MORPHOLOGY, SYSTEMATICS, EVOLUTION
Anopheles (Anopheles) pseudopunctipennis Theobald
(Diptera: Culicidae): Neotype Designation and Description
LEOPOLDO M. RUEDA,1 E. L. PEYTON,2
AND
SYLVIE MANGUIN3
Department of Entomology, Walter Reed Army Institute of Research, 503 Robert Grant Avenue,
Silver Spring, MD 20910 Ð7500
J. Med. Entomol. 41(1): 12Ð22 (2004)
ABSTRACT Detailed morphological descriptions and illustrations are provided for the adult male
and female, male genitalia, pupal, and larval stages of Anopheles (Anopheles) pseudopunctipennis
Theobald, a major vector of human malaria in Central and South America. Taxonomic and related
literature records, diagnostic features, distribution, and bionomics of the species are included. A
neotype male for the species from the type locality of Grenada is designated.
KEY WORDS Anopheles pseudopunctipennis, neotype, description, mosquitoes, malaria
Anopheles (Anopheles) pseudopunctipennis Theobald
is considered a major vector of human malaria in
Central and South America, particularly in Mexico,
Guatemala, Nicaragua, Bolivia, Ecuador, Peru, and
Argentina (Pan American Health Organization 1994).
It is widely distributed in the New World (Rozeboom
1941). It is found from the southern United States
(40⬚ N) to the northern part of Argentina (30⬚ S) along
the Andes, with eastern extension into Venezuela and
the Lesser Antilles (Manguin et al. 1996). It is the most
important malaria vector in the foothills of mountainous areas and other elevated (up to 2800 m), rugged
malaria-endemic areas of North, Central, and South
America (Aitken 1945, Rodriguez and Loyola 1989,
Gorham et al. 1973).
Anopheles pseudopunctipennis was Þrst described by
Theobald (1901: 305Ð306) from one male and one
female from Grenada (Dr. Hatton, per Dr. Daniels),
mounted in balsam. However, these two specimens, as
in the case of other Daniels material, are presumably
lost or nonextant. The original adult description
(Theobald 1901) was incomplete for accurate identiÞcation of the species, and no detailed descriptions of
the larval and pupal stages, or of the male terminalia
have been made from the type locality (Grenada). In
view of this, it becomes imperative to provide detailed
This research was performed under a Memorandum of Understanding between the Walter Reed Army Institute of Research and the
Smithsonian Institution, with institutional support provided by both
organizations.
1 Corresponding author: Walter Reed Biosystematics Unit, Museum
Support Center, MRC 534, Smithsonian Institution, 4210 Silver Hill
Road, Suitland, MD 20746 (e-mail: ruedapol@msc.si.edu).
2 Deceased.
3 Current address: Center of Biology and Management of Populations (CBGP) Ð IRD, Campus International de Baillarguet CS 30016,
34988 Montferrier, Lez Cedex. France.
descriptions of various life stages and to designate a
neotype for this important species.
From 1944 Ð1950, Þve subspecies and one variant of
An. pseudopunctipennis were morphologically described from different areas of South America, including Ecuador, Colombia, Chile, and Argentina. Three
names that were applied to this species between 1907Ð
1912 are currently in synonymy.
In the present paper, descriptions and illustrations
are provided for the adult female and male, pupa, and
larva of this species from the type locality. A male
neotype from the type locality is also designated.
Materials and Methods
Except for wing spot nomenclature, which is taken
from Wilkerson and Peyton (1990), the terminology
and abbreviations of Harbach and Knight (1980, 1982)
are used in the morphological characters and illustrations. Acronyms of type depositories are as follows:
Division de Malariologia/Instituto Nacional Para
Programas Especiales de Salud, Bogota, Colombia
(DMB), Instituto Biologie “Juan Noe,” Santiago,
Chile (IZC), Museo Argentino de Ciencias Naturales,
Buenos Aires, Argentina (MACN). Abbreviations
used are as follows: E, egg; F, female; G, genitalia;
L, larva; Le, larval exuviae; LU, location unknown;
M, male; NE, type nonexistent; P, pupa; Pe, pupal
exuviae; ssp., subspecies; var., variety. An asterisk following the abbreviation of a given life stage indicates
that part of the life stage was illustrated in the publication cited. Collection codes of the most recent collections consist of a country code in capital letters
followed by a collection number (e.g., GR-33-1 is an
individual from collection 33 from Grenada) (specimen numbers 1Ð99 are used if there are associated
larval and pupal exuviae, numbers 100 and up are used
January 2004
RUEDA ET AL.: NEOTYPE DESIGNATION AND DESCRIPTION of An. pseudopunctipennis
if there is only a pupal exuviae). Progeny from a single
female are indicated by a number in parentheses, e.g.,
GR 33(5)-1 is an individual from female number 5.
Taxonomic Treatment
Anopheles (Anopheles) pseudopunctipennis Theobald
(Figs. 1Ð3)
Anopheles pseudopunctipennis Theobald 1901: 305
(M, F). Type: Grenada (NE); Howard et al. 1917: 1020
(M*, F*, L*); Aitken 1945: 327 (M, F*, P*, L, E*,
taxonomy, biology); Vargas and Martinez Palacios
1956: 83 (M*, F*, P*, L*).
Anopheles peruvianus Tamayo 1907. In Tamayo and
Garcia 1907: 35 (M*, F*, P*, L*). Type: Huacachina,
San Pedro de Lloc, Lima, Verano, Otono, Chanchmayo, Peru (NE); Lane 1953: 160 (listed as synonym).
Proterorhynchus argentinus Brethes 1912: 15 (M, F).
Type: North Tucuman, Salta, Jujuy, Santiago del
Estero, Argentina (MACN); Howard et al. 1917: 1015
(listed as synonym); Casal, in Belkin, Schick and
Heinemann 1968: nine (lectotype desig.).
Anopheles tucumanus Lahille 1912: 253 (F*). Type:
Rio Sali, Argentina (NE); Howard et al. 1917: 1015
(listed as synonym).
Anopheles (Anopheles) pseudopunctipennis ssp.
pseudopunctipennis Theobald, Levi-Castillo 1944: 1
(M*, E*); Aitken 1945: 344; Carpenter, Middlekauff
and Chamberlain 1946: 66 (M*, F*, L*); Freeborn, in
Boyd 1949: 391; Lane 1953: 160 (M*, F*, P*, L*, E*);
Carpenter and LaCasse 1955: 46 (M* F*, L*).
Anopheles (Anopheles) pseudopunctipennis ssp. levicastilloi Levi-Castillo 1944: 1 (M*, E*; as variety).
Type: Guayasa, Ecuador (LU); Levi-Castillo 1945: 41
(M*, F, P, L*, E*; to ssp. status); Lane 1953: 160
(possible synonymy with An. (Ano.) pseudopunctipennis ssp. psuedopunctipennis).
Anopheles (Anopheles) pseudopunctipennis ssp.
rivadeneirai Levi-Castillo 1945: 33 (M*, F*, L*, E*).
Type: Provs. of Carchi, Imbabura, Pichincha, Cotopaxi, Tungurahua, Chimborazo, Canar, Azuay and
Loja; Interandian Region, Ecuador (LU); Lane 1953:
160 (possible syn. with An. (Ano.) pseudopunctipennis
ssp. psuedopunctipennis).
Anopheles (Anopheles) pseudopunctipennis ssp.
pattersoni Alvarado and Heredia 1947: 73 (E*; as var.).
Type: Tucuman, Argentina (NE); Lane 1953: 161 (to
ssp. status).
Anopheles (Anopheles) pseudopunctipennis var. bifoliata Qsorno-Mesa and Munoz-Sarmiento 1948: 105
(M*, L*, E*). Type: Florida, Valle del Cauca, Colombia (DMB).
Anopheles (Anopheles) pseudopunctipennis ssp.
neghmei Mann 1950: 34 (M, F*, L*, E*). Type:
Ouebrada de Minemine, Tarapaca, Chile (IZC).
Anopheles (Anopheles) pseudopunctipennis ssp. noei
Mann 1950: 37 (M, F, L*, E*). TYPE: Oasis de Suca,
Tarapaca, Chile (IZC).
Other Literature Records. Shannon and Davis 1927:
662Ð 678 (notes on biology, Argentina); Shannon 1930:
13
442Ð 447 (larval habitats, Peru); Hoffmann 1931: 523Ð
529 (larval habitats, Mexico); Hoffmann and Samano
1938: 182Ð192 (larval habitats, Mexico); Root and
Andrews 1938: 565Ð578 (larval habitats, Grenada);
Simmons 1941: 113Ð130 (as malaria vector, Central and
South America); Rodriguez and Loyola 1989: 15Ð 40
(as malaria vector in mountainous areas, Mexico);
Savage et al. 1990: 612Ð 619 (larval habitats, Mexico);
Rejmankova et al. 1991: 827Ð 839 (larval habitats,
Mexico), Rejmankova et al. 1993: 979 Ð991 (larval habitats, Belize); Estrada-Franco et al. 1992: 297Ð299
(cross breeding, electrophoretic analysis); EstradaFranco et al. 1993a: 735Ð745 (enzyme electrophoresis,
Mexico, Peru, Bolivia); Estrada-Franco et al. 1993b:
746 Ð755 (cross breeding, Mexico, Peru, Bolivia);
Fernandez-Salas et al. 1994 (larval habitats, Mexico);
Manguin et al. 1993: 405Ð 406 (larval habitats and
abundance, Grenada); Manguin et al. 1995: 362Ð377
(electrophoretic survey, population genetics, North,
Central and South America); Manguin et al. 1996:
620 Ð 625 (larval habitats, North, Central and South
America); Bond-Compean et al. 1998: 220 (larval habitat, Mexico); Coetzee et al. 1999: 650 Ð 652 (cross
breeding, cytogenetics, Mexico, Grenada).
Original Description
In support of previous and present interpretations
of the name pseudopunctipennis, the original description given by F. V. Theobald (1901) is as follows.
“Wings much as in An. punctipennis Say, but the
fringe with yellow spots. Legs long, unbanded, brown,
pale at the base. Fore ungues of male unequal, mid and
hind equal and simple. Female. Antenna brown, basal
joint testaceous, base of the second joint pale, and
also a small pale band at the base of all the following
joints; proboscis dark brown, labela yellowish; palpi
dark brown, densely scaled at the base, apex yellow,
and also two narrow yellow bands below, slightly
hairy, hairs black, except at the apex, where they are
yellow; clypeus dark brown. Thorax yellowish-brown
(denuded), with a dark patch on each side of the
mesonotum behind; metanotum dark brown; pleurae
yellowish brown, with darker brown patches. Abdomen brown, the segments paler at the base; hairy. Legs
deep brown, coxae, trochanters, and base of femora
pallid; knee spot pale; ungues equal and simple. Halteres with pale stem and fuscous knob. Wings with two
yellowish-white spots on the upper costal border, rest
of the edge black, rather densely scaled; Þrst submarginal cell longer and narrower than second posterior
cell, its stem nearly as long as the cell; mid cross-vein
a little nearer the base of the wing than supernumerary
cross-vein; posterior cross-vein still nearer the base of
the wing; scales of the wings disposed as follows: First
long vein with three distinct large white spots, one at
the base, one underneath the large costal spot, and one
between; second long vein with a dark patch near its
base, all the lower branch of the fork-cell dark, and
most of the upper; third long vein mostly yellowishwhite, with two black patches, one toward the base,
the other toward the tip; fourth long vein mostly pale,
14
JOURNAL OF MEDICAL ENTOMOLOGY
Vol. 41, no. 1
Fig. 1. An. pseudopunctipennis, adult. (A) Female habitus. (B) Female wing, part. (C) Male head. Scale in mm.
January 2004
RUEDA ET AL.: NEOTYPE DESIGNATION AND DESCRIPTION of An. pseudopunctipennis
15
Fig. 2. An. pseudopunctipennis. (A) Pupa cephalothorax. (B) Pupa metathorax and abdomen, left side dorsal, right side
ventral. (C) Male genitalia. Scale in mm.
16
JOURNAL OF MEDICAL ENTOMOLOGY
Vol. 41, no. 1
Fig. 3. An. pseudopunctipennis, larva. (A) Thorax and abdominal segments IÐVI, left side dorsal, right side ventral.
(B) Head, left side dorsal, right side ventral. (C) Spiracular apparatus, dorsal aspect. (D) Pecten and pecten teeth.
(E) Abdominal segments VIIIÐX, side view. Scale in mm.
January 2004
RUEDA ET AL.: NEOTYPE DESIGNATION AND DESCRIPTION of An. pseudopunctipennis
with two small black patches, branches of the fork-cell
all dark scaled; Þfth long vein with a black spot near
the base, rest mostly yellow, upper branch of the fork
mostly dark, a small yellow spot at the apex and another toward its base, lower branch mostly yellowish,
with a black apical spot; sixth vein with basal half
creamy, the apical half dark, except a small yellow
patch where it joins the wing border; fringe brown,
with a yellow spot at the junction of each vein. Length
Ð 5 mm. Male. Last two joints of the palpi swollen and
clavate, pale, basal joints dark brown, densely scaled
with deep brown scales, with a narrow pale band, not
quite as long as the thin proboscis, which is brown,
with yellow labelae; antennae gray, with narrow
brown bands and ßaxen brown hairs, apical joint about
half length of the joint; basal lobe of the genitalia
simple, claspers long and thin; fore ungues unequal,
the larger one uniserrated, the smaller minute and
simple; mid and hind ungues small, equal and simple.
Wings much as in the female, but the fork-cells
shorter. Length Ð 5 mm, with proboscis 7.5 mm.”
Supplemental Description
Below are additional characters of value in deÞning
this species.
Female (Fig. 1AÐB). Integument light to dark
brown with silvery or grayish pollinosity. Head. Interocular space with 7Ð10 (n ⫽ 12 for this and the
following measurements and counts except where indicated) long, pale setae and intermixed of long and
small, narrow, appressed white scales; vertex, occiput
and upper portion of postgena with numerous erect,
truncate scales; patch of white scales on the middle
portion of vertex; patch of dark brown to black scales
on lateral portion of vertex, occiput and upper portion
of postgena; long dark brown to black setae on ventral
portion of postgena. Clypeus bare. Pedicel of antenna
with 7Ð23 (n ⫽ 16) small, dorsolateral, narrow to
broad, grayish white spatulate scales; ßagellomere 1
with numerous narrow to broad white spatulate scales.
Scales of maxillary palpus slender, spatulate mostly
dark brown to black with intermixed dark brown setae; narrow band of white scales at base of palpomere
3, and at base and apex of palpomere 4; palpomere 5
mostly white scaled; base of maxillary palpus with
long, erect dark setae; length of maxillary palpus 1.59 Ð
2.3 mm (mean ⫽ 1.78 mm, n ⫽ 22); ratio of length of
palpomeres 2Ð5 to total length of palpus, 2 ⫽ 0.20 Ð 0.33
(mean ⫽ 0.26, n ⫽ 22), 3 ⫽ 0.32Ð 0.41 (mean ⫽ 0.37,
n ⫽ 22), 4 ⫽ 0.15Ð 0.22 (mean ⫽ 0.18, n ⫽ 22), 5 ⫽
0.08 Ð 0.13 (mean ⫽ 0.11, n ⫽ 22); ratio of palpomeres
2Ð5, 0.86 Ð 0.96 (mean ⫽ 0.92, n ⫽ 22); ratio of palpomeres 4 Ð5, 0.26 Ð 0.31 (mean ⫽ 0.29, n ⫽ 22); palpus
0.62Ð1.18 (mean ⫽ 0.99, n ⫽ 22) forefemur length.
Proboscis dark scaled, base with long, erect setae and
scales; proboscis length 1.71Ð2.10 mm (mean ⫽ 1.86
mm, n ⫽ 22); proboscis 0.97Ð1.13 (mean ⫽ 1.04, n ⫽
22) palpus length. Thorax. Scutal integument dark
brown with a broad, median longitudinal pale frosty
pruinose stripe; median stripe with narrow pale yellow
scales and setae; median anterior promontory with
17
patch of intermixed pale yellow, narrow, short and
long scales. Darker lateral portions of scutum with
longer dark setae. Scutal fossa, antealar area and supraalar area slightly pale dusted. Scutellum dark, slightly
pale dusted with 11Ð24 shorter and 13Ð24 long setae,
short setae intermixed pale yellow and dark brown,
long setae dark brown. Antepronotum with 14 Ð21
dark brown setae. Pleuron brown to dark brown; upper proepisternum with 2Ð7 setae, without scales;
prespiracular area with 1Ð 4 setae, without scales; prealar area with 4 Ð10 setae; without scales; upper mesokatepisternum with 1Ð5 setae, without scales; lower
mesokatepisternum with 1Ð 4 setae, without scales;
upper mesepimeron with 5Ð9 setae, rarely one fusiform white scale. Legs. Coxae and trochanters light to
dark yellow with pale to brown setae; hindcoxae usually with two short, fusiform, dark scales; anterior
surface of trochanter with light yellow scales; femora,
tibiae and tarsi dark; apices of femora and tibiae with
spots of pale scales. Forefemur length 1.56 Ð2.73 mm
(mean ⫽ 1.84 mm, n ⫽ 24), ratio of forefemur length
to proboscis length 0.77Ð1.53 (mean ⫽ 0.97). Wing
(Table 1). Length (measured from humeral cross
vein) 2.76 Ð3.21 mm (mean ⫽ 2.99 mm). Dark scales
brown to black, pale wing scales white and pale yellow. Vein C dark scaled from basal to sectoral area;
base of Rs white scaled; R4 ⫹ 5 with two dark spots; vein
M mostly white scaled. Anal vein (1A) with pale spots
at base and apex and dark spot (0.5 vein length) at
distal half before apex. Pale wing fringe spots present
at the distal end of each vein. Halter. Scabellum and
pedicel with pale to pale brown integument; dorsal
surface of pedicel with few pale scales at apex; capitellum dark brown to black. Abdomen. Integument
dark brown to black with some grayish pollinosity.
Terga and sterna covered with pale brown to golden
brown setae.
Male (Fig. 1C, 2C). As in female except for the
following sexual differences. Maxillary palpus
0.83Ð1.01 length of proboscis (mean ⫽ 0.91; n ⫽ 12 for
this and following measurements except where indicated), apex of palpomere 3 and all palpomere 4 and
5 enlarged. Maxillary palpus (Fig. 1C) with dark
brown and pale yellow scales; palpomere 2 with
slightly erect dark scales at base and few pale yellow
scales at apex; palpomere 3 dark scaled with pale
yellow scales at base and some pale yellow setae at
apex; palpomere 4 pale yellow scaled, inner surface
with yellowish long setae, and base and apex with few
dark scales; palpomere 5 usually totally pale yellow
with numerous yellowish short setae and few dark
short setae, sometimes with few dark scales on lateral
surface. Proboscis length 1.68 Ð2.46 mm (mean ⫽ 1.95
mm), dark brown scales; labela dark brown. Foreungues with slightly curved submedian tooth and blunt,
external basal tooth. Ninth tergal lobe (Fig. 2C) stout,
about as long as wide. Gonocoxite 1.08 Ð1.83 times as
long as wide; dorsal (postrotational) surface with
shorter and long setae, very long setae distally and
numerous very small spicules; most mesal parabasal
spines (parabasal 1) stout with slightly recurved tip,
borne on slightly raised base; parabasal 2 longer and
Ð
1 [1]
1 [1]
Ð
Ð
Ð
Ð
Ð
Ð
Ð
Ð
Ð
Ð
Ð
Ð
Ð
1 [1]
Ð
Ð
Ð
Ð
Ð
Ð
Ð
Ð
Ð
Ð
Ð
Ð
Ð
1 [1]
1 [1]
Ð
Ð
1Ð3 (2) [3]
Ð
Ð
Ð
Ð
1 [1]
Ð
Ð
Ð
Ð
1 [1]
1 [1]
1 [1]
2Ð4 (3) [3]
1Ð4 (3) [3]
1Ð4 (2) [2, 1]
1Ð3 (2) [2]
1Ð2 (1) [1]
1 [1]
3Ð5 (3) [3]
1 [1]
1Ð4 (2) [2]
1Ð3 (3) [3]
Ð
Ð
1 [1]
1 [1]
1Ð2 (1) [1]
1Ð3 (1) [3]
2Ð5 (2) [4]
1Ð2 (2) [1, 2]
1Ð3 (2) [3]
1Ð2 (1) [1]
1Ð3 (2) [3]
2Ð3 (3) [3, 2]
1 [1]
1Ð3 (2) [2, 1]
1Ð3 (1) [2]
Ð
Ð
1 [1]
1 [1]
1 [1]
1Ð3 (2) [3, 2]
1Ð5 (2) [4, 3]
1Ð5 (3) [3]
1Ð3 (2) [2]
1Ð2 (1) [1]
1Ð5 (3) [4, 3]
2Ð4 (3) [3, 2]
1 [1]
1Ð2 (1) [1]
1 [1]
Ð
Ð
1 [1]
1 [1]
1Ð3 (2) [2, 3]
2Ð3 (2) [3]
1Ð7 (6) [6, 7]
1Ð5 (1) [2, 5]
2Ð4 (3) [2, 3]
1Ð2 (1) [1]
1Ð7 (3) [3]
1Ð4 (3) [3]
1 [1]
1 [1]
1 [1]
Ð
Ð
1 [1]
1 [1]
2Ð4 (3) [2, 3]
2Ð6 (5) [6, 5]
1 [1]
1Ð3 (1) [2]
3Ð11 (6) [7, 5]
1Ð4 (3) [3]
1Ð6 (3) [6, 4]
1Ð4 (3) [4]
1 [1]
1Ð2 (1) [2]
1Ð3 (1) [1]
Ð
Ð
1 [1]
1 [1]
3Ð6 (4) [4]
3Ð6 (5) [5]
1Ð2 (1) [1]
1Ð8 (1) [8]
3Ð7 (5) [6, 5]
1Ð2 (1) [1, 2]
1Ð4 (2) [2, 3]
Ð
1 [1]
1Ð2 (1) [1]
1Ð2 (1) [1]
Ð
Ð
1 [1]
Ð
10Ð20 (12) [18, 20]
1Ð7 (5) [6, 5]
1Ð5 (3) [2, 1]
3Ð10 (5) [7]
1Ð3 (2) [2, 3]
1 [1]
1Ð5 (1) [Ð]
Ð
1 [1]
Ð
Ð
Ð
Ð
Ð
IX
VIII
Ð
1Ð3 (1) [1]
1Ð2 (1) [1]
1Ð3 (1) [1, 2]
1Ð2 (1) [1]
1Ð3 (1) [1]
1Ð2 (1) [1, 2]
1 [1]
1Ð3 (2) [2]
1 [1]
1Ð2 (1) [2, 1]
1Ð4 (1) [4, 1]
1Ð3 (2) [3, 1]
Ð
Ð
more slender than 1; parabasal 1 base 0.24 Ð 0.36 from
base of gonocoxite; parabasal 2 base 0.20 Ð 0.33 from
base of gonocoxite; internal setae slender, longer than
parabasal 1, base 0.51Ð 0.72 distance from base of gonocoxite. Claspette. Dorsal lobe of claspette (Fig. 2C)
with three overlapping bladelike apical Þlaments, and
ventral lobe with two long slender apical setae and a
short weak subapical seta; remainder of ventral lobe
and area between it and dorsal lobe with numerous
prominent short spicules. Aedeagus cylindrical, broad
and furcate at base; two pairs of aedegeal leaßets at
apex; leaßets slender, slightly curved and serrated.
Gonostylus 1.06 Ð1.48 length of gonocoxite; many
minute setae on dorsal side of gonostylus; gonostylar
claw short and blunt. The descriptive statistics for
ratios of male neotype costal and subcostal wing spot
lengths/length of wing measured from humeral crossvein are shown in brackets in Table 1.
Pupa (Fig. 2AÐB). Position and development of
setae as Þgured; range and modal number of branches,
and number of branches of male neotype shown in
Table 2. Exuviae colorless to light brown. Cephalothorax. Trumpet simple with deep meatal cleft; length
0.44 Ð 0.56 mm (mean ⫽ 0.51 mm, n ⫽ 24 for this and
the following measurements and counts except where
indicated), width 0.11Ð 0.16 mm (mean ⫽ 0.13 mm,
measured at base of pinna), index 2.99 Ð 4.24 (mean ⫽
3.85); pinna evenly rounded distally. Abdomen. Seta
6-I simple, slender; 7-I with 1Ð5 branches; 9-I simple,
slender, shorter than 6-I. Seta 1-II-VII well developed;
8-II absent; 9-II simple, slender; 9-III short, pointed
0.41Ð1.00 (mean ⫽ 0.68) length of 9-II; 9-IV strong,
pointed, 0.94 Ð2.12 (mean ⫽ 1.54) length of 9-III; 9-VVIII long, pointed, spine-like; 9-V 1.37Ð2.88 (mean ⫽
1.90) length of 9-IV; 9-VI 0.97Ð1.52 (mean ⫽ 1.19)
length of 9-V; 9-VII 1.00 Ð1.43 (mean ⫽ 1.22) length of
9-VI; 9-VIII 0.69 Ð1.69 (mean ⫽ 0.99) length of 9-VII;
9-VI 0.23Ð 0.42 (mean ⫽ 0.37) length of segment VI;
9-VII 0.35Ð 0.60 (mean ⫽ 0.44) length of segment VII;
9-VIII 0.30 Ð 0.65 (mean ⫽ 0.39) length of segment
VIII. Segment VII 0.76 Ð1.11 (mean ⫽ 1.01) length of
0
1
2
3
4
5
6
7
8
9
10
11
12
13
14
a
Fourteen wings from the neotype and alloneotype, and 12 individuals; male neotype is shown in brackets.
VII
0.13 ⫾ 0.02 [0.14]
0.11 ⫾ 0.01 [0.11]
0.19 ⫾ 0.02 [0.20]
0.08 ⫾ 0.02 [0.07]
0.21 ⫾ 0.03 [0.15]
0.06 ⫾ 0.02 [0.09]
0.03 ⫾ 0.00 [0.02]
VI
0.10Ð0.17
0.08Ð0.13
0.16Ð0.23
0.07Ð0.11
0.15Ð0.25
0.02Ð0.09
0.02Ð0.03
V
0.09 ⫾ 0.01 [0.08]
0.22 ⫾ 0.02 [0.20]
0.07 ⫾ 0.01 [0.10]
0.03 ⫾ 0.01 [0.03]
Abdominal segments
0.07Ð0.10
0.19Ð0.25
0.05Ð0.10
0.02Ð0.03
IV
0.69 ⫾ 0.06 [0.75]
III
0.57Ð0.79
II
Mean ⫾ SD
I
Vein C
Basal dark to sector dark
(BD⫹PHD⫹HD⫹PD⫹SD)
Subcostal pale (SCP)
Preapical dark (PD)
Preapical pale (PP)
Apical dark (AD)
Vein R-R1
Presector dark (PSD)
Sector pale (SP)
Sector dark (SD)
Subcostal pale (SCP)
Preapical dark (PD)
Preapical pale (PP)
Apical dark (AD)
Range
Cephalothorax
CT
Wing spot
Seta
no.
Table 1. An. pseudopunctipennis: descriptive statistics for ratios of veins C and R-R1 wing spot lengths/length of wing measured
from humeral crossveina
Vol. 41, no. 1
Paddle
Pa
JOURNAL OF MEDICAL ENTOMOLOGY
Table 2. Pupal setal branching for An. pseudopunctipennis: range mode (in parentheses) based on counts made on 14 –26 setae of the neotype, alloneotype, and 24 specimens collected with them;
male neotype is shown in brackets
18
January 2004
RUEDA ET AL.: NEOTYPE DESIGNATION AND DESCRIPTION of An. pseudopunctipennis
19
Table 3. Larval setal branching for An. pseudopunctipennis: range mode (in parentheses) based on counts made on 12–22 setae of
the neotype and alloneotype, and 20 specimens collected with them; male neotype is shown in brackets
Seta
no.
Head
Thorax
0
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
Ð
1 [1]
1 [1]
1 [1]
1 [1]
16Ð23 (20) [22]
15Ð18 (16) [18]
16Ð26 (25) [24, 25]
3Ð6 (4) [3, 4]
3Ð8 (4) [4]
2Ð5 (4) [4, 2]
23Ð37 (31) [35, 27]
3Ð7 (6) [4, 6]
1Ð7 (1) [7]
10Ð18 (16) [17, 15]
13Ð22 (16) [13]
C
P
Abdominal segments
M
T
I
II
III
Ð
Ð
Ð
Ð
1 [1]
1 [1]
1Ð2 (1)
28Ð44 (36)
1 [1]
2Ð4 (2) [4]
1Ð6 (2) [5]
10Ð17 (15) [16, 17]
5Ð11 (8) [5]
1
1 [1]
2Ð4 (3) [2, 3]
3Ð6 (5) [5, 4]
2Ð4 (3) [4]
1 [1]
1 [1]
1 [1]
1 [1]
1 [1]
1 [1]
12Ð19 (12) [18]
1 [1]
2Ð3 (3) [2]
4Ð5 (5) [5]
3Ð6 (6) [5, 6]
2Ð6 (3) [3]
17Ð28 (24) [21]
2Ð4 (4) [4] 21Ð58 (44) [49]
3Ð8 (5) [5]
5Ð7 (7) [5, 7]
4Ð9 (7) [5]
1 [1]
3Ð5 (4) [3]
2Ð6 (3) [5] 35Ð53 (38) [41, 36] 41Ð49 (49) [49]
35Ð49 (41) [37, 41]
15Ð30 (15) [30]
5Ð8 (7) [8] 30Ð53 (38) [Ð] 32Ð46 (42) [45, 42] 42Ð48 (44) [43, 48]
2Ð5 (3) [2, 3]
26Ð44 (44) [35, 39] 10Ð15 (12) [15] 36Ð58 (42) [42]
Ð
2Ð4 (3) [2]
2Ð4 (3) [2, 4]
1 [1]
1 [1]
1 [1]
4Ð6 (4) [4]
5Ð9 (8) [5, 2]
3Ð7 (7) [4, 7]
1 [1]
1 [Ð]
1 [1]
2Ð5 (3) [3]
2Ð3 (2) [2, 3]
1Ð3 (1) [2, 3]
1 [1]
1 [1]
1 [1]
2Ð5 (3) [5]
2Ð4 (2) [4]
2Ð3 (3) [2, 3]
1 [1]
2Ð3 (2) [2]
1Ð3 (1) [1]
1Ð3 (1) [1]
1Ð3 (1) [1, 3]
1Ð4 (2) [4, 1]
Ð
9Ð13 (12) [9]
2Ð3 (2) [2]
2Ð3 (3) [3]
3Ð5 (3) [3]
3Ð4 (3) [3]
5Ð8 (7) [6]
8Ð20 (8) [8]
Ð
Ð
Ð
1 [1]
Ð
Ð
Ð
Ð
Ð
Ð
Abdominal segments
Seta
no.
IV
V
VI
VII
VIII
X
0
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
1 [1]
14Ð18 (16) [17, 18]
1 [1]
1Ð4 (4) [4]
2Ð4 (2) [2]
3Ð6 (5) [5]
5Ð10 (8) [10, 9]
2Ð4 (3) [3]
2Ð4 (2) [4, 3]
3Ð6 (5) [4, 5]
1Ð3 (2) [1, 2]
1Ð4 (2) [4, 1]
1Ð3 (1) [1, 3]
3 [3]
1 [1]
Ð
1 [1]
14Ð18 (16) [15, 14]
1 [1]
3Ð4 (3) [3]
3Ð5 (5) [4, 5]
3Ð6 (4) [4, 6]
5Ð8 (5) [7, 8]
2Ð5 (3) [4, 3]
3Ð4 (3) [3]
3Ð5 (5) [5, 4]
1Ð5 (3) [3]
2Ð4 (3) [3]
1Ð3 (2) [3]
3Ð5 (3) [5, 4]
1 [1]
Ð
1 [1]
13Ð18 (16) [17, 18]
1Ð2 (2) [2]
1 [1]
1 [1]
4Ð7 (5) [5]
4Ð7 (6) [4, 5]
3Ð4 (3) [3]
3Ð4 (3) [Ð]
1 [1]
2Ð4 (3) [4]
1Ð4 (2) [4]
1Ð3 (3) [1]
8Ð13 (12) [13]
1 [1]
Ð
1 [1]
14Ð16 (15) [15, 14]
2Ð4 (4) [4]
2Ð3 (3) [3]
1Ð2 (2) [2]
4Ð5 (5) [4]
3Ð6 (3) [6]
2Ð4 (3) [3]
3Ð8 (7) [3]
1 [1]
3Ð5 (5) [3]
1Ð3 (2) [1]
2Ð3 (3) [3]
3Ð6 (4) [3]
1 [1]
Ð
1 [1]
1Ð3 (3) [2, 3]
3Ð5 (5) [5]
4Ð6 (5) [4, 5]
1Ð3 (1) [3, 2]
2Ð5 (4) [4, 5]
1-S
2-S
6-S
7-S
8-S
9-S
Ð
Ð
1Ð3 (1) [3]
Ð
Ð
1 [1]
16Ð51 (18) [19]
6Ð22 (6) [12]
9 [9]
Ð
2Ð6 (4) [2]
3Ð5 (4) [Ð]
1Ð2 (2) [2]
1 [1]
3Ð5 (3) [5]
2Ð4 (3) [3]
Ð
Ð
Ð
Ð
C, head; P, prothorax; M, mesothorax; T, metathorax.
segment VI; segment VIII 1.00 Ð1.24 (mean ⫽ 1.11)
length of segment VI; segment VIII 1.00 Ð1.63 (mean ⫽
1.12) length of segment VII. Segment VII 0.76 Ð1.11
(mean ⫽ 1.01) width of segment VI (width at posterior margins); segment VIII 1.00 Ð1.24 (mean ⫽ 1.12)
width of segment VI; segment VIII 1.00 Ð1.63 (mean ⫽
1.12) width of segment VII. Width/length of segment
VI 1.94 Ð2.71 (mean ⫽ 2.36), VII 1.79 Ð3.30 (mean ⫽
2.22), VIII 1.67Ð2.02 (mean ⫽ 1.89). Paddle length
0.74 Ð 0.96 mm (mean ⫽ 0.87 mm, n ⫽ 13), width
0.54 Ð 0.69 mm (mean ⫽ 0.61 mm, n ⫽ 13), length/
width ratio 1.32Ð1.56 (mean ⫽ 1.44, n ⫽ 13) somewhat
oval; refractile index 0.82Ð 0.94 (mean ⫽ 0.90, n ⫽ 13);
length of marginal spicules 0.01Ð 0.04 mm (mean ⫽
0.02 mm, n ⫽ 13).
Larva (Fig. 3). Position and development of setae as
Þgured; range and modal number of branches and
number of branches of male neotype as shown in
Table 3. Head. Lightly pigmented, particularly in the
middle part; length 0.80 Ð 0.94 mm (mean ⫽ 0.87 mm,
n ⫽ 11), width 0.56 Ð 0.78 mm (mean 0.72 mm, n ⫽ 11).
Antennal length 0.24 Ð 0.30 mm (mean ⫽ 0.27 mm, n ⫽
12), slightly tapered toward apex, 5.67Ð 8.67 (mean ⫽
6.76, n ⫽ 12) longer than wide; with 11Ð19 (mode ⫽
14, n ⫽ 18) spicules on mesal and ventral surfaces;
spicule length 0.01Ð 0.02 mm (mean ⫽ 0.01 mm, n ⫽
23). Seta 1-A single, slender, 0.04 Ð 0.08 mm (mean ⫽
0.07 mm, n ⫽ 12), inserted 0.34 Ð 0.42 (mean ⫽ 0.37)
from base of antenna; 2,3-A single, pointed; 4-A with
2Ð5 branches (mode ⫽ 3, n ⫽ 13); 5-A short, spine-like,
0.15Ð 0.60 (mean ⫽ 0.32, n ⫽ 12) length of seta 1-A; 6-A
spine-like ⬇2Ð3 times longer than seta 5-A. Seta 2-C
single 1.00 Ð1.53 (mean ⫽ 1.27, n ⫽ 12) length of 3-C;
seta 2-C almost close to mate of opposite side 0.02Ð 0.03
mm (mean ⫽ 0.03 mm, n ⫽ 11); 3-C single, 0.66 Ð1.00
(mean ⫽ 0.80, n ⫽ 12) length of 2-C, clypeal index
(distance between bases 2-C and 3-C on one side/
distance between bases of 2-C) 1.75Ð3.00 (mean ⫽
3.07, n ⫽ 12). Thorax. Seta 1-P single or double; 9 Ð12-P
single; 9 Ð12-P setal support plate spine length 0.05
mm. Seta 9 Ð11-M single; 9-M 2.00 Ð2.20 (mean ⫽ 2.09,
n ⫽ 7) length 10-M; seta 12-M with 2Ð3 branches;
9 Ð12-M setal support plate spine length 0.08 Ð 0.13 mm
(mean ⫽ 0.10 mm, n ⫽ 13). Seta 9 Ð11-T single; 9-T
2.02Ð2.40 (mean ⫽ 2.17, n ⫽ 10) length of 10-T; seta
12-T with 1Ð3 branches; 9 Ð12-T setal support plate
spine length 0.08 Ð 0.13 mm (mean ⫽ 0.09 mm, n ⫽ 12);
13-T with 2Ð3 branches. Abdomen. Seta 1-I with 2Ð 4
branches (mode 2, n ⫽ 12); 1-II single or with 2Ð 6
branches (mode ⫽ 2, n ⫽ 12) arising on the distal half.
20
JOURNAL OF MEDICAL ENTOMOLOGY
Seta 1-III-VII palmate with well developed leaßets,
each leaßet with short Þlament; 0-II-VIII, 14-III-VIII
weakly developed; 0, 8, 14-I, 14-II absent or rare;
3-I-III, VI single; 3-IV, V, VII, VIII branched; 6-II-VII
branched. Anterior tergal plates on segments III-VIII
small, ⬇0.20 width of the segment, not enclosing small
median posterior plate. Seta 1-X single, long, 0.92Ð1.67
(mean ⫽ 1.27, n ⫽ 11) length of saddle; 1-X inserted
on saddle. Saddle with minute, sparse spicules on lateral surface. Integument of posterior margin of segment X with strongly developed, dark spicules. Setae
2Ð3-X with hook-like tips that are used to hold the
larvae on substrate in a water current. Spiracular apparatus. Pecten plate with 12Ð18 spines; arrangement
of spines alternating long and short, with 5Ð10
(mode ⫽ 7, n ⫽ 20) long spines and 4 Ð9 (mode ⫽ 7,
n ⫽ 20) short spines; long spines 1.67Ð5.40 (mean ⫽
2.92, n ⫽ 38) length of short spines. Two posterolateral
spiracular lobe plates each with elongate, slender,
sclerotized projection or “tail” from inner caudal margin. Table 3 also shows the range and modal number
of branches of siphon setae (1, 2, 6 Ð9-S).
Type Material. Neotype: Male with associated slide
mounted larval and pupal exuviae and slide mounted
genitalia, from the progeny brood of a female captured
on human bait, data as follows: Grenada, Rio Sallee,
Chambord Estate, S. Manguin, and E. L. Peyton Coll.
13 April 1992, 12⬚ 12⬘ N, 61⬚ 37⬘W, collection and
specimen no. GR 30(1)-2. Deposited in the National
Museum of Natural History, Smithsonian Institution,
Washington, DC. (WRBU ACC No. 1539/WRBU/
USUHS). Alloneotype: Female with associated slide
mounted larval and pupal exuviae, collection and
specimen no. GR 30(1)-3, with same collection data as
male neotype.
Other Material Examined. A total of 182 specimens
in the National Museum of Natural History, Smithsonian Institution, Washington, DC, consisting of 50
females, 36 males, 48 pupal exuviae, 27 larval exuviae,
14 larvae, and 7 male genitalia.
Grenada. Rio Sallee, St. Patrick, E. L. Peyton coll.,
13 April 1992, 12o 12⬘ N, 61o 37⬘W. GR 29 Ð23 M PeLe;
GR 29 Ð33 M; GR 29 Ð36 M; GR 29 Ð37 F; GR 29 Ð108 M;
GR 30(1)-1 M PeLe; GR 30(1)-100 M Pe; GR 30(1)101 F Pe; GR 30(1)-102Ð103 M Pe; GR 31 L;
GR 31Ð3 PeLe; GR 31Ð17 F; GR 31Ð35-38 F; GR 31Ð113
M Pe; GR 31Ð114 Pe; GR 31Ð115 Pe; GR 31Ð116 F Pe;
GR 31Ð117-120 M Pe; GR 31Ð121-129 Pe; GR 31Ð131 F
Pe; GR 31Ð132 Pe; GR 31Ð134-135 M Pe; GR 31Ð137 Pe;
GR 31Ð138 M Pe; GR 31Ð137 M; GR 31Ð141 M Pe;
GR 31Ð142-144 Pe; GR 31Ð145-149 M Pe; GR 33 L; GR
33(1) L; GR 33Ð1 PeLe; GR 33Ð2-6 F PeLe;
GR 33Ð7 PeLe; GR 33Ð 8 F; GR 33Ð9 F PeLe; GR 33Ð10
F; GR 33Ð11-12 M PeLe; GR 33Ð13-15 PeLe; GR 33Ð
17-19 PeLe; GR 33Ð20 M PeLe; GR 33Ð21-24 F PeLe;
GR 33Ð25-26 F; GR 33Ð27 PeLe; GR 33Ð28 F PeLe;
GR 33Ð100-118 Pe; GR 33Ð117 M; GR 33Ð119 M;
GR 33Ð121-128 F; GR 33Ð129-130 M; GR 33Ð132-134 F;
GR 33Ð133-134 F; GR 33Ð135-136 M; GR 33Ð137-139 F;
GR 33Ð140 M; GR 33Ð142 F; GR 33Ð143 M; GR 33Ð145
F; GR 33Ð146 M; GR 33Ð147-153 F; GR 33Ð154 M;
GR 33Ð155-156 F; GR 33Ð158-160 M. Soubise River,
Vol. 41, no. 1
St. Andrew, W. A. Hoffman coll., 26 August 1929, LAR
41, 710106 Ð3, 4, 5, 6 G; LAR 41, 710201Ð1 G; Chambord
Mineral Spring, St. Patrick, LAR 48, 710201Ð 4 G; R.
Martinez, coll., 28 October 1963, Queens Park Oval,
St. George, GR 90, 710106 Ð3 G.
Distribution. Argentina, Belize, Bolivia, Chile, Colombia, Costa Rica, Ecuador, El Salvador, Grenada,
Guatemala, Haiti, Honduras, Mexico, Nicaragua, Panama, Peru, Trinidad and Tobago, United States, Venezuela.
Medical Importance. Through out its range, An.
pseudopunctipennis is generally the most important
vector of malaria in mountainous areas during the dry
season (Shannon et al. 1927, Aitken 1945, Rodriguez
and Loyola 1989). It transmits malaria in highly elevated areas up to 2,800 m in Bolivia (Hackett 1945,
Gorham et al. 1973). It is also the dominant malaria
vector in seven of 19 (37%) countries with endemic
malaria (Pan American Health Organization 1994),
including Argentina, Bolivia, Ecuador, Guatemala,
Mexico, Nicaragua, and Peru (Manguin et al. 1996).
Bionomics. The larvae of An. pseudopunctipennis
are found in a variety of habitats but they occur frequently in sun-exposed freshwater stream pools
containing Þlamentous green algae (e.g., Spirogyra,
Oedogonium, Cladophora, Closterium, Enteromorpha)
and aquatic vegetation with clear, shallow, and stagnant water (Manguin et al. 1996). The green algae
provide oviposition substrates for gravid adult females
as well as food and shelter for the mosquito larvae.
Larval habitats are common in dry environments in
valleys and foothills. Larvae are tolerant of water temperature ßuctuations and drought. This species is most
abundant during the dry season. Larval abundance is
usually negatively associated with seasonal rainfall.
Heavy rains cause rivers and tributaries to rise suddenly and transform into rapidly ßowing waters. As a
consequence, typical oviposition and larval breeding
sites such as ßood-plain pools, stream margins, and
ditches are destroyed by excessive ßooding. Alternative larval habitats include spring-seepages, ground
pools, lagoons, rock pools, artiÞcial containers (e.g.,
reservoirs, tanks, fountains, well holes), rice paddies,
and marshy meadows. Larvae are found in habitats
with acidic, neutral and alkaline water (pH 4.5Ð 8.8),
freshwater to brackish water (conductivities from below 650 up to 8,350 uS), at elevations as low as sea level
up to 3,200 m. Adult females are highly anthropophilic
and they enter houses readily for shelter. The indoor
resting females usually attack humans. They also feed
freely outdoors on humans, cattle, horses, and other
animals.
Discussion
Although Theobald (1901) provided the original
description of An. pseudopunctipennis, it was not sufÞcient for accurate identiÞcation of the species. This
resulted in confusions and misidentiÞcations of the
species in many parts of its geographical range in
North, Central, and South America (Manguin et al.
January 2004
RUEDA ET AL.: NEOTYPE DESIGNATION AND DESCRIPTION of An. pseudopunctipennis
1993). The morphological information in this paper
may help in solving those problems.
Anopheles pseudopunctipennis has the following diagnostic features. Adult female: Maxillary palpus has
palpomere 5 mostly white scaled; base of wing vein Rs
white scaled; vein M predominantly pale scaled. Adult
male: The male terminalia has dorsal lobe of claspette
with three overlapping bladelike apical Þlaments.
Aedeagus is cylindrical, broad and furcate at base; two
pairs of aedegeal leaßets at apex; leaßets slender,
slightly curved, and serrated. Larva: The spiracular
apparatus has two posterolateral spiracular lobe plates
each with elongate, slender, sclerotized projection or
“tail” from inner caudal margin. Seta 2-IV single; 3-C
single; 9-M and 9-T about twice the length of 10-M and
10-T. Detailed comparisons of pupal characters of
An. pseudopunctipennis and related species are needed
to further clarify species differences. Other morphological features described in this paper for larva, pupa,
and adults may be used to separate An. pseudopunctipennis from related species.
The status of An. pseudopunctipennis as a single
species or a species complex is controversial and confusing (Estrada-Franco et al. 1992, 1993a, 1993b; Manguin et al. 1995; Munstermann 1995; Coetzee et al.
1999). Manguin et al. (1995) conducted a comprehensive electrophoretic survey of 42 populations of
this species collected from 10 countries in North,
Central, and South America throughout its geographic
distribution. They found no Þxed electromorphic differences separating the populations of the species.
Based on the isoenzme analyses, however, they found
three geographic populations of An. pseudopunctipennis, with Grenada (type-locality) populations as a distinct one. Estrada-Franco et al. (1992, 1993a, 1993b)
found genetic differences among geographic strains of
An. punctipennis in neotropical America, and they suggested the presence of at least allopatric sibling species
in the region. Coetzee et al. (1999) suggested a third
species of An. pseudopunctipennis complex based on
cytogenetic tests of mosquito populations from
Mexico and Grenada.
With the designation of neotype and detailed descriptions of various life stages of An. pseudopunctipennis, future studies may be conducted using various
tools, including morphological, molecular, or biochemical, to solve the complexity of this widespread
species. Because of its major involvement in malaria
transmission, there is an urgent need to clarify the
taxonomy of An. pseudopunctipennis complex, if multiple species exist, through comparisons of various
populations of mosquitoes from different countries of
North, Central and South America.
Acknowledgments
We thank Bruce A. Harrison, Richard C. Wilkerson, YiauMin Huang, and Jan E. Conn for reviewing the manuscript
and providing invaluable advice. E. L. Peyton (deceased)
initiated this research project but was unable to continue
because of his illness and early death. Thanks also to Taina
R. Litwak for her illustrations, and Ralph E. Harbach for
21
checking and conÞrming the nonexistent of type specimens
of the An. pseudopunctipennis in the Natural History Museum, London. Jim Pecor provided technical support in the
curation of specimens and preparation of slide mounts.
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Received for publication 3 October 2002; accepted 3 September 2003.