Phlebotomine Sandflies in Venezuela: Review of the verrucarum Species Group (in Part) of Lutzomyia (Diptera: Psychodidae) with Description of a New Species from Lara M. DORA FELICIANGELI, CONRADO ARREDONDO,1 AND RICHARD WARD2 Facultad de Ciencias de la Salud, BIOMED, Universidad de Carabobo, Nucleo Aragua, Maracay, Venezuela

J. Med. Entomol. 29(5): 729-744 (1992)

ABSTRACT The series townsendi and verrucarum of the verrucarum species group of the phlebotomine genus Lutzomyia Franca are reviewed. Lutzomyia nadiae, new species, from the mountains of Yacambu, Lara State, is described. Distribution maps, illustrated keys, notes on medical importance, taxonomy, and ecology are presented for species in these series known from Venezuela. KEY WORDS Insecta, Lutzomyia verrucarum group, taxonomy, general review

(1965) DEFINED THE Lutzomyia verrucarum group as those species that possess striated, saclike spermathecae and male genitalia with a basal tuft on the coxite and a simple paramere. Within the group, Theodor (1965) recognized two series: serrana and verrucarum. The males in the serrana series (=subgenus Pifanomyia Ortiz & Scorza, 1963), as defined by Barretto (1962) and Martins et al. (1978), have three large spines on the style (two distal and one basal), whereas those in the verrucarum series have four spines. Recently, the verrucarum series was divided into two series by Kreutzer et al. (1990): the townsendi series, which included males with an isolated basal spine and three distal spines on the style; and the verrucarum series, which included males with two paired basal spines on the style of the terminalia. Most females of the townsendi species complex are isomorphic and are therefore impossible to distinguish using morphological criteria. At present, there are three species in the series serrana known to exist in Venezuela: Lutzomyia serrana (Damasceno y Causey, 1949), L. ottolinai (Ortiz & Scorza, 1963), and a third species closely related to L. odax (Fairchild & Hertig, 1961). L. serrana is not abundant and has a patchy distribution in western Venezuela (Zulia, Trujillo, Tdchira, Merida, Apure, and Barinas States) and in southeastern Bolivar State (Feliciangeli 1988). L. ottolinai is known only from its type locality, Rancho Grande, THEODOR

1 Facultad de Medicina, Universidad Centro-Occidental "Lisandro Alvarado" Barquisimeto, Venezuela. 2 Department of Medical Entomology, Liverpool School of Tropical Medicine, Liverpool, U.K.

Aragua State, where, in spite of numerous collections, only three females were caught. Unfortunately, the type material is no longer available for study. In La Gran Sabana, Bolivar State, two males were collected which were identified temporarily as L. odax. However, more specimens are needed to confirm the presence of this sandfly in Venezuela. Consequently, because of the shortage of material in the serrana series, the present revision of Venezuelan sandflies in the verrucarum group is restricted to species in the townsendi and verrucarum series. Medical Importance. The verrucarum group is of special interest because most species are highly anthropophilic (Young 1979). Lutzomyia verrucarum (Townsend, 1913) was the first taxon described in this group and also the first to be incriminated as a vector of bartonellosis in Peru. In Venezuela, there is strong evidence that L. youngi Feliciangeli & Murillo, 1987, previously misidentified as L. townsendi in the Andean region, is the vector of cutaneous leishmaniasis in that area, although the identification of the Leishmania species is still not completely clear. Scorza et al. (1984a) reported the natural infection of L. youngi (cited as L. townsendi) with Leishmania braziliensis Vianna, 1911) in the suburban area of the city of Trujillo. Experimental transmission of Leishmania garnhami (Scorza et al. 1979) by L. youngi (=L. townsendi) was achieved by Scorza & Anez (1984). Carnevali & Scorza (1976) infected L. youngi (cited as L. townsendi) with Leishmania braziliensis sensu latu from Carabobo State. This parasite was later identified as Leishmania mexicana amazonensis (Scorza et al. 1979).

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L. youngi also was infected experimentally with Leishmania braziliensis from Trujillo State (Scorza & Delgado 1982) and with Leishmania garnhami from M6rida State (Moreno & Scorza 1981, Anez et al. 1985). L. youngi also is suspected of transmitting Leishmania (V.) panamensis in Costa Rica (R. Zeled6n, personal communication). Lutzomyia spinicrassa Morales, Osorno, Osorno, and Hoyos, 1960) is the most common human-biting species in Arboledas, Norte Santander, Colombia. This town borders a highly endemic Venezuelan focus of cutaneous leishmaniasis where L. spinicrassa has been found infected naturally with promastigotes identified by isoenzyme analysis as Leishmania braziliensis in Arboledas, Colombia (Young et al. 1987). Lutzomyia nuneztovari anglesi Le Pont & Desjeux 1984 is presumed to be the vector of cutaneous leishmaniasis in the Yungas focus, Bolivia, where it is the only anthropophilic sandfly caught in houses. During 1982 and 1983, several L. n. anglesi were found with promastigotes in the peripyloric position, suggesting that the parasite might be a Leishmania of the braziliensis complex (Le Pont et al. 1989). Lutzomyia ovallesi (Ortiz, 1952) has been reported to be infected with flagellates in Panama" (Williams 1970) and Colombia (Young et al. 1987). In San Esteban, Carabobo State, Venezuela, it was found naturally infected with promastigotes attached to the pylorus (Feliciangeli et al. 1988a). Previously, in that focus, a strong correlation was observed between the monthly abundance of this species and the monthly incidence of leishmaniasis (Feliciangeli 1987a). That study led to the suggestion that this highly anthropophilic species may be the vector of the disease at this focus. Recently, L. evansi (Nunez Tovar, 1924), a sandfly which often shares habitats with L. longipalpis, has been regarded as a secondary or even a primary vector of visceral leishmaniasis in the Department of Cordoba, Colombia. Promastigotes isolated from one naturally infected specimen of L. evansi multiplied in a hamster, and parasites recovered from a second animal readily grew in culture. The isoenzyme pattern proved to be identical to those of the Leishmania chagasi and Leishmania donovani reference strains (Travi et al. 1990). As part of the revision of this important phlebotomine group in Venezuela, a new species is described and illustrated keys for both sexes in the totvnsendi and verrucarum series are provided. State distribution maps also are presented (Fig. 1-3). Because Young (1979) reviewed the published literature on most of the species considered here, only those references dated after 1979 have been included.

Vol. 29, no. 5

L. verrucarum Species Croup A. Series totvnsendi Lutzomyia amilcari Arredondo Lutzomyia amilcari Arredondo 1984: 63 (male holotype, Yacambu, Lara State, Venezuela); Arredondo et al. 1989: 227 (female, Yacambu, Lara State, Venezuela). Distribution. Venezuela. Lutzomyia spinicrassa Morales, Osorno, Osorno & Hoyos Lutzomyia spinicrassa Morales, Osorno, Osorno & Hoyos 1969: 383 (male holotype, vereda Umbabita, Almeida, Boyac£, Colombia, female vereda Chitavita, Guayata, Boyaca, Colombia); Tesh et al. 1986: 1311 (Phlebovirus isolated in Colombia); Tesh et al. 1987: 654 (naturally infected with the Alagoas serotype of vesicular stomatitis virus in Colombia); Feliciangeli & Murillo 1987: 141 (misidentified as L. townsendi); Young et al. 1987: 587 (naturally infected with Leishmania braziliensis); Alexander 1987: 552 (dispersal); Kreutzer et al. 1987: 609 (karyotype); Kreutzer et al. 1988: 455 (identification of L. spinicrassa studied in question); Anez et al. 1988: 457 (Merida State); Ryan 1989: 718 (multiple forced feeding); Kreutzer et al. 1990: 1 (isoenzyme profiles). Distribution. Colombia, Venezuela. Lutzomyia townsendi Ortiz Phlebotomus townsendi Ortiz 1960: 23 (male holotype, Rancho Grande, Aragua state, Venezuela); Ortiz & Scorza 1963: 347 (male redescribed, female described). Lutzomyia townsendi: Young 1979: 86 (cf. L. sauroida); Rojas et al. 1982-1983: 78 (Yaracuy state); Feliciangeli & Murillo 1987: 141 (misidentification of L. youngi and L. spinicrassa as "L. townsendi" in western Venezuela); Kreutzer et al. 1990: 1 (isoenzyme profiles). Distribution. Venezuela. Lutzomyia youngi Feliciangeli & Murillo Lutzomyia youngi Feliciangeli & Murillo 1987: 141 (male holotype), 143 (female allotype, Las Calderas, 1,350 m, Trujillo, Venezuela), 141 (suspected vector misidentified as "L. townsendi" in endemic foci of cutaneous leishmaniasis in western Venezuela and Costa Rica); Murillo & Zeled6n 1985: 70 (listed, figures, distribution in Costa Rica); Scorza 1988: 72 (proven vector of cutaneous leishmaniasis);

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Lutzomyia verrucarum GROUP IN VENEZUELA

65° 00' M A R \ C A R I B E

731

60*00'

ESTADQS 1 ANZOATEGUI 2 APURE 3 ARAGUA 4 BARINAS 3 BOLIVAR 6 CARABOBO 7 COJEOES 8 OISTRITO FEDERAL 9 FALCON 10 GUARICO I I LARA 12 MERIOA I 3 MIRANDA 14 MONAGAS I S NUEVA ESPARTA

16 PORTUGUESA 17 SUCRE 1 8 TAC HIRA 19 T. FEDERAL AMAZONAS 20 DELTA AMACURO 2 I TRUJILLO

22 YARACUY

%

23 ZULIA

— I* 00

^

L. s p i n i c r a s s q

L. t o w n s e n d i ——

^—^————————

L.. y o u n q i

•

L_. n a d i a e n. sp.

Fig. 1. Known geographical distribution of L. townsendi, L. spinicrassa, L. youngi, and L. nadiae, n. sp.

Anez et al. 1988: 457 (altitudinal distribution in M6rida State); Kreutzer et al. 1990: 1 (isoenzyme profiles); Rojas & Scorza 1989: 29 (xenodiagnosis in patients with Leishmania braziliensis). Lutzomyia townsendi (not L. townsendi Ortiz, 1960): Carnevali & Scorza 1976: 333 (experimental infection with Leishmania braziliensis sensu latu; Mogoll6n et al. 1977: 206 (altitudinal distribution in Trujillo State); Valera et al. 1978: 246 (suspected vector of cutaneous leishmaniasis in M6rida State, Venezuela); Moreno & Scorza 1981: 180 (behavior of Leishmania garnhami); Scorza & Carnevali 1981: 229 (natural and experimental infections with Ascocystis chagasi); Moreno & Scorza 1982: 6 (morphology of Leishmania garnhami in hamsters infected by L. townsendi); Scorza & Delgado 1982: 217 (development of Leishmania mexicana pifanoi); Mdrquez & Scorza 1982: 229 (age grading); Mdrquez & Scorza 1984: 8 (population dynamics); Scorza et al. 1984a: 21 (natural infection with Leishmania braziliensis,

Trujillo State); Scorza et al. 1984b: 54 (markrelease technique for estimating population density); Anez & Oviedo 1985: 739 (larval diet); Rojas & Scorza 1986: 31 (refeeding activity). Distribution. Costa Rica, Venezuela. Lutzomyia nadiae Feliciangeli, Arredondo & Ward, new species (Fig. 4) Tables 1 and 2 give descriptive statistics and some detailed estimates of variability, expressed as coefficients of variation, for diagnostic morphological structures of L. nadiae, n. sp. For measurements (in millimeters) and terminology, we adopted the system used by Young (1979). Male. Mesonotum dark, pleura pale. Eyes small. Ascoids simple on all flagellomeres except last 2. Palp formula: 1-4-2-3-5. Cibarium with few, dotlike vestigial teeth, cibarial arch complete, pigment patch inconspicuous. Pharynx unarmed. Pleura with 4-4 to 11-10 upper and 2-2 to

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JOURNAL OF MEDICAL ENTOMOLOGY 73°OO*

60*00'

— t - 00'

ESTADOS 1 ANZOATEGUI 2 APURE 3 ARA6UA 4 BARINAS 5 BOLIVAR 6 CARABOBO 7 COJEOES 8 DISTRITO FEDERAL 9 FALCON 10 GUARICO I I LARA 12 MERtOA 13 MIRANDA 14 MONAGAS I S NUEVA ESPARTA 16 PORTUGUESA 17 SUCRE I 8 TACHIRA 19 T FEDERAL AMAZONAS 20 DELTA AMACURO 21 TRUJILLO 22 YARACUY 23 ZULIA

•

L. g m i 1 c g r i

A L. oulari •

L. nuneztovgri

Fig. 2. Known geographical distribution of L. amilcari, L. aulari, and L. nuneztovari in Venezuela.

5-4 lower episternal setae on each side. Femora without spines. Genitalia: style with 4 spines at different levels. Subterminal bristle present. Coxite with a ventral tuft of 13-17 fine hairs (x, 15; CV, 1.94%; n = 26). Paramere slender and slightly clubbed bearing long hairs (Fig. 4G). Aedeagus well sclerotized, subtriangular and pointed at tip. Genital filaments with simple tips. Female. Coloration as in male. Ascoids simple and present in all except antennal segments XIII and XIV. Palp formula: l-4-(2-3)-5. Cibarium with 4 sharp equidistant horizontal teeth; one row of dotlike vertical teeth, and few, inwardly bent lateral teeth; pigment patch inconspicuous; cibarial arch complete, diffuse in middle. Pharynx unarmed but with distinct ridges. Pleura with 5-8 to 12-14 upper and 2-2 to 5-5 lower episternal setae. Spermathecae as in Fig. 4E. Individual ducts 0.1125 long, about 1.13 times length of common duct in female allotype. Discussion. Lutzomyia nadiae, with its isolated basal spine on the style, is allied closely to

L. townsendi, L. quasitownsendi, L. longiflocosa, L. spinicrassa, L. amilcari, and L. sauroida, all of which constitute the series townsendi. The male of L. nadiae is separated readily from closely allied species by the difference in the shape of the coxite tuft of fewer than 20 straight and forwardly directed setae and a concave paramere covered by long and sinuous upper setae. Although this species was caught with L. aulari and L. amilcari, the knowledge of previously described females of these two species from separated localities and the mensural data helped to distinguish females of L. nadiae from other species. The spermathecae of L. nadiae are easily distinguishable from those of L. amilcari and L. aulari because the common and individual ducts are thinner than those of L. aulari but are wider than those of L. amilcari. Moreover, the terminal knob of the spermathecae in L. nadiae is broader than the preceding segment and seems to project from the rest of the body, thus making these females very distinctive and readily separable

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Lutzomyia verrucarum

GROUP IN VENEZUELA

733

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63°00' kl A R \ C A R I B E

— 9° 00'

ESTADOS 1 2 3 4 5 6 7 8 9 10 I I I2 I 3 14 I 5 I6 17 18 19 20 2I 22 23

ANZOATEGUI APURE ARAGUA BARINAS BOLIVAR CARABOBO COJEOES DISTRITO F E D E R A L FALCON GUARICO LARA MERIOA MIRANDA MONAGAS NUEVA ESPARTA PORTUGUESA SUCRE TAC HIRA T F E D E R A L AMAZONAS DELTA AM ACURO TRUJILLO YARACUY ZULU

•

L. ovallesi

A L evansi Fig. 3. Known geographical distribution of L. ovallesi and L. evansi in Venezuela.

from all other members of the verrucarum species group. Etymology. This species has been dedicated to Nadia de Arredondo, whose interest, patience, and friendship have facilitated our studies of Venezuelan phlebotomine sandflies. Distribution. Venezuela. Type material. HOLOTYPE: 6 (slide no. 2-25.113.1), VENEZUELA: Lara, Yacambu, Zanare (1,840 m), tree trunk, 28-11-87. ALLOTYPE: 9 (slide no. 2-25.113.2), same data as holotype. PARATYPES: 306 6,209 9 (same data as holotype); 76 6, 219 9, same locality as holotype but 1,800 m, tree trunks, 28-11-87 (A. Ramirez, F. Arias). Holotype and allotype are deposited at the Centro Nacional de Referencia sobre Taxonomia de Flebdtomos, Universidad de Carabobo, Maracay, Venezuela. Paratypes are to be deposited in the same center; in the Florida State Collection of Arthropods, Gainesville, and at the British Museum (Natural History), London.

B. Series L. verrucarum Lutzomyia aulari Feliciangeli, Ordonez & Manzanilla Lutzomyia aulari Feliciangeli, Ordonez & Manzanilla 1984: 592 (male holotype, female, Venezuela, Trujillo State, Vitisay). Distribution. Venezuela. Lutzomyia evansi (Nunez Tovar) Phlebotomus evansi Nunez Tovar 1924: 44 (male, Mariara, Carabobo State, Venezuela); Ristorcelli & Van Ty 1941: 255 (female). Lutzomyia evansi: Mogoll6n et al. 1977: 209 (altitudinal distribution, Trujillo State); Ramirez Perez et al. 1978: 52 (Aragua state); 1982a: 14 (Sucre state); Rojas et al. 1982-1983: 78 (Yaracuy state); Aguilar et al. 1984: 187 (Cojedes state, caught on donkey); Zeled6n et al. 1984: 455 (association with L. longipalpis);

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6 Fig. 4. Lutzomyia nadiae, n. sp. (A) Male head, (a) Male flagellomere II. (B) Female head, (b) Female flagellomere II. (C) Male wing. (D) Female cibarium. (E) Spermathecae. (F) Male genitalia. (G) Paramere (enlarged). (H) Genital pump and filaments. Cibarium, spermathecae, and enlarged paramere drawn to same scale.

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FELICIANGELI ET AL.:

Lutzomyia verrucarum

Table 1. Ranges, ratios, and CVs of some features of male L. nadiae, n. sp. Characters" Wing WL WW

P Head HH HW ID PH FI F2+F3 L FI/L PI P2 P3 P4 P5 Legs Foreleg F T B Midleg F T B Hindleg F T B Genitalia ST CO LL GP GP GF/GP

GROUP IN VENEZUELA

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Table 2. Ranges, ratios, and CVs of some features of female L. nadiae n. sp.

n

Min

Max

X

cv

31 31 33 33 31 33

2.07 0.57 0.44 0.21 0.34 0.09

2.32 0.69 0.60 0.31 0.45 0.22

2.18 0.63 0.52 0.27 0.42 0.17

3.02 4.92 6.82 8.95 12.81 19.68

33 27 31 35 35 35 35 35 35 35 35 35 34

0.36 0.28 0.11 0.15 0.29 0.26 0.23 1.14 0.03 0.14 0.14 0.10 0.28

0.41 0.39 0.13 0.18 0.36 0.31 0.28 1.44 0.05 0.17 0.18 0.14 0.42

0.38 0.33 0.12 0.16 0.32 0.29 0.26 1.27 0.04 0.16 0.17 0.12 0.36

2.83 7.37 6.22 5.12 5.15 4.04 4.26 5.65 9.01 5.89 5.37 6.90 9.11

30 30 30

0.73 0.88 0.46

0.91 1.02 0.60

0.83 0.96 0.55

4.72 4.18 5.52

34 34 34

0.70 1.03 0.57

0.86 1.21 0.70

0.80 1.13 0.65

4.12 4.63 4.93

34 34 34

0.78 1.29 0.63

0.95 1.45 0.79

0.88 1.37 0.74

3.94 3.63 5.01

s Head HH HW ID PH FI F2+F3 L FI/L PI P2 P3 P4 P5 Legs Foreleg F T B Midleg F T B Hindleg F T B

35 34 35 35 32 32

0.14 0.30 0.31 0.09 0.39 3.31

0.17 0.36 0.35 0.13 0.52 5.78

0.16 0.34 0.33 0.09 0.46 4.85

4.17 4.54 4.78 7.80 6.92 9.90

Measurements are iin millimiters. , femur: FI. flagellomere 1; F2+F3 " B, basitarsus flagellomere 2+ flagellomere 3; HH, head height; HW, head width; ID, interocular distance; L, labrum ; PI, palpomere 1; P2, palpomere 2;; P3, palpomere 3: P4, palpomere 4; P5, palpomere 5; T, tibia; WL, wing length; WW, wing w idth.

Measurements are in millimiters. " B, basitarsus; CO, coxite; F, femur; FI, flagellomerel; F2+F3, flagellomere 2 + flagellomere 3; GF, genital filaments; GP, genital pump; HH, head height; HW, head width; ID, interocular distance; L, labrum; LI, lateral lobe; PI, palpomere 1; P2, palpomere 2; P3, palpomere 3; P4, palpomere 4; P5, palpomere 5; PH, pharynx; ST, style; T, tibia; WL, wing length; WW, wing width.

Murillo & Zeleddn 1985: 78 (Costa Rica: distribution, collecting methods, figures); Arredondo 1987 (distribution Lara State); Feliciangeli et al. 1988b: 48 (Territorio Federal Amazonas, distribution); Travi et al. 1990: 676 (suspected secondary vector of Leishmania chagasi). Distribution. Guatemala, El Salvador, Honduras, Nicaragua, Costa Rica, Colombia, Peru, Venezuela. Lutzomyia nuneztovari (Ortiz) Phlebotomus nunez-tovari Ortiz 1954: 232 (male holotype, Duaca, Lara, Venezuela). Lutzomyia nuneztovari: Young 1979: 83 (description female, full references); Ramirez

Characters" Wing WL WW

P

n

Min

Max

X

CV

38 38 37 38 37 37

2.35 0.65 0.55 0.27 0.44 0.14

2.73 0.87 0.75 0.37 0.56 0.30

2.60 0.77 0.66 0.33 0.48 0.23

3.44 5.86 6.86 10.01 6.70 14.46

37 29 34 38 38 38 38 38 38 38 38 38 36

0.39 0.35 0.12 0.18 0.28 0.24 0.34 0.77 0.07 0.18 0.18 0.13 0.38

0.45 0.46 0.15 0.21 0.32 0.27 0.39 0.86 0.06 0.22 0.22 0.18 0.51

0.43 0.40 0.14 0.20 0.30 0.26 0.38 0.80 0.05 0.20 0.20 0.16 0.42

3.66 10.16 8.51 4.29 4.38 3.13 3.52 9.07 11.15 4.36 5.31 7.92 9.66

36 36 36

0.83 0.87 0.52

0.96 1.07 0.65

0.91 0.99 0.57

3.75 5.28 4.66

38 38 38

0.82 1.05 0.61

0.96 1.29 0.77

0.90 1.17 0.69

4.30 4.73 4.72

37 37 37

0.90 1.33 0.70

1.06 1.65 0.89

0.98 1.50 0.81

4.06 4.84 5.51

Perez et al. 1982b: 58 (T6chira State); Rojas et al. 1982-1983: 78 (Yaracuy State); Le Pont & Desjeux 1984: 281 (compared with L. nuneztovari anglesi); Tesh et al. 1986: 1311 (Phlebovirus isolated in Colombia); Tesh et al. 1987: 654 (natural infection with the Alagoas serotype of vesicular stomatitis virus in Colombia); Anez et al. 1988: 457 (MSrida State). Distribution. Bolivia, Colombia, Peru, Venezuela. Lutzomyia ovallesi (Ortiz) Phlebotomus ovallesi Ortiz 1952: 155 (male holotype, Duaca, Lara, Venezuela); Lewis & Garnham 1959: 87 (description female, Belize). Lutzomyia ovallesi: Mogoll6n et al. 1977: 209 (altitudinal distribution, Trujillo State); Ramirez Perez et al. 1978: 50 (Aragua State); Christensen & Herrer 1980: 523 (host attraction profiles); Ramirez Perez & Ramirez 1981—

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1982: 23 (Barinas State); Ramirez Perez et al. 6. Paramere concave, with long curved hairs 1982a: 14 (Sucre state); 1982b: 58 (Tachira throughout; Basal tuft of coxite with «s20 State); Rojas et al. 1982-1983: 78 (Yaracuy straight hairs (Fig. 4F) State); Christensen et al. 1983: 463 (ecology); . . . . L. nadiae Feliciangeli, Arredondo & Scorza et al. 1984a: 27 (epidemiological imporWard, n. sp. tance); Aguilar et al. 1984: 187 (Cojedes, natuParamere straight, with short hairs over diral infection with epimastigotes and trypostal % and long proximal hairs; basal tuft mastigotes, caught on man and dog); Murillo & of coxite with >20 curved hairs (Fig. 6B) Zeled6n 1985: 75 (Costa Rica, figures, distriL. townsendi Ortiz bution, collecting methods); Tesh et al. 1986: 7. Paramere slender; style with or without 1311 (Phlebovirus isolated in Colombia); subterminal bristle (Fig. 5D) Arredondo 1987: 1 (Lara State); Tesh et al. L. nuneztovari Ortiz 1987: 654 (natural infection with the Alagoas Paramere stout; style with subterminal serotype of vesicular stomatitis virus in Colombristle 8 bia); Young et al. 1987: 588 (natural infection, 8. Paramere hyaline and swollen (Fig. 6D) Arboledas, Colombia); Feliciangeli 1987a: 178 L. ovallesi Ortiz (suspected vector of cutaneous leishmaniasis); Paramere spatulate (Fig. 5B) 1987b: 171 (seasonal fluctuations); FeliL. evansi Nunez-Tovar ciangeli et al. 1988a: 393 (peripylorus naturally infected with promastigotes, San Esteban, Females Venezuela); Anez et al. 1988: 457 (altitudinal distribution, M6rida). 1. Individual ducts of spermathecae >4 times longer than common duct; body of sperDistribution. Mexico, Belize, Honduras, Nicamatheca very small (Fig. 7A) ragua, Costa Rica, Panama^ Colombia, Trinidad, L. evansi Nunez-Tovar Venezuela. Individual ducts of spermathecae about same size as common duct; body of spermatheca comparatively large 2 2. Spermathecae very elongated, with a Keys to the Venezuelan Species in the L. clearly defined central constriction (Fig. verrucarum Croup 7B) L. ovallesi Ortiz Spermathecae less elongated, lacking such Males a central constriction 3 1. Basal spines of style inserted on distinct 3. Common duct of spermathecae stout, >2 tubercles; coxite with subapical group of times width of individual ducts; head of long hairs (Fig. 5A) spermatheca narrow and prominent (Fig. L. aulari Feliciangeli, Ordonez & 7C) Manzanilla L. aulari Feliciangeli, Ordonez & Basal spines of style not inserted on such Manzanilla tubercles; coxite without subapical group Common duct of spermathecae relatively of long hairs 2 narrow, always less than twice width of individual ducts; head of spermatheca 2. Style with 1 isolated basal spine 3 otherwise 4 Style with 2 paired basal spines 7 4. Terminal knob of spermatheca equal in 3. Terminal spine of style thick and S-shaped width to preceding segment; head of (Fig. 6A) spermathecae deeply invaginated (Fig. . . L. spinicrassa Morales, Osorno, Osorno 7D) & Hoyos L. nuneztovari Ortiz Terminal spine of the style slender and C-shaped 4 Terminal knob of spermatheca wider or narrower than preceding segment; head 4. Paramere with 1 small group of dorsal seof spermatheca not invaginated 5 tae restricted to apex 5 5. Terminal knob of spermatheca distincParamere with dorsal setae extending entively wider than preceding segment tire length 6 (Fig. 4E) 5. Paramere enlarged in middle; terminal . . . . L. nadiae Feliciangeli, Arredondo & group of dorsal setae subequal in size (Fig. 5C) Ward, n. sp. L. amilcari Arredondo Terminal knob of spermatheca distinctively narrower than preceding segment . 6 Paramere narrow in middle; terminal group of dorsal setae decreasing in size 6. Spermathecae finely striated and roughly toward apex (Fig. 6C) conical (Fig. 7E) L. youngi Feliciangeli & Murillo L. amilcari Arredondo

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Fig. 5. Male genitalia. (A) L. aulari. (B) L. evansi. (C) L. amilcari. (D) L. nuneztovari.

Spermathecae wrinkled and less conical or roughly spherical (Fig. 7F) L. townsendi Ortiz (Fig. 7G) . L. youngi Feliciangeli & Murillo (Fig. 7H) . . L. spinicrassa Morales, Osorno, Osorno & Hoyos Discussion Taxonomy. At present, the L. verrucarum series of the L. verrucarum group includes 11 taxa: Lutzomyia andina Osorno, Osorno & Morales, 1972; L. aulari Feliciangeli, Ordonez & Manza-

nilla, 1984; L. columbiana (Ristorcelli & Van Ty, 1941); L. disjuncta Morales, Osorno & Osorno, 1974; L. evansi (Nunez-Tovar, 1924); L. moralesi Young, 1979; L. nevesi (Damasceno & Arouck, 1956); L. nuneztovari (Ortiz, 1954); L. nuneztovari anglesi Le Pont & Desjeux, 1984; L. ovallesi (Ortiz, 1952); and L. verrucarum (Townsend, 1913). To date, the townsendi series includes eight species: Lutzomyia amilcari Arredondo, 1984; L. longiflocosa Osorno, Morales, Osorno & Hoyos, 1970; L. quasitownsendi Osorno, Osorno & Morales, 1972; L. sauroida Osorno, Morales & Os-

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Vol. 29, no. 5

Fig. 6. Male genitalia. (A) L. spinicrassa. (B) L. townsendi. (C) L. youngi. (D) L. ovallesi.

orno, 1972; L. spinicrassa Morales, Osorno, Osorno & Hoyos, 1969; L. townsendi (Ortiz, 1960); L. youngi Feliciangeli & Murillo, 1987; and the new species described herein, L. nadiae, n. sp.

The verrucarum series species that undoubtedly exist in Venezuela include L. aulari, L. evansi, L. nuneztovari, and L. ovallesi; there is doubt over the presence of L. verrucarum. Two

September 1 9 9 2

F E L I C I A N G E L I E T A L . : Lutzomyia

verrucarum

G R O U P IN VENEZUELA

739

Fig. 7. Spermathecae. (A) L. evansi. (B) L. ovallesi. (C) L. aulari. (D) L. nuneztovari. (E) L. amilcari. (F) L. townsendi. (G) L. youngi. (H) L. spintcrassa.

early records are available: one b y Anduze in Merida State (reported b y Pifano & Ortiz 1 9 5 2 ) , which does not stipulate the sex o f the speci­ mens collected; and that b y Floch & A b o n n e n c ( 1 9 5 0 - 1 9 5 3 ) , referring to the finding, in Borburata, Carabobo State, o f only a single female; it commonly is accepted that, in this group, species

identification based on females in the absence o f conspecific males is not reliable (Young 1 9 7 9 ) . Recent research in Venezuela has not confirmed the presence o f this species there. T h e description o f L. aulari was based on two males and four females which were in p o o r con­ dition. T h e association of the sexes was tentative,

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JOURNAL O F M E D I C A L E N T O M O L O G Y

Table 3.

Distribution of Venezuelan sandflies in the L. verrucarum

V o l . 29, no.

5

group, according to life zones fc

Life zones" (dry mo/y) Species

L. L. L. L. L. L. L. L. L.

evansi ovallesi nuneztovari aulari amilcari nadiae spinicarassa youngi townsendi

BHT

BST

BMST

BET

BHP

BSP

BMSP

BEP

BHMB

BSMB

(1)

(4)

(7)

(10)

(1)

(4)

(7)

(10)

(1)

(4)

X X

X X

X

X

X

X X

— — — — — — —

—

X X

— — — — — — —

— — — — —

X X X

X

— — — — — — — —

X X X X X X X X

— — — — — —

— — — — — —

X

X X

—

X

— — — — X X

—

— — — — — — —

— —

—

— — — —

" After Veillon, 1989. Tropical (0-500 m, >24°C): BHT, moistforest;BST, dry forest; BMST, very dry forest; BET, thorn woodland. Premontane (500-1,500 m, 18-24°C): BHP, moist forest; BSP, dry forest, BMSP, very dry forest; BEP, thorn woodland. Lower montane (1,500-2,500 m, 12-18°C): BHMB, moist forest; BSMB, dry forest. b

and the females were not included in the type series (Feliciangeli et al. 1984). Later, w e col­ lected fresh material which was similar to the original description o f L. aulari from Trujillo State. The spermathecae are unique, although they rather resemble those o f L. moralesi. H o w ­ ever, an amendment needs to b e made with re­ spect to the features o f the female cibarium o f L. aulari. The original description included a draw­ ing o f the cibarium with 10—12 teeth o f various sizes that appeared to b e twisted in different positions. Nevertheless, fresh material shows this species having the typical cibarium o f the group with four straight horizontal teeth, a row o f vertical teeth, and a few fine lateral teeth. Lutzomyia nuneztovari lacks the subterminal spine on the style as described from type speci­ mens from Duaca (Lara State, 275 m above sea level). However, 1 o f 8 males collected in Rancho Grande (Aragua State, 1,160 m), 8 o f 18 males from Tachira State, and 3 o f 5 males caught in Lara State (1,450-1,800 m) show such a bristle. However, other characters, such as the number of setae in the coxite tuft and genital filaments versus genital p u m p length, are consistent and specific to L. nuneztovari. At present, w e prefer to treat the two Venezu­ elan morphs as conspecific because the loss o f the bristie may represent intraspecific variation similar to the Colombian L. rorotaensis, which have only four rather than five spines on the style (Young 1979). Among the eight species that constitute the townsendi species complex, four are autochtho­ nous to Venezuela: L. amilcari; L. nadiae, n. sp.; L. townsendi; and L. youngi. T h e others have been described from the Colombian Andes. Among these, only L. spinicrassa has b e e n re­ ported in Venezuela. In this series, taxonomic problems have b e e n encountered in separating males o f L. youngi and L. spinicrassa from males o f L. townsendi in the Venezuelan Andean region (Feliciangeli & Murillo 1987). Males o f L. sauroida are also re­

markably similar in structure to those o f L. townsendi (Young 1979). Although paramere setation'will readily distinguish males, females o f these closely related species are morphologically indistinguishable (isomorphic). This is a signifi­ cant problem in epidemiological studies o f vec­ tor incrimination. In Tachira State, where the highest numbers o f cutaneous leishmaniasis cases are reported, L. spinicrassa, L. youngi, and a species closely related to L. townsendi have b e e n found to occur sympatrically. Kreutzer et al. (1990) used isozyme profiles to separate females in the L. townsendi series. Moreover, they emphasized that information from only a few enzymes would b e necessary for spe­ cific identification at certain localities. L. youngi and L. spinicrassa each have a fixed diagnostic allomorph for phosphogluconate dehydrogenase and fumarate hydratase. The c o m b i n e d data from these enzymes plus 6-phosphofructokinase, phosphoglucomutase, and glucose phosphate isomerase, separate L. townsendi from other spe­ cies as well as from L. sauroida, L. longiflocosa, and L. quasitownsendi. However, the three lastnamed species were not separated from each other using enzyme data. Ecology. Research on the phlebotomine fauna in Venezuela has b e e n carried out primarily at e n d e m i c foci o f leishmaniasis. However, sandfly collection records are available (Fig. 1-3) from all states (20) except eastern Territorio Federal Delta Amacuro, Monagas, and Anzoategui. The distribution o f the species reviewed is shown in relation to life zones in Table 3. Veillon (1989) recognizes only 16 life zones in Venezu­ ela rather than the 22 previously described b y E w e l & Madriz (1968), w h o followed the Holdridge system which is primarily based on annual rainfall levels and temperature as determinants of climax vegetation. In contrast, Veillon (1989) preferred the annual average rainfall for the dry months as a more useful and realistic ecological factor in describing life zones.

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F E L I C I A N G E L I E T A L . : Lutzomyia

Life zones are based on climax vegetation; thus, they offer a static overview o f ecological distributions. Continuous and often drastic inter­ vention b y man often results in the substitution of primary b y secondary vegetation, which in turn affects the fauna. Such exploitation for agri­ cultural purposes is especially intensive in the foothills o f the fertile Andean region and along the Serrania de la Costa. Under such distinctive circumstances, sandfly and reservoir introduc­ tions may explain abrupt changes in the inci­ dence o f Leishmania cases. Species with w i d e altitudinal ranges o c c u p y a greater variety o f life zones than species re­ stricted to high altitudes. This is demonstrated by the w i d e geographical distribution o f L. evansi, L. ovallesi, and L. nuneztovari, which have wider altitudinal ranges than the other members o f the group that are restricted to areas close to or above 1,000 m. Lutzomyia evansi and L. ovallesi are wide­ spread in Central America, Colombia, and Ven­ ezuela. T h e former reaches as far west as Peru. In Venezuela, their distribution almost overlaps the cis-Andean lowland forests as well in the Andean region (Fig. 3). T h e lack o f reports o f L. evansi in Merida State may reflect the need for more collections. T h e medical importance o f these two highly anthropophilic species has been discussed previously. Lutzomyia nuneztovari is distributed through­ out Colombia, Venezuela, Bolivia, and Peru. In spite o f a w i d e geographical and altitudinal dis­ tribution in Venezuela, L. nuneztovari is not abundant. It is occasionally caught in tree holes or with Shannon traps. Data from Colombia (Young 1979; Tesh et al. 1986,1987) also confirm this observation. In contrast to L. nuneztovari anglesi from Bolivia, which is abundant and highly anthropophilic (Le Pont & Desjeux 1984, Le Pont et al. 1989), it is not known if L. nunez­ tovari bites humans. Although most o f the Andean species in this taxon seem to have restricted and allopatric dis­ tributions (Young 1979), some occur sympatrically. For example, L. amilcari, L. aulari, and L. nadiae, which are confined to Venezuela, occur together in tree holes in the mountains o f Yacambii, Lara State (Fig. 1 and 2), although they are never captured in Shannon traps (M.D.F., unpublished data). Lutzomyia townsendi also has b e e n reported in certain parts of Venezuela (such as Aragua and Yaracuy States) (Fig. 1) which are characterized by undisturbed moist premontane forests. This species is, however, highly phototropic and an­ thropophilic. Its biology and e c o l o g y have b e e n described extensively in a series o f studies (Scorza et al. 1963, 1967, 1968a, b , c, d, e, f, Scorza 1972). L. spinicrassa, described in neigh­ boring Colombia, extends into the Venezuelan states o f Tachira and Merida. L. youngi so far has

verrucarum

G R O U P IN V E N E Z U E L A

741

b e e n recorded only in Venezuela and Costa Rica. In Venezuela, it is distributed throughout the Andean states o f Tachira, Merida, and Trujillo, attaining the mountains in Lara State (Fig. 1). Lutzomyia spinicrassa and L. youngi are found in disturbed areas o f lower montane moist and premontane moist forests as well as in pre­ montane dry forests. O n several occasions, they were collected together in agricultural areas and villages in Tachira State, where both w e r e at­ tracted b y light and human bait. L. spinicrassa enters houses in C o l o m b i a and Tachira State, Venezuela, as does L. youngi in the periurban area o f the city o f Trujillo (Scorza 1988). Pre­ ferred biotopes o f both species seem to b e sec­ ondary forest such as coffee plantations with l o w nocturnal temperatures ( 8 5 % R H ) . Because o f its medical impor­ tance, L. youngi has b e e n studied extensively (Marguez & Scorza 1982; Scorza et al. 1984b; Rojas & Scorza 1986, 1989, Anez et al. 1988).

Acknowledgments W e are grateful to D. G. Young for helpful discus­ sions and facilities given at his laboratory, and to Margot Duncan for drawings of the new species. The con­ scientious technical assistance of Alirio Ramirez, Arturo Bravo, and Freddy Arias is also acknowledged. This work was supported by the Commission of the European Communities (project CEC-STD-TS2-0034UK-AM), the Consejo Nacional de Investigaciones Cientificas y Tecnologicas (CONICIT, Project S1-1444), the University of Carabobo ( C O D E C I H , Project FCS005-84), and by the PAHO Unit in Maracay, which frequently provided a vehicle for field work.

References Cited Aguilar, C. M., E. Fernandez, R. de Fernandez & L. M . Deane. 1984. Study of an outbreak of cutaneous leishmaniasis in Venezuela. The role of domestic animals. Mem. Inst. Oswaldo Cruz Rio J. 79: 1 8 1 195. Alexander, J. B. 1987. Dispersal of phlebotomine sand flies (Diptera: Psychodidae) in a Colombian coffee plantation. J. Med. EntomoL24: 552—558. Anez, N. & M . Oviedo. 1985. Two new larval diets for rearing sandflies in the laboratory. Trans. R. Soc. Trop. Med. Hyg. 79: 739-740. Anez, N., E. Nieves & J. V. Scorza. 1985. El status taxonomico de Leishmania garnhami, indicado por su patron de desarrollo en el vector. Mem. Inst. Oswaldo Cruz Rio J. 80: 113-119. Anez, N., D . Cazorla, E. Nieves, B. Chataing, M . Castro & A. L. De Yarburg. 1988. Epidemiologia de la leishmaniasis tegumentaria en Merida, Venezuela. I. Diversidad y dispersibn de especies flebotominas en tres pisos altitudinales y su posible role en la transmision de la enfermedad. Mem. Inst. Oswaldo Cruz Rio J. 83: 4 5 5 - 4 6 3 . Arredondo, C. C. 1984. Phlebotominae de Venezu­ ela: Lutzomyia amilcari sp. n. del Estado Lara. Mem. Inst. Oswaldo Cruz Rio J. 79: 6 3 - 6 6 . 1987. Flebotomos del Estado Lara. Memorias Iller

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Simposio Venezolano de Leishmaniasis. Barquisimeto. Universidad Centro Occidental Lisandro Alvarado Publ. Arredondo, C. C , A. L. Falcao & E. S. Dias. 1989. Phlebotominae de Venezuela: description of the fe­ male of Lutzomyia amilcari (Diptera: Psychodidae: Phlebotominae). Mem. Inst. Oswaldo Cruz Rio J. 83: 227-228. Barretto, M . P. 1962. Novos subgeneros de Lutzomyia Franca, 1924 (Diptera: Psychodidae, subfamilia Phlebotominae). Rev. Inst. Med. Trop. Sao Paulo 4: 91-100. Carnevali, M . & J. V. Scorza. 1976. Infecci6n exper­ imental de Lutzomyia townsendi (Ortiz, 1959) con una cepa venezolana de Leishmania braziliensis. Bol. Dir. Malariol. Saneamiento Ambiental 16: 3 3 3 343. Christensen, H. A. & H. Herrer. 1980. Panamanian Lutzomyia (Diptera: Psychodidae) host attraction profiles. J. Med. Entomol. 17: 522-528. Christensen, H. A., G. B. Fairchild, A. Herrer, C. M . Johnson, D. G. Young & A. M . de Vasquez. 1983. The ecology of cutaneous leishmaniasis in the Re­ public of Panama. J. Med. Entomol. 20: 453-484. Ewel, J. J. & A. Madriz. 1968. Zonas de vida de Venezuela. Memoria explicativa sobre el mapa ecol6gico. Sucre, Caracas, Venezuela. Feliciangeli, M . D . 1987a. Ecology of sandflies (Diptera: Psychodidae) in a restricted focus of cuta­ neous leishmaniasis in northern Venezuela. IV. Sandfly monthly fluctuation and leishmaniasis inci­ dence relationship. Mem. Inst. Oswaldo Cruz Rio J. 82: 177-179. 1987b. Ecology of sandflies (Diptera: Psychodidae) in a restricted focus of cutaneous leishmaniasis in northern Venezuela. III. Seasonal fluctuation. Mem. Inst. Oswaldo Cruz Rio J. 82: 167-176. 1988. La fauna flebot6mica (Diptera: Psychodidae) en Venezuela: I. Taxonomia y distribucion geografica. Bol. Dir. Malariol. Saneamiento Ambi­ ental 28: 99-113. Feliciangeli, M . D . & J. Murillo. 1987. Lutzomyia youngi (Diptera: Psychodidae), a new phlebotomine sand fly previously misidentified as L. townsendi in endemic foci of cutaneous leishmania­ sis in Venezuela and Costa Rica. J. Med. Entomol. 24: 141-146. Feliciangeli, M . D . , R. Ordonez & P. Manzanilla. 1984. Lutzomyia aulari, a new phlebotomine sandfly (Diptera: Psychodidae) from Trujillo State, Venezuela. J. Med. Entomol. 21: 592-596. Feliciangeli, M. D . , R. M . Reyes & J. Limongi. 1988a. Natural infection of Lutzomyia ovallesi (Diptera: Psychodidae) with parasites of the Leishmania bra­ ziliensis complex in a restricted focus of cutaneous leishmaniasis in northern Venezuela. Mem. Inst. Oswaldo Cruz Rio J. 83: 393-394. Feliciangeli, M . D . , J. Ramirez Perez & A. Ramirez. 1988b. The phlebotomine sandflies of Venezuela Amazonia. Med. Vet. Entomol. 2: 4 7 - 6 5 . Floch, H. & E. Abonnenc. 1950-1953. Presence de Phlebotomus verrucarum Townsend, 1913, et de Phlebotomus lichyi n. sp. au Venezuela. Bol. Ento­ mol. Venez. 9: 3 - 8 . Kreutzer, R. D . , G. B. Modi, R. B. Tesh & D . G. Young. 1987. Brain cell kariotypes of six species of New and Old World sand flies (Diptera: Psychodidae) in the laboratory. J. Med. Entomol. 24: 6 0 9 - 6 1 2 .

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Kreutzer, R. D . , A. Morales, E. Cura, C. Ferro & D . G. Young. 1988. Brain cell kariotypes of six New World sand flies (Diptera: Psychodidae). J. Am. Mosq. Control Assoc. 4: 4 5 3 - 4 5 5 . Kreutzer, R. D . , M . T. Palau, A. Morales, C. Ferro, D . Feliciangeli & D . G. Young. 1990. Genetic rela­ tionship among phlebotomine sand flies (Diptera: Psychodidae) in the verrucarum species group. J. Med. Entomol. 27: 1-8. Le Pont, F. & P. Desjeux. 1984. Phlebotomes de Bolivie. 1. Lutzomyia nuneztovari anglesi n. sp. (Diptera, Psychodidae), nouveau phlebotome anthropophile du piemont andin. Cah. O.R.S.T.O.M., Ser. Entomol. Med. Parasitol. 4: 277-282. Le Pont, F., J. Mouchet & P. Desjeux. 1989. Leish­ maniasis in Bolivia—VI. Observations on Lutzo­ myia nuneztovari anglesi Le Pont & Desjeux, 1984 the presumed vector of tegumentary leishmaniasis in the Yungas focus. Mem. Inst. Oswaldo Cruz Rio J. 84: 277-278. Lewis, D . J. & P.C.C. Garnham. 1959. The species ofPhlebotomus (Diptera: Psychodidae) in British Honduras. Proc. R. Entomol. Soc. Lond. Ser. B Taxon. 28: 7 9 - 8 9 . Martins, A. V., P. Williams & A. L. Falcao. 1978. American sandflies (Diptera: Psychodidae, Phlebot­ ominae). Academia Brasileira de Ciencias, Rio de Janeiro, Brazil. Marquez, M . & J. V. Scorza. 1982. Criterios de nuliparidad y de paridad en Lutzomyia townsendi (Or­ tiz, 1959) del occidente de Venezuela. Mem. Inst. Oswaldo Cruz Rio J. 77: 229-246. 1984. Dinamica poblacional de Lutzomyia townsendi (Ortiz, 1959) (Diptera, Psychodidae) y su paridad en Trujillo, Venezuela. Bol. Dir. Mai. San. Amb. 24: 8 - 2 0 . Mogollon, J., P. Manzanilla & J. V. Scorza. 1977. Distribucion altitudinal de nueve especies de Lut­ zomyia (Diptera, Psychodidae) en el Estado Tru­ jillo, Venezuela. Bol. Dir. Malariol. Saneamiento Ambiental 17: 206-223. Morales, A. A., E. Osorno, F. de Osorno & P. de Hoyos. 1969. Phlebotominae de Colombia (Diptera, Psy­ chodidae) V. Descripcion de una nueva especie de Lutzomyia. Rev. Acad. Colomb. Cienc. Exactas Fis. Nat. 13: 383-390. Moreno, E. & J. V. Scorza. 1981. Comportamiento in vivo e in vitro de siete aislados de Leishmania garnhami del occidente de Venezuela. Bol. Dir. Malariol. Saneamiento Ambiental 21: 179—191. 1982. La estabilidad del caracter taxonomico especifico de Leishmania garnhami de Venezuela. Bol. Dir. Malariol. Saneamiento Ambiental 22: 1-10. Murillo, J. & R. Zeledon. 1985. Fleb6tomos de Costa Rica. Brenesia 23: 1—137. Nunez Tovar, M . 1924. Mosquitos y flebotomos de Venezuela. Comercio, Caracas, Venezuela. Ortiz, I. 1952. Sobre dos nuevos machos del genero Phlebotomus (Diptera: Psychodidae). Rev. Venez. Sanid. Asist. Soc. 17: 153-158. 1954. Descripci6n de dos nuevas especies del gen­ ero Phlebotomus Rondani (Diptera, Psychodidae) de Venezuela. Acta Biol. Venez. 1: 232-250. 1960. Phlebotomus townsendi n. sp., interesante representante de dos Psychodidae (Dipt.) de Rancho Grande en el Estado Aragua. Bol. Venez. Lab. Clin. 4: 23-26. Ortiz, I. & J. V. Scorza. 1963. Notas biologicas y

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FELICIANGELI ET AL.:

Lutzomyia verrucarum GROUP IN VENEZUELA

taxon6micas sobre algunos Phlebotominae (Diptera, Psychodidae) de Rancho Grande, Venezuela. Acta Biol. Venez. 3: 341-361. Pifano, F. & I. Ortiz. 1952. Representantes Venezolanos del g6nero Phlebotomus Rondani, 1840 (Diptera: Psychodidae). Rev. Venez. Sanid. Asist. Soc. 17: 135-151. Ramirez Perez, J. & A. Ramirez. 1981-1982. Estudio de la fauna flebot6mica del Estado Barinas (Venezuela). Bol. Dermatol. Sanit. 18: 21-50. Ramirez Perez, J., G. Rodriguez Ochoa, A. Ramirez & F. Carvillo. 1978. Estudio de la fauna flebot6mica del estado Aragua (Venezuela). Bol. Dir. Malariol. Saneamiento Ambiental 18: 43-80. Ramirez Perez, J., G. Rodriguez Ochoa & A. Ramirez. 1982a. Estudio de la fauna flebot6mica del Estado Sucre (Venezuela). Bol. Dir. Malariol. Saneamiento Ambiental 22: 53-75. 1982b. Estudio de la fauna flebot6mica del estado Tdchira (Venezuela). Bol. Dir. Malariol. Saneamiento Ambiental 22: 53-75. Ristorcelli, A. & D. Van Ty. 1941. Plebotomus d'une regione de Colombie ou la Verruga du P6rou est devenue ende'mique depuis deux ou trois ans (seconde note). Ann. Parasitol. Hum. Comp. 18: 251-269. Rojas, E. & J. V. Scorza. 1986. Relaciones entre las ingestas sanguineas incompletas y la realimentaci