Parasitology, Harold W. Manter Laboratory of
Faculty Publications from the Harold W.
Manter Laboratory of Parasitology
University of Nebraska - Lincoln Year
A New Species of Dipetalonema
(Filarioidea: Onchocercidae) from Ateles
chamek from the Beni of Bolivia
F. Agustin Jimenez-Ruiz
Scott Lyell Gardner
Centro de Estudios Parasitolo´gicos y de Vectores, firstname.lastname@example.org
Southern Illinois University, Carbondale, email@example.com
University of Nebraska - Lincoln, firstname.lastname@example.org
This paper is posted at DigitalCommons@University of Nebraska - Lincoln.
J. Parasitol., 93(3), 2007, pp. 661–667
American Society of Parasitologists 2007
A NEW SPECIES OF DIPETALONEMA (FILARIOIDEA: ONCHOCERCIDAE) FROM
ATELES CHAMEK FROM THE BENI OF BOLIVIA
Juliana Notarnicola, F. Agustı´n Jime´nez*, and Scott L. Gardner*
Centro de Estudios Parasitolo´gicos y de Vectores–CEPAVE–CONICET–UNLP, Calle 2 Nu´mero 584 (1900) La Plata, Argentina.
: We describe a new species of Dipetalonema occurring in the body cavity of Ateles chamek (Humboldt, 1812) from
north-central Bolivia. Morphologic characters serving to separate Dipetalonema yatesi n. sp. from known forms include a vagina
vera with a simple tube and thin walls and a left spicule, which possesses a handle shorter than the lamina (ratio 2.7); the latter
displays an anterior membranous alae similar in length to the terminal ﬂagellum, a distal extremity of the left spicule within a
simple hook and a membrane, phasmids at the basis of the lappets, and heterogeneous muscles occupying the whole cavity.
Dipetalonema yatesi n. sp. can be separated from Dipetalonema robini, Dipetalonema gracile, and Dipetalonema graciliformis,
between other characters, in having a simple vagina vera instead of a sinuous one, and from Dipetalonema caudispina and
Dipetalonema freitasi in having the lamina of the left spicule divided in a membranous alae and a terminal ﬂagellum.
While carrying out expeditionary research on the biodiversity
of mammals and their parasites of Bolivia by joint collecting
teams from the Museum of Southwestern Biology, the Ameri-
can Museum of Natural History, and the Coleccio´n Boliviana
de Fauna, small- and medium-sized mammals were collected
and examined for parasites (Gardner and Campbell, 1992; An-
derson, 1997). During our work in the Departamento de Beni
in 1985, one of us (S.L.G.) had the opportunity to examine a
specimen of Ateles sp. E
. Geoffroy Saint-Hilaire, 1806 (Pri-
mates: Cebidae) that had been collected by local Chimane hunt-
ers. Herein, we report on the ﬁlarioid nematodes discovered at
necropsy of this single individual spider monkey.
Spider monkeys, Ateles spp., have a wide distribution in the
Neotropics, with Ateles geoffroyi Kuhl, 1820, reaching a north-
ern limit of its range in the lowlands of southern Veracruz State
in Mexico. Six species are included in the genus, with only
Ateles chamek (Humboldt, 1812) known to be from Bolivia
(Anderson, 1997). Ateles chamek usually occurs in undisturbed
primary forests in southeastern Peru, western Brazil, and in the
lowlands of eastern Bolivia in the Amazon basin (Anderson,
1997; Eisenberg and Redford, 1999).
Several gastrointestinal parasites, e.g., pinworms, hook-
worms, whipworms, and protozoans, have been reported from
species of Ateles in Panama, Guyana, and other Central and
South American countries (Hugot et al., 1996; Thoisy et al.,
2000; Phillips et al., 2004). Filarioid nematodes were reported
from the body cavity of Ateles spp. by Freitas (1943) and Ca-
ballero (1947). From Bolivia, Freitas (1964) ﬁrst reported Di-
petalonema gracile (Rudolphi, 1809) in Cebus capucinus (L.);
Karesh et al. (1998) also reported this species from a single
specimen of A. chamek (originally mentioned as Ateles paniscus
chamek; see Anderson, 1997) from Parque Nacional Noel
Kempff Mercado in northeastern Bolivia. Karesh et al. (1998)
also reported an unidentiﬁed species of Strongyloides, lice eggs,
and evidence of previous infections with spirochaetes (Lepto-
spira sp.) and viruses, including those causing encephalitis and
MATERIALS AND METHODS
A single specimen of A. chamek shot by hunters was prepared as a
study specimen by Luis Ruedas and examined for parasites by S.L.G.
Received 3 June 2006; revised 23 August 2006, 25 October 2006;
accepted 22 November 2006.
* The Harold W. Manter Laboratory of Parasitology, University of Ne-
braska State Museum, Lincoln, Nebraska 68588-0514.
on 28 August 1985. The thoracic and abdominal cavities of the monkey
were searched for parasites following the general methods of Gardner
(1996). Filarioid nematodes, found only among the mesenteries in the
abdominal cavity, were washed in saline, ﬁxed in cold 10% formalin
solution, and stored in 70% ethanol (see Gardner, 1996). For light mi-
croscopy, specimens were cleared in lactophenol and mounted on a
microscope slide. A cross section of the anterior end of a female was
made to obtain an en face view. Lateral chords and the disposition of
the muscles were observed in a midbody cross section from both male
and female worms. Microﬁlariae were obtained via dissection of the
uterus of a mature female specimen. Drawings were made with a Wild
microscope equipped with a drawing tube.
Measurements were taken directly from specimens, either with an
ocular micrometer or with digital measuring software (Jandel Sigma
Scan Pro, San Rafael, California; Albinger et al., 1995), with a Zeiss
Ultraphot microscope. Measurements are given in micrometers, unless
otherwise stated. For each character, we give the mean value followed
by the standard deviation and the range in parentheses (Sokal and Rohlf,
1995). We also give the measurements from 1 small-sized specimen and
note that it is a juvenile male.
Specimens prepared for scanning electron microscopy (SEM) were
treated with osmium–thiocarbohydrazide–osmium–thiocarbohydrazide–
osmium (OTOTO), dehydrated in 100% ethanol, dried to a nonliquid
state by critical-point drying using CO
, attached to an SEM stub, and
sputter-coated with gold palladium.
For comparative purposes, we examined specimens of Dipetalonema
gracile collected from Ateles chamek (syn. Ateles paniscus chamek; see
Anderson, 1997) from Parque Nacional Noel Kempff Mercado, Bolivia.
The specimens are deposited in the U.S. National Parasite Collection
Dipetalonema yatesi n. sp.
General: Long, whitish worms. Anterior end blunt, posterior end ta-
pering to a point. Vulva at level of esophagus; esophagus divided into
anterior muscular and posterior glandular portions. Papillae on cephalic
plate arranged in a dorso-ventrally ﬂattened rectangle. Caudal extremity
with subterminal lappets.
Male: Labial papillae rectangular pattern 50 by 20; cephalic papillae
rectangular pattern 90 by 35 (Figs. 1, 2, 23). Additional male, 60 by
25 and 90 by 40, respectively. One male with labial papilla displaced
to axis of buccal opening (Fig. 24). Cuticular axis of right spicule with
subterminal curve; distal extremity ending in a simple hook with a
membrane (Figs. 8, 10, 11). Left spicule with handle shorter than lam-
ina; lamina with proximal membranous alae and distal ﬁlament or ﬂa-
gellum; membranous alae and ﬂagellum similar in length (Figs. 4, 6,
7). Gubernaculum present. Area rugosa, extending through coiled re-
gion, including tail, formed by rows of small longitudinal crests (Fig.
26). Precloacal area rugosa consisting of 1 ventral band (Fig. 28); po-
stcloacal area rugosa formed by 2 subventral bands; left band ends far
more posteriorly than right band (Fig. 25). Five pairs of genital papillae
arranged in 2 adcloacal rows, a single precloacal papilla, and a sub-
662 THE JOURNAL OF PARASITOLOGY, VOL. 93, NO. 3, JUNE 2007
1–12. Dipetalonema yatesi n. sp. Male. (1–2) Anterior extremity median and lateral views, respectively. (3) Detail of anterior end of
testis and the esophagus-intestinal junction. (4) Posterior extremity, lateral view, showing the entire left spicule, the right spicule, and the
gubernaculum. (5) Tail, lateral view. (6–7) Left spicule. (6) Handle, lateral view. (7) Lamina showing the membranous alae and the beginning of
the ﬂagellum, lateral view. (8) Right spicule, lateral view. (9) Gubernaculum. (10–11) Distal extremity of a dissected right spicule. (10) Dorso-
lateral view. (11) Dorsal view. (12) Midbody cross section showing the muscles.
NOTARNICOLA ET AL.—A NEW FILARIOID FROM BOLIVIA 663
13–22. Dipetalonema yatesi n. sp. Female. (13) Anterior end showing relative position of nerve ring and vulva. (14–16) Anterior
extremity, median, lateral, and en face views, respectively. (17–18) Vagina vera, lateral and ventral views. (19) Posterior extremity, ventral view
showing the lappets. (20) Cross section posterior to the vulva. (21) Tail, lateral view. (22) Uterine microﬁlaria.
664 THE JOURNAL OF PARASITOLOGY, VOL. 93, NO. 3, JUNE 2007
23–29. Dipetalonema yatesi n. sp. Male scanning electron photography. (23–24) En face view of the anterior end showing labial
papillae (white thin arrows), cephalic papillae (black thin arrows), and amphids (white thick arrows). (24) Male with an abnormal distribution of
labial papillae (white arrow). (25) Posterior extremity showing the 2 subventral bands of the postcloacal area rugosa, the white arrow marks the
end of the right band. (26) Posterior extremity coiled showing the area rugosa. (27) Cloacal region showing the papillae, the precloacal area
rugosa constituted with 1 band, and the postcloacal area rugosa with 2 subventral bands. (28) Detail of the area rugosa at midlength. (29) Posterior
extremity showing the lateral papillae (thin white arrow), the median papillae (thick arrows), and the lappets (black arrow).
NOTARNICOLA ET AL.—A NEW FILARIOID FROM BOLIVIA 665
30–32. Dipetalonema yatesi n. sp. Female scanning elec-
tron photography. (30) Detail of vulva. (31–32) Posterior extremity
showing the caudal lappets (black arrow), and the phasmid opening
(white arrow), lateral and ventral views, respectively.
medial postcloacal pair (Fig. 27). Four caudal papillae, 2 submedial and
4 sublateral (Fig. 29). Caudal lappets situated 25–35 from posterior end.
Large muscles in heterogeneous packs, smaller in dorsal and ventral
ﬁelds, longer at lateral ﬁelds, occupying the whole cavity and drawing
up the boundaries of a rhomb (Fig.12).
Holotype: Length 111.9 mm; width 272; nerve ring 150 from apex;
buccal capsule 8 long and 17 wide; esophagus 2,993 long; muscular
portion 400 long; tail 340 long; left spicule 1,070 long, handle 320
long; right spicule 180 long. Spicular ratio 5.94. Area rugosa 16.02 mm
Paratypes (based on 8 specimens): Length 99
10.3 mm (81.9–
111.1); width 309
11 (303–333); nerve ring 233
from apex; buccal capsule 7.1
1.4 (5–9) long and 20
wide; esophagus 2,719
243 (2,242–2,999); long, muscular portion
59 (388–550); tail 368
34 (340–440) long; left spicule 1,154
80 (1,020–1,260) total length, handle 307
20 (270–340) long,
membranous alae 466
57 (400–500) long, and ﬂagellum 436
(370–480) long; right spicule 242
15 (210–260) long; spicular ratio
0.46 (4.2–5.7); gubernaculum 22
3.7 (20–30) long. Area
1.1 (9–12) mm long.
Juvenile male: Length 54.43 mm; nerve ring 150 from apex; buccal
capsule 5 long by 20 wide; esophagus 2,484 long; muscular portion 300
long; tail 350; left spicule 1,250 long, handle 300 long; membranous
alae and ﬂagellum 700 and 250, respectively; right spicule 270 long.
Spicular ratio 4.62. Area rugosa 8.84 mm long.
Female: Labial papillae, rectangular pattern 40 by 25; cephalic pa-
pillae, rectangular pattern 70 by 40; other female, 55 by 25 and 90 by
40; additional female 60 by 25 and 95 by 40, respectively (Figs. 14–
16). Vagina vera consisting of a simple straight tube surrounded by thin
walls and ending in a semicircular vulva (Figs. 13, 17, 18, 30). Lateral
chords conspicuous (Fig. 20). Simple caudal lappets with a broaden
base. Phasmid opening at the base of the lappets (Figs. 19, 31, 32).
Allotype: Length 237.3 mm; width 339; buccal capsule 10 long and
20 wide; nerve ring 250 from apex; esophagus 3,175 long; muscular
portion 350 long; tail 635 long. Vulva at level of esophagus 588 from
anterior end; vagina 269 long and 92 wide; ovijector 4,242 long. Caudal
lappets 10 long, situated 30 from posterior end.
Paratypes (based on 2 complete specimens, 3 anterior extremities,
and 2 posterior extremities): Length 239.6 and 254.2 mm; width 530
40 (496–575); buccal capsule 8.5
1.9 (6–10) long and 20.7
(20–22) wide; nerve ring 268
37 (226–300) from apex; esophagus
653 (3,569–4,787) long, muscular portion 687
750) long; tail 775
47 (710–810) long. Vulva 1,187
1,636) from anterior end.
Microﬁlariae: Body fusiform. Anterior extremity rounded with a ce-
phalic hook, short cephalic space. Tail attenuated, tip tail anucleated.
Large sheath. Measurements based on uterine microﬁlariae from 2 dif-
ferent females (n
4.2 (158–172) long; 5.53
6) wide. Length of sheath 206.46
19.7 (159–226) and 8.7
Type host: Chamek Spider Monkey Ateles chamek (Humboldt, 1812)
collected 28 August 1985.
Type locality: 14
W; 45 km north by road of Yacuma,
Site of infection: Abdominal cavity.
Specimens deposited: Holotype male HWML48375; allotype female
HWML48376, paratypes HWML48377 through HWML48380 (9 males
and 5 females).
Etymology: The species is named for Dr. Terry L. Yates, along with
Sydney Anderson, 1 of the primary leaders of our work on diversity of
mammals of Bolivia.
Dipetalonema yatesi n. sp. resembles Dipetalonema caudispina (Mol-
in, 1858) in having a vagina vera with a simple straight tube (Bain et
al., 1986) but differs in that females possess a vagina vera with thin
walls and the vulva opens more posterior (mean of 1,187 vs. 400–420
m). In males, the left spicule has a terminal ﬂagellum, and the po-
stcloacal area rugosa displays 2 subventral bands of small crests, instead
of 1 on the left side.
666 THE JOURNAL OF PARASITOLOGY, VOL. 93, NO. 3, JUNE 2007
Both species, D. yatesi n. sp. and D. gracile (Rudolphi, 1809) possess
2 subventral bands of postcloacal area rugosa and a similar shaped right
spicule; however, D. gracile display a biﬁd end of the right spicule, and
the membranous alae of the left spicule is longer than the ﬂagellum.
The new species also has a vagina vera with a simple tube, instead of
a sinuous one, and a longer microﬁlaria (range of 166–172 vs. 125–145
m) (Bain et al., 1986; J. Notarnicola, per. obs.).
Dipetalonema yatesi n. sp. differs from D. graciliformis Freitas, 1964,
in having a longer right band of the postcloacal area rugosa, a smaller
handle–lamina ratio of the left spicule (2.7 vs. 3.5), a simple vagina
vera, a longer tail (710–810 vs. 250–300
m), and a much longer mi-
croﬁlaria (166–172 vs. 93–115
m). In addition, the tails of the micro-
ﬁlariae are tapering and without obvious nuclei compared with those of
D. graciliformis, which are stout and have nuclei at the tips (Freitas,
1964; Bain et al, 1986).
The new species can be separated from D. freitasi Bain, Diagne and
Muller, 1987, by possessing a postcloacal area rugosa (not present in
D. freitasi) and the presence of a terminal ﬂagellum on the left spicule
(not present in D. freitasi). Moreover, D. yatesi n. sp. has females with
longer tails (mean of 635
m vs. 510
m) and much longer microﬁlaria
(166–172 vs. 100–107
m) (Bain et al., 1987).
Dipetalonema yatesi n. sp. resembles to D. robini Petit, Bain and
Roussilhon, 1985, in the shape and size of the spicules and the micro-
ﬁlaria, but the new species displays a distal extended membrane of the
right spicule; 2 ventral bands in the postcloacal area rugosa, compared
with1inD. robini; and a simple tube of the vagina vera instead of a
sinuous one. Phasmids of the new species have a simple opening at the
base of the lappets instead of presenting a biﬁd lappet with the opening
of the phasmid on a small posterior tubercle (Petit et al., 1985; Bain et
al., 1987). Scanning electron micrographs conﬁrm that the openings of
the phasmids are on the base of the lappets, and that lappets are a simple
tubercle with a broad base (see Figs. 31, 32).
Dipetalonema yatesi n. sp. can be separated from the other
Dipetalonema species by the combination of the following
characters: the presence of a simple tube of the vagina vera,
similar length of the membranous alae and the ﬂagellum on the
left spicule, a simple hook on the distal end of the right spicule,
2 postcloacal bands of the area rugosa, heterogeneous muscles
occupying the whole cavity, and microﬁlaria with a large sheath
and anucleated tip tail. However, some of these characters are
shared with other species of Dipetalonema, i.e., the ratio of the
left spicule with D. robini, the disposition of the postcloacal
area rugosa with D. gracile and D. graciliformis, and the simple
vagina vera with D. caudispina. Following the sequences of
character evolution stated by Bain et al. (1987), D. yatesi n. sp.
could be an intermediate form between D. freitasi and D. ro-
bini, when the shape of the left spicule and male musculature
characters are considered, or between D. caudispina and D.
freitasi, when the shape of the vagina vera is considered. A
ﬁnal statement on these points awaits a phylogenetic analysis
of the species in this genus.
The ﬁnding of 1 male, which is much shorter than the other
specimens in the same lot and with the same characters, sug-
gests this is a juvenile. This specimen shows no sign of molting,
as in the juveniles of other ﬁlarioid species (Guerrero et al.,
2002; Notarnicola, 2005).
The ﬁrst record of ﬁlarioid nematodes from monkeys in Bo-
livia was the report of D. gracile by Freitas (1964). The locality
was not recorded and remains unknown, but was probably
somewhere in southeastern part of the country because the ma-
terial was collected by the Comissa˜o de Estudos Epidemiolo´-
gicos soˆbre Leishmaniose Visceral Americana (CEELVA)
(Freitas, 1964). The other report, mentioned above, of D. grac-
ile was published by Karesh et al. (1998) for Ateles chamek
(syn. A. paniscus chamek; see Anderson, 1997) from primary
forest in the Parque Nacional Noel Kempff Mercado in the
eastern department of Santa Cruz. These specimens are avail-
able from the USNPC (USNPC86233).
The occurrence of D. gracile in several samples of Bolivian
spider monkeys suggests that this parasite is common. However,
more detailed work is conducted on the biodiversity of parasites
of Bolivia primates, data on prevalence and intensity of these
parasites in natural populations will be missing. Pathogenesis
of these nematodes in Ateles spp. is uncertain, but some nega-
tive inﬂuence was indicated in the report by Karesh et al. (1998)
in which, from an old individual male monkey, hundreds of
ﬁlarial worms were found in the abdominal cavity, with many
attached to the serosa of the intestines.
In Bolivia, as deforestation continues and crowding of the
monkeys increases in the remaining patches of primary lowland
forest, this nematode may play a signiﬁcant role in the health
and perhaps long-term viability of monkeys remaining. Al-
though the life cycle is unknown for D. yatesi at this time, the
vector is assumed to be some kind of an hematophagous dip-
teran, most likely a species of Ceratopogonidae (Eberhard et
al., 1979). Hyperinfections of these nematodes can probably be
expected to result from increased numerical density of hosts.
We encourage ecologists and forest and wildlife managers in
Bolivia to take special care to collect data on parasites of any
primate species available. The example of data taking on both
living and dead primates by Karesh et al. (1998) is a good one
to follow in this regard.
We thank the Coleccio´n Boliviana de Fauna of the Museo de Historia
Natural in La Paz for long term logistic support. We also thank Kit Lee
from the Scanning Electron Microscopy Laboratory–University of Ne-
braska for his help; Marı´a Cristina Estivarı´z from CEPAVE, for the
drawings; and Pat Pillit from USNPC, Beltsville, Maryland, for the
material loaned. This study was partially funded by a Beca para Estadı´as
Breves en el Extranjero, from Consejo Nacional de Investigaciones
Cientı´ﬁcas y Te´cnicas–CONICET–Argentina to J.N. and from the Har-
old W. Manter Laboratory–University of Nebraska–USA and by U.S.
National Science Foundation Grants (BSR8612329, BSR9024816,
DEB9496263, and DEB9631295 to S.L.G.).
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