Ultrastructure of the Antennae and Sensilla of Nyssomyia intermedia (Diptera: Psychodidae), Vector of American Cutaneous Leishmaniasis

Abstract

The antennal sensilla and the antenna of females Nyssomyia intermedia, one of the main vectors of American cutaneous leishmaniasis, were studied by scanning electron microscopy. The main goal was to characterize the quantity, typology, and topography of the sensilla with particular attention to the olfactory types. The insects were captured in the city of Corte de Pedra, State of Bahia, Brazil, by CDC-type light traps and raised in a laboratory as a new colony. Fourteen well-differentiated sensilla were identified, among six cuticular types: trichoidea, campaniformia, squamiformia, basiconica, chaetica, and coeloconica. Of these, six sensilla were classified as olfactory sensilla due to their specific morphological features. Smaller noninnervated pilosities of microtrichiae type were also evidenced by covering all antennal segments. The antennal segments differ in shapes and sizes, and the amount and distribution of types and subtypes of sensilla. This study may foment future taxonomic and phylogenetic analysis for a better evolutionary understanding of the sand flies. Besides, it may assist the targeting of future electrophysiological studies by Single Sensillum Recording, and aim to develop alternative measures of monitoring and control of this vector.

Keywords: Phlebotominae; sand fly; scanning electron microscopy; sense organs; sensillary typology.

Fig. 1.

Electron micrographs of the antennae of females Nyssomyia intermedia. (A) Latero-internal view of the antennae of the showing the first two segments: scape (S) and pedicel (P), with short sharp-tip trichoid (st), arranged in a set of two on the scape and a set of three on the pedicel, long blunt-tipped trichoid (bt) sensilla, next to some ommatidia (om) of one of the sandfly´s compound eyes; and squamiform sensillum (sq; scale bar = 28.2 µm). (B) Latero-external view of the scape and pedicel showing short sharp-tip trichoid (st), arranged in a set of two on the Scape (S) and in a set of three on the pedicel (P; scale bar = 10.4 µm). (C and D) Short sharp-tip trichoid (st) observed in higher magnification on the scape ([B] circle area) and pedicel (B box area), respectively, and microtrichia (m) covering all the surface of these antennal segments (scale bars = 3.9 µm, both). (E) Dorsoexternal view of antenna showing the scape (S) with a set of three short sharp-tip trichoid (st) (scale bar = 6.8 µm). (F) Two campaniform sensilla, surrounded by microtrichia (m), laterally observed on the Pedicel (P; scale bar = 2.6 µm). (G) Higher magnification of one campaniform sensillum (scale bar = 1.3 µm).

Fig. 2.

Scanning electron micrographs of the flagellomeres of females Nyssomyia intermedia. (A) Flagellomere I showing long blunt-tipped trichoid (bt), and squamiform sensilla (sq; scale bar = 20 µm). (B) Higher magnification showing two squamiform sensilla (s), and microtrichia (m; scale bar = 10 µm). (C) Box area showing squamiform (sq), basiconic (b), and short blunt-tip trichoid (sb) sensilla, in higher magnification, besides microtrichia (m; scale bar = 10 µm). (D) The same sensilla in higher magnification (scale bar = 5 µm). (E) Flagellomere VI showing long blunt-tipped trichoid (bt) and chaetic (ch) sensilla, and microtrichia (m; scale bar = 20 µm).

Fig. 3.

Electron micrographs of the flagellomeres of females Nyssomyia intermedia. (A) Flagellomere XI showing long blunt-tipped trichoid (bt), short prominent-base trichoid (sp), and chaetic sensilla, single-base subtype (ch; scale bar = 20 µm). (B) Box area showing long blunt-tipped trichoid (bt), and short prominent-base trichoid (sp; scale bar = 6.35 µm). (C) Higher magnification of the antennal flagellomere V showing a base of a chaetic sensillum, single-base subtype (ch), with the cuticle perforated with wall pores (po), and microtrichia (m; scale bar = 1.8 µm). (D) Flagellomere I showing chaetic sensillum, forked-base subtype (ch_fb), and of grooved coeloconic sensillum, palmately lobed subtype (gc_pl; scale bar = 14.6 µm). (E) Higher magnification of the antennal segment showing grooved coeloconic (gc) sensillum, palmately lobed subtype, with structures fused at its base, but distally lobed, arranged around its inner cone, which has longitudinal wall grooves (lg); and microtrichia (m; scale bar = 4 µm).

Fig. 4.

Scanning electron micrographs of the flagellum of females Nyssomyia intermedia. (A) Flagellomere XIII showing implantation sites of common grooved coeloconic sensilla (gc), a short prominent-base trichoid (sp) sensillum, chaetic sensilla, single-base subtype (ch), long blunt-tipped trichoid (bt), and medium pointed-tipped trichoid (pt) sensilla (scale bar = 10 µm). (B) Three common grooved coeloconic sensilla (gc), surrounded by microtrichia (m) on flagellomere XII, beyond the base of implantation of two medium pointed-tipped trichoid (pt) sensilla, the apex of two long blunt-tipped trichoid (bt) sensilla (scale bar = 10 µm). (C) Flagellomere XII in higher magnification sowing a common grooved coeloconic sensilla (gc), showing longitudinal wall grooves (lg), surrounded by microtrichia (m; scale bar = 5 µm). (D) Last antennal flagellomere (XIV) showing long blunt-tipped trichoid (bt), medium pointed-tipped trichoid (pt), grooved coeloconic (gc) sensilla, short fixed-base sensilla (sf), and the apical trichoid sensillum (ap; scale bar = 10 µm). (E) The apex of the last flagellomere in higher magnification showing medium pointed-tipped trichoid (pt), long blunt-tipped trichoid (bt), short fixed-base sensilla (sf), and the apical trichoid sensillum (ap; scale bar = 5 µm).

Fig. 5.

Number and size of the antennal segments of Nyssomyia intermedia females and of some of their antennal sensilla (P < 0.05). (A) Dimensions of the antennal segments. (B) Dimensions of the single-base chaetic sensilla found on different subsegments of the antenna. (C) The total number of sensilla observed on the antennal segments (D) Number of long blunt-tipped trichoid sensilla found on antennal segments. (E) The number of medium pointed-tipped trichoid sensilla found on the last three antennal subsegments. (F) Number of common grooved coeloconic sensilla located on the last three antennal subsegments.