Antennal sensilla of triatominae (Hemiptera, Reduviidae): A comparative study of five genera

Pergamon

In!.

J. Insect

Morphol.

& Embryo/,

Vol.

26, No

2, pp.

67-13.

1997

1997 Ekvier Science Ltd Bntain. All rights reserved 0020 7322!97 $17 OO+O.OO

C

PII: SOOZO-7322(97)00014-7

ANTENNAL

Prmted

m Great

SENSILLA OF TRIATOMINAE (HEMIPTERA, REDUVIIDAE): A COMPARATIVE STUDY OF FIVE GENERA

Silvia S. Catala Laboratorio de Insectos Hematbfagos, Facultad de Ciencias Exactas, Fisicas y Naturales, V. Sarsfield 299, Cbrdoba, 5000, Argentina (Received 14 February 1997; accepted 9 June 1997) Abstract-The paper analyses the antenna1 sensilla pattern of 22 species of triatomine bugs (Hemiptera, Reduviidae). The pedicels of species from tribe Rhodniini differ from species of Cavernicolini and Triatomini, mainly by the absence of trichoid and basiconic sensilla and by a greater number of Bristles I. Fifth-instar nymphs of T. sordida and R. pictipes show several differences in sensilla patterns compared with their respective adults. They lack basiconic sensilla and thin-and thick-walled trichoid sensilla over the first flagellar segment and over the proximal half of the second flagellar segment. T. sordida nymphs also lack these sensilla on the pedicel. There appears to be a significant sexual dimorphism in relation to trichoid sensilla in T. sordida, but not in R. pictipes. There exists a remarkable correlation between the density of basiconic and trichoid sensilla on the pedicels of different species, and a crude estimation of habitat range assessed as number of habitat types reported for each species. G 1997 Elsevier Science Ltd Index descriptors (in addition to those in the title): Sensilla patterns; chemoreceptors; Chagas disease; Pansfrongylus megisius; Panstrongylus lignarius; Triatoma mazzotti; Triatoma dimidiata; Triatomaguasayana; Triatoma infestans; Triatoma tibiamaculata; Triatomaprotracta; Triatomaspinolai; Triatomasordida; Triatoma rubrofasciata; Triatomapatagonica; Triatomapseudomaculata; Triatoma vitticeps; Triatoma rubida; Triatoma sanguisuga; Triatoma platensis; Triatoma delpontei; Triatoma brasiliensis; Dipetalogaster maxima; Cavernicola lenti; Rhodnius pictipes.

INTRODUCTION

As obligate bloodsuckers, the Triatominae (Hemiptera, Reduviidae) have considerable importance in Latin America. Well over 100 species have been described, arranged into 14 genera and 5 tribes (Lent and Wygodzinsky, 1979; Schofield, 1994). Most of them occupy silvatic habitats, associated with a range of small mammals, birds and, in some cases, reptiles. Several are also able to colonise peridomestic and domestic habitats, assuming epidemiological significance as vectors of Trypanosoma cruzi, causative agent of Chagas disease or American trypanosomiasis. The 5 nymphal stages and both sexes of adult Triatominae are equipped with a pair of 4-segmented antennae bearing an array of different sensilla. These structures are important in the relationship between a bug and its environment, and can be expected to reflect an ancestral pattern overlaid by adaptive features related to specific habitat and behavioural characteristics (Chapman, 1982). Aspects of the morphology and function of antenna1 se&la of 2 triatomine species, Rhodnius prolixus and Triatoma infestans, have been examined by several authors (Wigglesworth and Gillett, 1934; Barth, 1952; Mayer, 1968; Bernard, 1974; McIver and Siemicki, 1984, McIver and Siemicki, 1985; Lazzari, 1990) and more detailed description of the antenna1 sensilla in the genus Rhodnius has been provided by Catala and Schofield (1994). The aim of the present work was to extend our comparative knowledge of the antenna1 arrays in a wider number of triatomine species, and to examine

the extent to which the sensilla patterns could be related to habitat specificity.

MATERIALS AND METHODS Available for this comparative study were adults of 22 species of Triatominae, together with fifth-stage nymphs of Triatoma sordida and Rhodnius pictipes representing the 2 most important genera. All bugs were from laboratory colonies as indicated in Table 1. For scanning electron microscopy (SEM) antennae were cut from the head through the base of the scape and laid on a small piece of plastazote. An SEM stub coated with araldite was laid on its side on an appropriately shaped piece of plastazote and brought into contact with the cut end of the scape. The preparation was allowed to dry overnight and then sputter-coated with 3 layers of gold-palladium and examined by SEM; the segments were photographed over 4 equal quadrants (outer, inner, upper and lower). To orientate each preparation we used 3 features of the pedicel common to all species: the presence of trichobothria exclusively on the upper surface, the presence of a deep median groove at the tip of the lower sector, and the presence of the cave organ (Barth, 1952; Catala, 1994) on the outer sector. The different types of sensilla were classified and counted from the electron micrographs. The pedicel and both segments of the flagellum were analysed for T. infestans, T. sordida, T. guasayana and R. pictipes. From the other species, only the pedicel was considered.

RESULTS

Sensilla types

Analysis of sensilla patterns showed that the types of sensilla present for all species were essentially the same morphological types described for the 2 genera of the tribe Rhodniini (Rhodnius and Psammolestes) by Catala and Schofield (1994). Because the species studied here

S. S. Catala

68 Table Servicio National

de Chagas,

Institute

Cruz, Rio de Janeiro,

Natural

Oswald0 History

Dr M. Lehane,

Museum, Bangor

Cordoba,

London,

University,

1.List of species and their sources (museums and or individuals)

Argentina Brazil

UK Wales, UK

included representatives

Panstrongylus megistus, P. lignarius, Rhodnius pictipes, Triatoma sordida, T. mazotti, T. dimidiata, T. guasayana, T. infestans Cavernicola lenti, Triatoma tibiamaculata, T. protracta, T. spinolai, T. sordida, T. rubrojksciata, T. patagonica, T. pseudomaculata, T. vitticeps, Rhodnius pictipes Dipetalogaster maxima, Triatoma rubida, T. sanguisuga, T. platensis, T. delpontei, T. brasiliensis Triatoma infestans

of 4 other genera (Triatoma, and Cavernicola) representing 2 other tribes (Triatomini and Cavernicolini), we expect that the types of sensilla described (Fig. 1; Table 2) probably encompass all sensilla types on the antennae of Triatominae. Using the classification of Altner and Prillinger (1980) we categorise the sensilla Dipetalogaster,

Panstrongylus

types as follows: NP-FS: No pore sensilla in flexible sockets (includes trichobothria, tapered hairs, sensilla campaniformia, and 3 types of bristles); NP-IS: No pore sensilla with inflexible sockets (sensilla coeloconica), and WP-IS: Wall pore sensilla with inflexible socket (includes basiconic sensilla and 2 types of trichoidea) In general, the distribution of NP-IS sensilla was simi-

1. (a) Panstrongylus megistus pedicel showing bristles 1 (B), tnlck (lk)- and thm (I’h)-walled trichoid and basiconic sensillum (Bs) x 1000. (b) Triutoma rubrofasciata pedicel with bristles 1, thin-walled trichoidea, campaniformia (Cp) and coeloconica (Co) sensilla. x 200. (c) Triutoma sordida first flagellar segment from a fifth-stage nymph holding bristles I and coeloconic sensilla. No trichoid and basiconic sensillum had been observed as in adults (d).

Antenna1

Sensilla of Triatominae

Table 2. Sensilla types on Triatominae Group

Sensillum

No pore se&la sockets NP-FS

in flexible

69 antennae

Morphology

Trichobothria

Function

Long and slender hairs inserted large cup-like depressions

in

Mechanoreception Innervated neurone’”

by a single bipolar

Bristles I

Stout bristle set in a double rimmed socket. Thick walls with grooves. Tubercles on the tip

Mechanoreception innervated single bipolar neurone’”

by a

Bristles II

Straight and long bristles. Sockets are less developed than in Bristles I.

Mechanoreception innervated single bipolar neurone”’

by a

Bristles III

Bristles with socket and a short and straight shaft.

Mechanoreception?

Tapered

Hairs with tapered

Propriocetion? Monitoring antenna1 movements

hairs

conical shaft.

Campaniformia

Oval domes surrounded cuticle.

No pore sensilla with inflexible socket (NP-IS)

Coeloconica

Pegs set in the floor of shallow pits

Thermohygroreceptors innervated by 3 neurons with unbranched dendrites.“,4,5’

Wall pore sensilla with inflexible socket (NP-IS)

Basiconica

Pegs with a grooved surface

Thermo-hygro and chemoreception’4’ innervated 5-6 neurons’@

(1) Altner and Prihinger, and Gillet.

1934; (7) Mayer,

and porous

Proprioception? cuticular stress

Monitoring

Trichoidea

thin-walled

Long hairs with blunt tip and a highly porous surface.

Chemoreception I5 neurons.

Trichoidea

thick-walled

Similar to the thin-walled but more slender and tapered to a fine tip. No visible pores on the surface but permeable to dyes”’

Pheromones receptors? 14’ innervated by 5-6 neurons@’

1980; (2) McIver and Siemiki, 1984; (3) McIver and Siemiki, 1985; (4) Bernard, 1968.

Adult sensilla patterns

Comparison of the sensilla patterns on the 3 distal segments of the antennae of 3 species of Triatoma (Table 3) and 6 species of Rhodnius studied by Catala and Schofield (1994) indicates no significant difference in total sensilla density for the 2 flagellar segments (ANOVA, p>O.Ol). In contrast, the 2 genera show marked differences in sensilla density on the pedicel, due mainly to the absence of trichoid and basiconic sensilla as well as a greater number of type 1 bristles on the pedicel of Rhodnius (Fig. 2). The antenna1 flagellum of Rhodnius shows a fairly homogeneous distribution of sensilla over the 4 quadrants (Catala and Schofield, 1994) and the flagellum of (in 104pm2) on pedicel and both segments

1974; (5) Lazzari.

by

I’.” innervated

1990: (6)

by

Wigglesworth

Triatoma shows a broadly similar picture. In Triatoma however, and in other representatives of the Triatomini, there is a tendency for greater accumulation of trichoid and basiconic sensilla over the inferior face of the pedicel (Fig. 3). All the Triatomini and Cavernicolini species have thinwalled trichoid sensilla on the pedicelus but thick-walled trichoid and basiconic sensilla are not always present. Some species (Triatoma platensis, T. spinolai, T. rubrofasciata, T. infestans and T. protracta) lack the thickwalled trichoid and basiconic sensillum. Triatoma maculata and T. mazzottii do not have the basiconic type on the pedicel and T. brasiliensis lacks the thick-walled trichoid type. Adults of Cavernicola lenti, one of the 2 recognised species of the tribe Cavernicolini, shows sensilla patterns similar to those of the Triatomini, with the pedicel showing basiconic sensilla and both types of trichoid sensilla. In contrast, adults of T. spinolai show several different antenna1 characteristics: the pedicel

lar in all species studied, but major differences were found in the patterns of type 1 bristles, and the 3 types of WPIS sensilla, which are presumed to be mainly chemoreceptors (see below).

Table 3. Sensilla density

by a ring of

of Triutoma infesfans, T. sordida; T. guasayana flagellum

(ALL females)

sP

BI

Tth

Ttk

Bas

BII

Flagellum I Tth Ttk

Bas

BII

Flagellum11 Ttk Tth -_____

Bas

sor gua mf

3.35 2.92 3.13

2.01 1.8 0.49

1.39 0.2 0

0.08 0.08 0

1.01 0.25 1.26

5.93 2.63 4.96

3.87 9.52 1.49

0.99 1.03 1.28

5.16 4.82 3.22

6.19 8.06 3.22

Pedicel

25.5 18.2 18.1

29.9 23.4 23.81

Bas = basiconica; BI = bristles I; BII = bristles II; gua = Triatoma guasayana; inf = Triatoma infestans; sor = Triaroma sordida; sp = species; Tth = trichoidea thin-walled; Ttk = trichoidea thick-walled. All values are means from 3 specimens.

S. S. Catala

70 6

of both species lack basiconic sensilla and thin- and thickwalled trichoid sensilla over the first flagellar segment and over the proximal half of the second flagellar segment. These sensilla are also absent from the pedicel of T, sordida nymphs.

m Rhodnius 0

Triatoma

n

BI

Tth

Ttk

Bas

Sensillum type Fig. 2. Mean sensilla density (Bas= basiconic, BI = bristles I, Tth= trichoid thin-walled, Ttk = trichoid thick-walled) on pedicel of Rhodnius and Triatoma.

shows no basiconic sensilla, but is equipped with very long bristles and scarce-but also unusually long-trichoid sensilla (especially in males) (Fig. 4). Using T. sordidu and R. pictipes for more detailed analysis, there appears to be significant sexual dimorphism in relation to trichoid sensilla in T. sordidu, but not in R. pictipes. On the pedicel, female T. sordida show a significantly greater density of thick-walled trichoids, whereas males show a higher density of thin-walled trichoids (Table 4). Nymphal sensilla patterns

Fifth-instar nymphs of T. sordida and R. pictipes show several differences in sensilla patterns compared with their respective adults (Table 5). Although overall sensilla density on the second flagellar segment does not differ between adults and their respective nymphs, the nymphs “P 2%

Fig. 3. Proportion of trichoid and basiconic sensilla over the pedicel surface on Triatomini. The values are means from all the Triatomini studied.

DISCUSSION difference in sensilla

patterns between nymphs and adults of T. infestans has been noted by Bernard (1974) who drew attention to the absence of basiconic and trichoid sensilla on the pedicel and first flagellar segment of nymphs, and to the increased number of trichobothria on the adult antennae. We have confirmed this for several other species of Triatominae, and also noted that another receptor known as the cave organ is present on the pedicel of adults but not nymphs (Catal& 1994; Catala and Schofield, 1994). These observations are in accord with a general tendency in insects to increase the number of receptors in the adult stage, particularly chemoreceptors, such as basiconic and trichoid sensilla. As suggested by Chapman (1982), it seems likely that the increase in chemoreceptors in the adult stage would reflect additional sensorial requirements of the adults, such as those related to reproduction and active dispersal by flight. Electrophysiological studies on the basiconic sensilla of adult T. infestans indicated responses to heat, humidity, and aromatic acids, and the thin-walled multiporous trichoids respond to human breath (Mayer, 1968) as well as to pyruvate, lactate, and amyl acetate (Bernard, 1974). However, the thick-walled trichoids showed no response to humidity or to thermal or chemical stimuli, leading Bernard (1974) to suggest that they may respond only to special compounds such as pheromones. In Cimex lectularius, the morphologically similar E2 trichoids have been identified as receptors of the alarm pheromone of this species (Steinbrecht and Mtiller, 1976) Sexual differences in the density of both types of trichoid sensilla on the pedicel of T. sordida are also suggestive of a function related to reproduction. The thin-walled trichoids are more abundant in males, while the thickwalled trichoids are more abundant in females. Sexual differences in receptor patterns are quite common in other insects such as mosquitoes, where males and females have different feeding habits, or in moths such as Bombyx mori which have powerful sex pheromones (McIver, 1982). In the case of Triatominae however, both sexes of adults, and all nymphal stages, generally have similar feeding habits, and sex pheromones have not been clearly demonstrated (Schofield, 1979). An aggregation pheromone has been demonstrated in T. infestans (Schofield and Patterson, 1977) and there is evidence of a possible sex pheromone in R. prolixus, where males are sometimes attracted to copulating pairs (Baldwin et al., 1971). A similar effect has occasionally been observed in T. infestans (C. Lazzari, personal communication). The transitional

Antenna1

Sensilla of Triatominae

71

Fig. 4. Triaroma spinolai pedicel from a female (a) and a winged male (b). No trichoid or basiconic sensilla have been observed female pedicel but a few unusually large trichoid (T) are present on the male (winged or not) pedicel x 200.

Table 4. Sensilla density (in IO4 pm*) on pedicel and both segments

of Triatoma

Pedicel SP T.s. male Ts fern T.s. nph R.p. male R.p. fern R.p. nph

on

sordida and Rhodnius pictipes flagellum

BI

Tth

Ttk

Bas

BII

Flagellum I Tth Ttk

Bas

BII

Flagellum Tth -

II Ttk

Bas

3.25 3.25 2.49 4.34 4.18 3.87

4.17(*) 2.01 (*) 0 0 0 0

0.63(**) 1.43(**) 0 0 0 0

0.24 0.08 0 0 0 0

1.03 1.01 0.52 2.06 2.15 3.87

5.42 5.93 0 9.92 8.3 0

4.38 3.87 0 3.72 3.2 0

0.99 0.99 0.5 2.23 2.09 1.24

4.9 5.16 4.9 7.94 7.0 1 4.12

31 29.9 31.2 20.8 18.2 15.4

4.9 6.19 5.42 7.42 7.79 7.99

26.8 25.5 0 16.3 17.5 0

Bas = basiconica; BI = bristles I; BII = bristles II; fern = female; nph = nymph V stage; R.p. = Rhodnius pictipes; sp = species; T.s. = Triatomn sordida; Tth = trichoidea thin-walled; Ttk = trichoidea thick-walled. All values are means from 3 specimens.* and ** differ significantly between species.

Table 5. Characteristics

of the adult antennae

Pedicel Adults

Sensilla Trichoid

and basiconic

Triatomini Trichobothria Cave organ

present

Rhodniini

Nymphs absent

and the fifth-stage

antennae

Flagellum I Nymphs Adults

absent

present

absent

absent

present

absent

present

5 to 8 on upper face one in external face

reduced to one absent

Nevertheless, whereas R. prolixus and T. infestans are well known as domestic species, often building up colonies of several thousand bugs in a single dwelling, T. sordida tends to occupy silvatic and peridomestic habitats at much lower population densities (Schofield, 1994). Moreover, T. sordida appears to have a much greater capacity for active flight compared with T. infestans (Schofield et al., 1991. 1992) so that it may have greater need for

of Triatominae Flagellum

II

Adults

Nymphs

present

restricted to the distal half restricted to the distal half

a system of sexual recognition to facilitate encounters between dispersing adults. It may be that the need to identify habitats during active adult dispersal is a key factor in determining the sensilla patterns on adult antennae (cf. Chapman, 1982). This would explain the abundance of basiconic and trichoid sensilla on the pedicel of T. sordida, compared with other species of the tribe. In contrast, species adapted to

72

S. S. Catala

4 :

:

e

0

4 4

4

4

4

4

0

4

I

I

I

2

4

6

Habitat Fig. 5. Relationship

between sensilla density (trichoid

+ basiconic)

a limited range of habitat types, such as T. infestans, which is almost exclusively domestic, and T. protracta, which is almost exclusively associated with nests of packrats (Neotoma spp), show considerable reduction in the density of these types of sensilla. At the extreme, T. spinolai-whose females and most males are invariably apterous-shows very few trichoids and an absence of basiconic sensilla on the pedicel. This idea is reinforced by the remarkable correlation between the density of basiconic and trichoid sensilla on the pedicel of different species, and a crude estimation of habitat range assessed as number of habitat types reported for each species (r=0.777; p
range on pedicel and habitat

range of 17 Triatomini

species.

Acknowledgenzenrs-Special thanks are due to Dr C. J. Schofield for criticisms and fruitful discussions as well as for revision of the manuscript, to the Institutions that provided specimens, and to Natural History Museum (Medical Entomology and Electron Microscopy) where the work was carried out. The project received financial support from CONICOR, British Council, SECYT, Universidad National de

Cbrdobaand ECLAT,

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