, 79º 47’ reported the presence of anthropophagic and 60” E) and Chunnakam (9º 45’ 0 N, 80º 1’ 0” E) zoophagic Ph. argentipes s.l. populations on in the northern province of Sri Lanka (Fig. 1). Delft island of northern Sri Lanka and later Samples were collected on a monthly basis reported the presence of both morphospecies and collected samples were brought to A and B in the country (Surendran et al., Zoology Laboratory of the University of 2005b). However, the taxonomy of Ph. Jaffna. Sandflies were categorized according argentipes species complex was reassessed to the collection site, host (human or cattle), recently (Ilango, 2010) and reported to be and sex. Phenotypic characters such as composed of three members namely Ph. colour and size of the flies were recorded and argentipes sensu stricto Annandale & coded accordingly. Phlebotomine sandflies Brunette 1908, Phlebotomus glaucus Mitra were identified using published keys of Lewis & Roy 1953 and Phlebotomus annandalei (1978) and Lane (1993). The collected flies Sinton 1923 after considering the relative were preserved in 70% ethyl alcohol for later length of s. chaetica compared to that of the analysis. antennal flagellomere in the second antennal flagellomere, wing index, wing overlap and Morphometric and meristic analysis the length of the common spermathecal duct Whole specimens were temporarily mounted for females and the gonocoxite and gonostyle in distilled water to study the morphometric ratio for males based on statistical analysis. and meristic characteristics. The flies were 260 tibial and basitarsal segments of each appendages, abdomen, coxa and style (clasper), paramere, aedegal sheath, genital pump and aedegal filament was done with the ocular micrometer and the number of teeth found in both ventral and lateral sides of the maxillae were counted under the light microscope equipped with a camera (Olympus Model BX 51, Japan). Analysis of data The wing index (R 2/R 2+3), wing overlap (R1 overlap/ R2) and the ratios between wing length and width, second s. chaetica and AFII, (AFIII+AFIII) and AFI, gonocoxite and gonostyle, genital pump and aedegal filament, length of head and eye, length of appendage segments of each thoracic appendage, and maxillary palp segments were calculated and recorded. Species were recognized primarily according to published keys (Ilango, 2010) and their characteristics were then analyzed separately. The selected morphometric parameters were analyzed using Student’s t-test (Microsoft Office Excel Figure 1. Collection sites in northern Sri Lanka 2003, USA) and compared with the published (D – Delft, P – Pungudutheevu, C – Chunnakam) description for the members of the Argentipes species complex (Ilango, 2010). Principal component analysis (PCA) was performed for observed under a stereo microscope (Kyowa males and females separately. The log Model SE- L, Japan) and a monocular light transformed values of the measured microscope (Kyowa, Japan) equipped with a morphometric characters were used. moving Vernier scale and an ocular Covariance matrix based PCA was performed micrometer. Permanent mounting of the using Minitab software (Minitab Release whole specimen were done for some flies in 14.12.0). Eigen values and proportions Canada balsam after alcohol treatment (Ko, (variability) were obtained for the first 5 2008). principal components. Photographs of the morphometric structures like the wing veins, genitalia, Identification of members of the mouth parts and appendages were taken with Argentipes complex the Nikon Coolpix Digital Camera fixed to Members of the Argentipes complex were the microscopes. Camera Lucida was used identified based on the descriptions of to draw images of the structures like sensilla Ilango (2010). Female flies were identified chaetica in some specimen, and mainly for according to the ratio of SCII/AFII: for the assessment of the teeth of the maxilla and Ph. annandalei, Ph. argentipes s.s., and for the dimension of spermathecae. The Ph. glaucus the ratio is <0.4, 0.4< >0.5, and measurement of the structures such as wing >0.7 respectively (Fig. 2). Male flies were (length and maximum width), wing venation identified based on the ratio between (Radial (R) R2, R 3, R 2+3 and R Overlap), gonocoxite and gonostyle: for Ph. glaucus, length of halter, lengths of head, eye, labium, Ph.
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