ArticlePDF Available

A New Species of Dipetalonema (Filarioidea: Onchocercidae) from Ateles chamek from the Beni of Bolivia

Authors:

Abstract and Figures

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.
Content may be subject to copyright.
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
Juliana Notarnicola
F. Agustin Jimenez-Ruiz
Scott Lyell Gardner
Centro de Estudios Parasitolo´gicos y de Vectores, julinota@cepave.edu.ar
Southern Illinois University, Carbondale, fruiz@unlserve.unl.edu
University of Nebraska - Lincoln, slg@unl.edu
This paper is posted at DigitalCommons@University of Nebraska - Lincoln.
http://digitalcommons.unl.edu/parasitologyfacpubs/37
661
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.
e-mail: julinota@cepave.edu.ar
ABSTRACT
: 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
yellow fever.
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
2
, 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
(USNPC86233).
DESCRIPTION
Dipetalonema yatesi n. sp.
(Figs. 1–32)
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
F
IGURES
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
F
IGURES
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
F
IGURES
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
F
IGURES
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
long.
Paratypes (based on 8 specimens): Length 99
10.3 mm (81.9
111.1); width 309
11 (303–333); nerve ring 233
22 (200–250)
from apex; buccal capsule 7.1
1.4 (5–9) long and 20
0.5 (20–21)
wide; esophagus 2,719
243 (2,242–2,999); long, muscular portion
485
59 (388–550); tail 368
34 (340440) 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
58
(370480) long; right spicule 242
15 (210–260) long; spicular ratio
4.77
0.46 (4.2–5.7); gubernaculum 22
3.7 (20–30) long. Area
rugosa 10.5
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
0.95
(20–22) wide; nerve ring 268
37 (226–300) from apex; esophagus
4,314
653 (3,5694,787) long, muscular portion 687
86 (560
750) long; tail 775
47 (710–810) long. Vulva 1,187
362 (750
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
13): 166.2
4.2 (158–172) long; 5.53
0.35 (4.8–
6) wide. Length of sheath 206.46
19.7 (159–226) and 8.7
1.35
(6.1–10.6) wide.
Taxonomic summary
Type host: Chamek Spider Monkey Ateles chamek (Humboldt, 1812)
collected 28 August 1985.
Type locality: 14
42.5
S; 67
04
W; 45 km north by road of Yacuma,
Beni, Bolivia.
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.
Remarks
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. 400420
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).
DISCUSSION
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.
ACKNOWLEDGMENTS
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.).
LITERATURE CITED
A
LBINGER
, G., A. F
ONTES
J
R
., K. K
ERLE
,N.L
INK
,A.M
ACY
,
AND
S.
S
IMON
. 1995. SigmaScan Pro. Jandel Scientific Software, San Ra-
fael, California.
A
NDERSON
, S. 1997. Mammals of Bolivia: Taxonomy and distribution.
Bulletin of the American Museum of Natural History 231: 1–652.
B
AIN
, O., G. P
ETIT
,
AND
L. R
OSALES
-L
OESENER
. 1986. Filaires de Singes
sud-ame´ricains. Bulletin du Museum National de Histoire Naturelle,
Paris 4
a
serie 8, sectio´n A, 3: 513–542.
———, M. D
IAGNE
,
AND
R. M
ULLER
. 1987. Une cinquie`me filaire du
genre Dipetalonema , parasite de singes sud-ame´ricains. Annales de
Parasitologie Humaine et Comparee´ 62: 262–270.
C
ABALLERO
, E. 1947. Algunas filarias de mamı´feros y de reptiles de las
Repu´blicas de Colombia y Panama´. Anales del Instituto Biologico
de la Universidad Nacional de Me´xico 18: 169–188.
E
BERHARD
, M. L., R. C. L
OWRIE
J
R
.,
AND
T. C . O
RIHEL
. 1979. Devel-
opment of Dipetalonema gracile and D. caudispina to the infective
stage in Culicoides hollensis. Journal of Parasitology 65: 89–95.
E
ISENBERG
,J.F.,
AND
K. H. R
EDFORD
. 1999. Mammals of the Neotropics:
The central Neotropics. Ecuador, Peru, Bolivia, Brazil. Volume 3.
University of Chicago Press, Chicago, Illinois, 609 p.
F
REITAS
, J. F. T. 1943. Estudios sobre nematodeos filarideos Dipetalo-
NOTARNICOLA ET AL.—A NEW FILARIOID FROM BOLIVIA 667
nema caudispina (Molin, 1858). Memorias do Instituto Oswaldo
Cruz 38: 361–372.
——— 1964. Achegas Helminthologicas. Revista do Ciencias Biolo´-
gicas, Bele`m 3: 3–40.
G
ARDNER
, S. L. 1996. Essential techniques for collection of parasites
during surveys of mammals. In Measuring and monitoring biolog-
ical diversity—Standard methods for mammals, D. Wilson, R.
Cole, J. D. Nichols, P. Rudran, and M. Foster (eds.). Smithsonian
Institution Press, Washington, D.C., p. 291–298.
———,
AND
M. L. C
AMPBELL
. 1992. Parasites as probes for biodiver-
sity. Journal of Parasitology 78: 596–600.
G
UERRERO
, R., C. M
ARTIN
,S.L.G
ARDNER
,
AND
O. B
AIN
. 2002. New
and known species of Litomosoides (Nematoda: Filarioidea): Im-
portant adult and larval characters and taxonomic changes. Com-
parative Parasitology 69: 177–195.
H
UGOT
, J. P., S. L. G
ARDNER
,
AND
S. M
ORAND
. 1996. The Enterobiinae
subfam. nov. (Nematoda, Oxyurida) pinworm parasites of primates
and rodents. International Journal for Parasitology 26: 147–159.
K
ARESH
, W. B., R. B. W
ALLACE
,R.L.E.P
AINTER
,D.R
UMIZ
,W.E.
B
RASELTON
,E.S.D
IERENFELD
,
AND
H. P
UCHE
. 1998. Immobilization
and health assessment of free-ranging black spider monkeys (Ateles
paniscus chamek). American Journal of Primatology 44: 107–123.
N
OTARNICOLA
, J. 2005. Description of adults and fourth-stage larva of
Litomosoides navonae n. sp. (Nematoda: Onchocercidae), a parasite
of five species of sigmodontine rodents from northeastern Argen-
tina. Systematic Parasitology 62: 171–183.
P
ETIT
, G., O. B
AIN
,
AND
C. R
OUSSILHON
. 1985. Deux nouvelles Filaires
chez un Singe Saimiri sciureus au Guyana. Annales de Parasito-
logie Humaine et Comparee´ 60: 65–81.
P
HILLIPS
, K. A., M. E. H
AAS
,B.W.G
RAFTON
,
AND
M. Y
RIVARREN
. 2004.
Survey of the gastrointestinal parasites of the primate community
at Tambopata National Reserve, Peru. Journal of Zoology 264:
149–151.
S
OKAL
, R. R.,
AND
F. J. R
OHLF
. 1995. Biometry: The principles and
practice of statistics in biological research, 3rd ed. W. H. Freeman,
New York, New York, 887 p.
T
HOISY
,B.
DE
,J.C.M
ICHEL
,I.V
OGEL
,
AND
J. C. V
IE
´
. 2000. A survey
of hemoparasite infections in free-ranging mammals and reptiles in
French Guiana. Journal of Parasitology 86: 1035–1040.
... The genus Dipetalonema (DIESING, 1861) belongs to the family Onchocercidae, and it has had other names including Filaria (RUDOLPHI, 1809;MOLIN, 1858) and Acanthocheilonema (BOULENGER, 1920). Rodents, pinnipeds and non-human primates have previously been considered to be hosts (ELEY, 1981;NOTARNICOLA et al., 2007), but phylogenetic studies conducted by Lefoulon et al. (2015) restricted Dipetalonema to non-human primate hosts in the Neotropics. ...
... However, the geographical distribution of Dipetalonema throughout the Neotropics is imprecise because most records are from captive primates or only one host, such as D. freitasi in a necropsy of Cebus capucinus at the London Zoo (BAIN et al., 1987), D. robini in Saimiri sciureus in Guyana (PETIT et al., 1985), D. graciliformis in Saguinus midas in French Guiana (BAIN et al., 1986), and D. yatesi in Ateles chamek in the Beni region of Bolivia (NOTARNICOLA et al., 2007). In the case of D. caudispina and D. gracile, most records in the last century have been concentrated in Brazil and Guiana (FREITAS, 1943;NOTARNICOLA et al., 2008) and cover a larger number of non-human primate hosts (WEBBER, 1955;NOTARNICOLA et al., 2008). ...
... These characteristics are shown in detail for the first time by scanning electron microscopy, which also shows the lateral thickening along the body in both sexes of the nematode. The uterine microfilariae Bain et al. (1986) and Notarnicola et al. (2007). Notarnicola et al. (2008) and Bain et al. (1986). ...
Article
Full-text available
Dipetalonema gracile (Rudolphi, 1809) (Filarioidea: Onchocercidae) is one of six species of cavities filarial parasites of Neotropical non-human primates. The present study recorded the occurrence of D. gracile, provides morphological and morphometric data and extends the geographical distribution. Adult filariae were obtained from the thoracic and abdominal cavities of 38 specimens of woolly monkey, which were used for local human consumption, in the northeastern Peruvian Amazon. Male and female filarids were processed and analysed using light and scanning electron microscopy. Details of the cephalic papillae, post-cloacal bands and papillae, vulva, phasmid position and lateral appendages are showed by scanning electron microscopy and is recorded the occurrencce of Lagothrix poeppigii monkey as a new host of this filaria in the Yavari-Mirin river basin, Peruvian Amazon.
... Cavitary Dipetalonema infections can cause mild inflammatory reactions, including peritonitis and pleuritis with fibrinous adhesions (Strait et al., 2012). To date, biting midges of the genus Culicoides (Arthropoda: Ceratopogonidae) are the only biologically confirmed intermediate hosts and biological vectors of Dipetalonema (Eberhard et al., 1979;Travi et al., 1985;Notarnicola et al., 2007). There are six species in the genus Dipetalonema which parasitize Neotropical primates: D. gracile (Rudolphi, 1809); D. caudispina (Molin, 1858); D. graciliformis Freitas (1964); D. robini Petit, Bain, and Roussilhon, 1985;D. ...
... There are six species in the genus Dipetalonema which parasitize Neotropical primates: D. gracile (Rudolphi, 1809); D. caudispina (Molin, 1858); D. graciliformis Freitas (1964); D. robini Petit, Bain, and Roussilhon, 1985;D. freitasi Bain et al. (1987); and D. yatesi Notarnicola et al. (2007) (Vanderhoeven et al., 2017). These nematodes have been isolated from over 20 species of monkeys from nine different genera of Neotropical primates of the tribe Platyrrhini. ...
... However, the true geographic distribution of many of these species is unknown since most reports of Dipetalonema infection in Neotropical primates come from animals in captivity (Conga et al., 2018). Only two Dipetalonema species have been reported in the black-faced spider monkey A. chamek: D. gracile, found in the Noel Kempff Mercado National Park, Bolivia (Karesh et al., 1998), and D. yatesi, a newly described species first isolated in north-eastern Bolivia (Notarnicola et al., 2007). The description of this latter species was solely based in morphological characteristics (i.e., structure and dimensions of the spicules and gubernaculum in males; morphology of the vulva and posterior end in females) (Notarnicola et al., 2007). ...
Article
Full-text available
Species of the genus Dipetalonema are parasitic nematodes of the family Onchocercidae (Nematoda; Filarioidea) which infect the peritoneal cavity of Neotropical primates. Of these, six species have been taxonomically described, two of these have been reported infecting the black-faced spider monkey (Ateles chamek): Dipetalonema gracile and Dipetalonema yatesi. Description of Dipetalonema species have been based on morphological characteristics, and their phylogenetic relationships remain unresolved. A few molecular studies have been carried out in Dipetalonema spp. infecting Neotropical primates. Seven filarioid nematodes (6 females and one male) recovered from one A. chamek in the Peruvian Amazon rainforest were morphologically identified as D. yatesi and molecularly characterized. A multi-locus genetic analysis of nuclear ribosomal region (18S) and mitochondrial (cox1, 12S, and nad5) gene sequences supported D. yatesi as a distinct lineage and yielded a highly resolved phylogenetic lineage tree for this filarioid genus of Neotropical primates. Our results highlighted that Dipetalonema species are divided in two well-supported clades, one containing D. yatesi and D. caudispina, and the second containing D. robini, D. gracile, and D. graciliformis. Due to sequence ambiguities from GenBank entries, relationships among isolates of D. gracile and D. graciliformis cannot be fully resolved, which requires further investigation. However, this suggests that these could represent a species complex. Our study confirms that D. yatesi is a valid species and constitutes the first molecular phylogenetic analysis of this parasite in black-faced spider monkeys.
... Overall, the genus Dipetalonema includes: D. caudispina (Molin, 1858), Dipetalonema freitasi Bain, Diagne andMuller, 1987, D. gracile (Rudolphi, 1809), Dipetalonema graciliformis Freitas, 1964, Dipetalonema yatesi Notarnicola, Jimenez andGardner, 2007 and Dipetalonema robini Petit, Bain and Roussilhon, 1985 (Table S1). Adhering to the concept of morphological species, the six species above are mainly distinguished by the complex structures of the vagina vera, caudal lappets in females as well as the spicules, the area rugosa of the tail and arrangement of the musculature in males and the shape of microfilariae (Petit et al., 1985;Bain et al., 1987). ...
Article
Six Dipetalonema species have been reported from neotropic monkeys, Dipetalonema gracile, Dipetalonema graciliformis and Dipetalonema caudispina being the dominant species found in French Guiana primates. Adult filaroids isolated from the abdominal cavity of tamarins (Saguinus midas) in French Guiana were morphologically and molecularly identified as D. graciliformis. Phylogenetic analysis based on DNA and amino acid sequences of the cox1 gene as well as the concatenated sequences of the cox1 and the 18S genes indicated that D. graciliformis belongs to the clade 4 (ONC4) of Onchocercidae. Blast analysis of the 18S rDNA revealed that D. graciliformis in studied tamarins is conspecific with the filaroid circulating in howler monkeys (Alouatta macconnelli) in French Guiana, previously referred to as unidentified Onchocercidae species.
Chapter
Trypanosomes and filarial nematodes are important pathogens in humans and domestic animals. However, the majority of the infections reported from nonhuman primates (NHPs) are nonpathogenic. Moreover, those hemoparasites are relatively host-specific, which means that transmission from NHPs to humans is highly unlikely with the exception of nonpathogenic Trypanosoma rangeli and Trypanosoma cruzi and the T. brucei complex, which cause Chagas disease and sleeping sickness in humans, respectively. NHPs may also act as reservoir hosts for some nonpathogenic human filarial parasites, e.g., Mansonella streptocerca. Though many studies on those hemoparasites were conducted in the last century, recent studies remain rather neglected due to the logistical, ethical, and administrative challenges associated with the collection of blood or tissue samples in wild NHPs. In this chapter, we present an overview of trypanosomes and filarial nematodes infecting NHPs with information about their distribution, biology, pathogenesis, and their zoonotic potential.
Article
Full-text available
Sydney Anderson and the "Mammalian Diversity in Bolivia" (MDB) project (1984-1993) established a highly productive model for integrated specimen-based field expeditions. We assess the extended impact of that decade-long series of holistic surveys of mammalian diversity as a productive model for building enduring and highly integrated infrastructure for biodiversity research. We point to specific examples of impact, but more generally make a case for Sydney Anderson’s prescient view that collections, over time, become ever more powerful and essential scientific tools for understanding mammalian diversity and our rapidly changing planet. To assess the number of specimens held in collections and their availability for spatial analyses, we queried the Global Biodiversity Information Facility (GBIF) for Bolivian specimens. Results were downloaded and non-georeferenced specimens were georeferenced in GeoLocate. Publications utilizing specimens or data from the MDB project were identified in Google Scholar, these were used to build a citation profile to analyze impact and breadth of research. Over the course of the decade-long MDB project ca. 10,000 new “holistic” specimens were added to natural history collections in Bolivia and the United States. These specimens and data were used in over 500 papers across a broad range of research areas, including new records for the country, and many descriptions of mammals (nine) and parasites (34) new to science. The Google Scholar profile generated for these publications has more than 20,000 citations and a citation H-index = 68 and an i-10 = 340. Sydney Anderson’s legacy will endure through the exceptional collections he helped to build and the wide array of students he helped to inspire. As societal concerns related to environmental change (e. g., biological annihilation, climate change, emerging zoonotic pathogens) become more pressing, scientific questions evolve, and technology continues to develop, these critical resources will be called upon more and more frequently. Thus we can confidently predict that the value and use of the Bolivian mammal specimens archived under Syd Anderson’s leadership will continue to increase in the future.
Article
Full-text available
Previous studies have reported filarial parasites of the genus Dipetalonema and Mansonella from French Guiana monkeys, based on morphological taxonomy. In this study, we screened blood samples from nine howler monkeys (Alouatta macconnelli) for the presence of filaria and Wolbachia DNA. The infection rates were 88.9% for filaria and 55.6% for wolbachiae. The molecular characterization, based on the 18S gene of filariids, revealed that A. macconnelli are infected with at least three species (Mansonella sp., Brugia sp. and an unidentified Onchocercidae species.). Since the 18S and cox1 generic primers are not very effective at resolving co-infections, we developed ITS genus-specific PCRs for Mansonella and Brugia genus. The results revealed coinfections in 75% of positives. The presence of Mansonella sp. and Brugia sp. was also confirmed by the 16S phylogenetic analysis of their associated Wolbachia. Mansonella sp., which close to the species from the subgenus Tetrapetalonema encountered in New World Monkeys, while Brugia sp. was identical to the strain circulating in French Guiana dogs. We propose a novel ITS1 Brugia genus-specific qPCR. We applied it to screen for Brugia infection in howler monkeys and 66.7% were found to be positive. Our finding highlights the need for further studies to clarify the species diversity of neotropics monkeys by combining molecular and morphological features. The novel Brugia genus-specific qPCR assays could be an effective tool for the surveillance and characterization of this potential zoonosis.
Article
Dipetalonema gracile is a common parasite in squirrel monkeys ( Saimiri sciureus ), which can cause malnutrition and progressive wasting of the host, and lead to death in the case of massive infection. This study aimed to identify a suspected D. gracile worm from a dead squirrel monkey by means of molecular biology, and to amplify its complete mitochondrial genome by polymerase chain reaction (PCR) and sequence analysis. The results identified the worm as D. gracile , and the full length of its complete mitochondrial genome was 13,584 bp, which contained 22 tRNA genes, 12 protein-coding genes, two rRNA genes, one AT-rich region and one small non-coding region. The nucleotide composition included A (16.89%), G (20.19%), T (56.22%) and C (6.70%), among which A + T = 73.11%. The 12 protein-coding genes used TTG and ATT as start codons, and TAG and TAA as stop codons. Among the 22 tRNA genes, only trn S1 AGN and trn S2 UCN exhibited the TΨC-loop structure, while the other 20 tRNAs showed the TV-loop structure. The rrn L (986 bp) and rrn S (685 bp) genes were single-stranded and conserved in secondary structure. This study has enriched the mitochondrial gene database of Dipetalonema and laid a scientific basis for further study on classification, and genetic and evolutionary relationships of Dipetalonema nematodes.
Article
Full-text available
Species of the genus Dipetalonema are filarial parasites of Neotropical monkeys. Herein, we report the first record of Dipetalonema robini from Argentina and from the black horned capuchin monkey, Sapajus nigritus, providing additionally information on its morphology. Nematodes were found in the abdominal cavity of a male capuchin monkey found in the Parque Nacional Iguazú, Misiones, Argentina. Among Dipetalonema species, the proportion of the different parts of the left spicule (handle and lamina; membranous alae and filament) is a character of taxonomic relevance. The membranous ala is longer than the filament in the single male parasite examined, differing from published data. The differences observed could be due to the small number of specimens measured. RESUMEN. Primer registro de Dipetalonema robini Petit, Bain & Roussilhon 1985 (Nematoda: Oncho-cercidae) parásito de Sapajus nigritus en el noreste de Argentina. Las filarias del género Dipetalonema son parásitos de monos neotropicales. En este trabajo, reportamos el primer registro de Dipetalonema robini para la Argentina y para el mono caí, Sapajus nigritus, además de proveer nuevos datos de la morfología de la es-pecie. Tres filarias fueron encontradas en la cavidad abdominal de un mono caí macho hallado en el Parque Nacional Iguazú, Misiones, Argentina. Un carácter taxonómico relevante entre las especies de Dipetalonema es la proporción de las diferentes partes de la espícula izquierda (mango y lámina; alas membranosas y filamento). En el macho hallado, la sección de alas membranosas es más larga que el filamento, difiriendo con los datos publicados. Esta diferencia puede deberse al pequeño número de ejemplares medidos.
Article
Full-text available
Pseudopecoelus mccauleyi n. sp. (Opecoelidae: Opecoelinae) is described from the intestine of the bigfin eelpout, Lycodes cortezianus (Gilbert, 1890) (Perciformes: Zoarcidae), collected at 200–800 m depths in the Northeastern Pacific Ocean off Oregon and Vancou-ver Island, British Columbia. The new species is distinguished by possessing a unique combination of the following diagnostic characters: vitelline fields that extend to the posterior margin of the ventral sucker; a slender, tubular and sinuous seminal vesicle that extends some distance into the hindbody; an unspecialized, protuberant ventral sucker; a genital pore at pharynx level; lobed to deeply multi-lobed testes; a lobed ovary; and an egg size of 68–80 μm × 30–46 μm. A single specimen of Podocotyle Dujardin, 1845 (Digenea: Plagioporinae) is also described from the intestine of an individual Coryphaenoides sp. (Gadiformes: Macrouridae) collected at 2,800 m depth off Oregon. A listing of parasites from the bigfin eelpout as well as observations of parasite diversity within relevant hosts are offered, new host and locality records are noted, and a brief discussion of Pseudopecoelus von Wicklen, 1946 in the deep sea is presented taking note of the low level of host specificity recorded (i.e. spp. of Pseudopecoelus are now known to parasitize deep-water fish from at least 20 piscine families). A new dichotomous key to the 39 recognized species of Pseudopecoelus is introduced.
Article
Full-text available
During field surveys in Venezuela, Peru, and French Guiana, species of Litomosoides were recovered from bats and from a didelphid marsupial. Their morphology was studied, giving particular attention to the head and caudal papillae, the spicules (used to distinguish the carinii and sigmodontis groups of Litomosoides), and the microfilariae. Litomosoides wilsoni sp. n. from the short-tailed opossum Monodelphis emiliae is described from Peru; Litomosoides brasiliensis, Litomosoides chandleri, and Litomosoides guiterasi from bats are redescribed, and new hosts are recorded. For the first time, larval stages were recovered from bats (1 male and 1 female fourth-stage larvae of Litomos. brasiliensis). Litomosoides solarii sp. n. from the fringe-lipped bat Trachops cirrhosus (Phyllostomidae) in Peru is distinguished from the other species by its peculiar microfilaria (the male is unknown). Filaria serpicula from Phyllostomus sp. in Brazil is renamed Litomosoides serpicula (Molin, 1858) comb. n. This study confirms the close morphological resemblance between the species of Litomosoides from flying and terrestrial mammals and reinforces the hypothesis of host-switching in the evolution of this genus. The 2 North American species of Litomosoides from the Geomyidae were reexamined and are peculiar in several adult and microfilarial characters that resemble those of Litomosa, parasitic in Old World bats. The following new combinations are proposed: Litomosa westi (Gardner and Schmidt, 1986) comb. n. and Litomosa thomomydis (Gardner and Schmidt, 1986) comb. n. However, Litomosa and Litomosoides have in common a thick buccal capsule embedded posteriorly in the esophagus, which suggests that they are closely related. Litomosoides andersoni, a parasite of a caviomorph rodent, likely results from conflation of a species of Litomosoides and one of Ackertia.
Article
Full-text available
Eight free-ranging black spider monkeys (Ateles paniscus chamek) were immobilized with Telazol® in Bolivia for the purpose of radio-collaring. During this procedure, the animals received complete medical examinations, and samples were collected for health analyses. Biochemical test results varied with the degree of condition of the animals, and a variety of physical abnormalities were found. Evidence of previous infections with Leptospira sp., encephalitis virus, and yellow fever virus was found. All findings contribute to establishing baseline health values for the species. The handling of primates for research projects provides a valuable opportunity to collect health-related data and samples that can contribute to wildlife management and conservation efforts. The capture and handling of free-ranging primates is always accompanied by risk of injury or mortality. It is ethically important to maximize the amount of information gathered during these procedures. Furthermore, sharing the undesirable impacts with the scientific community enables informed decisions to be made during future project development. Am. J. Primatol. 44:107–123, 1998. © 1998 Wiley-Liss, Inc.
Article
Full-text available
Cestodes of the genus Linstowia, parasitic in marsupials, show patterns of coevolution and ancient historical-ecological connections. Correlated with the breakup of the austral landmasses (Gondwanaland) of the Neotropical and Australian regions from the Antarctic continent, the age of this host-parasite community is estimated to be between 60 and 70 million years old. Based on the data from the survey of parasites of mammals from throughout Bolivia and from the phylogenetic analysis of the cestodes, we urge the planners of biodiversity preserves in the neotropics to consider the Yungas of Bolivia as a region that supports an ancient ecological community worthy of consideration as a biopreserve.
Article
Description of two new Filariae, parasites of Saimiri sciureus L. (Georgetwon type, karyotype 14/7) from Guyana. Dipetalonema robini n. sp., fourth species of the genus, is frequent and associated with the morphologically similar species, D. gracile (Rud., 1809) ; D. robini differs from D. gracile by structure of caudal lappets of female, vagina, microfilaria and area rugosa. The second filaria, also frequent, belongs to the subgenus Tetrapetalonema which contains a dozen species ; Mansonella (T.) mariae n. sp. is similar to M. (T.) marmosetae Faust, 1935 and M. (T.) tamarinae Dunn & Lambrecht, 1963 but is distinguished by the position of the head papillae, the cuticular ornamentation of the body and the microfilaria.
Article
The main objective of this project was to provide baseline data on faecal parasites of groups of non-human primates from Tambopata Research Center, Tambopata National Reserve, Peru. All primate species found in this area were sampled: red howler monkeys Alouatta seniculus, night monkeys Aotus vociferans, spider monkeys Ateles bezlebuth chamek, brown titi monkeys Callicebus brunneus, white-fronted capuchins Cebus albifrons, brown capuchins Cebus apella, saddleback tamarins Saguinus fuscicollis and squirrel monkeys Saimiri sciureus. Individuals from four howler monkey troops, three brown titi monkey troops, two squirrel monkey troops and one troop each of night monkeys, spider monkeys, brown capuchins, white-fronted capuchins and saddleback tamarins were sampled. Faecal samples were collected from July to October 2002 from 86 individuals. A concentration test was used to analyse faecal samples. Results indicate the presence of various protozoans, Ancyclostoma sp., Ascaris sp., Strongyloides stercoralis, Trichuris trichiura, Prosthenorchis elegans and Schistosoma mansoni.
Article
The microfilariae of 2 species of Dipetalonema (i.e., D. gracile and D. caudispina), common parasites of South American monkeys, develop to the third (infective) stage in the biting midge, Culicoides hollensis. Development of both species occurs in the abdominal fat body; D. gracile requires 13 days and D. caudispina 9 days. Despite similarities in the patterns of development of both species, the third-stage larvae of each is morphologically distinct.
Article
Description of D. freitasi n. sp., a parasite of Cebus capucinus: this species, close to D. caudispina, is distinguished by the slightly more complex structure of the vagina and right spicule, the lack of area rugosa on the tail and by the shorter microfilaria. Additional morphological data on the male of D. robini Petit et al., 1985 are given. A comparative table of 4 principal evolutive characters of the genus Dipetalonema (vagina, left and right spicules, epithelio-muscular body wall) is given. D. caudispina and D. freitasi n. sp. represent a small primitive group opposed to the more evolved one made up of D. robini, D. gracile and D. graciliformis.
Article
Description of two new Filariae, parasites of Saimiri sciureus L. (Georgetown type, karyotype 14/7) from Guyana. Dipetalonema robini n. sp., fourth species of the genus, is frequent and associated with the morphologically similar species, D. gracile (Rud., 1809); D. robini differs from D. gracile by structure of caudal lappets of female, vagina, microfilaria and area rugosa. The second filaria, also frequent, belongs to the subgenus Tetrapetalonema which contains a dozen species; Mansonella (T.) mariae n. sp. is similar to M. (T.) marmosetae Faust, 1935 and M. (T.) tamarinae Dunn & Lambrecht, 1963 but is distinguished by the position of the head papillae, the cuticular ornamentation of the body and the microfilaria.