Lemuricola (Madoxyuris) bauchoti Chabaud, Brygoo et Petter, 1965 is redescribed from material collected from the ring-tailed lemur, Lemur catta, from the Beza Mahafaly Special Reserve in Madagascar using the scanning electron microscope. This is a new host record and the first oxyurid reported from the ring-tailed lemur. Previously, records of each species of the subgenus Madoxyuris have been restricted to a single host species, but the close relationship between these nematodes and their Strepsirrhini hosts will only be proven when additional records fill in the gaps in their distribution.Centro de Estudios Parasitológicos y de Vectore

Cuozzo, Frank R

Hunter-Ishikawa, Mandala

Kinsella, John M.

Loudon, James E.

Miller, David S.

Robles, María del Rosario

Sauther, Michelle L.

Acta Parasitologica

English

SEDICI - Repositorio de la UNLP

VERSITA
DO 1:10.2478/sl 1686-010-0040-4
© W. Stefanski Institute oí Parasitology, PAS
Acta Parasitológica, 2010, 55(3), 270-275; ISSN 1230-2821
Redescription of Lemuricola (Madoxyuris) bauchoti 
(Nematoda, Oxyuridae) from Lemur catta in Madagascar
María del Rosario Robles1*, James E. Loudon2, John M. Kinsella3, Mandala Hunter-Ishikawa4, 
David S. Miller4, Michelle L. Sauther2 and Frank R Cuozzo5
‘Centro de Estudios Parasitológicos y de Vectores CEPAVE (CCT-CONICET-La Plata) (UNLP), Calle 2 # 584 La Plata (1900),
Buenos Aires, Argentina; ‘Department of Anthropology, University of Colorado, Boulder, CO 80309, USA; ‘HelmWest Laboratory, 
2108 Hilda Avenue, Missoula, MT 59801, USA; 4College of Veterinary Medicine and Biomedical Sciences, Colorado State University, 
Fort Collins, CO 80524, USA; 5Department of Anthropology, University of North Dakota, Grand Forks, ND 58202, USA
Abstract
Lemuricola (Madoxyuris) bauchoti Chabaud, Brygoo et Petter, 1965 is redescribed from material collected from the ring-tailed 
lemur. Lemur catta, from the Beza Mahafaly Special Reserve in Madagascar using the scanning electron microscope. This is 
a new host record and the first oxyurid reported from the ring-tailed lemur. Previously, records of each species of the subgenus 
Madoxyuris have been restricted to a single host species, but the close relationship between these nematodes and their Strep- 
sirrhini hosts will only be proven when additional records fill in the gaps in their distribution.
Keywords
Lemuricola (Madoxyuris) bauchoti, Oxyuridae, ring-tailed lemur. Lemur catta, Hapalemur, Madagascar, SEM
Introduction
Species of Oxyuridae (Nematoda) can be found in most fam­
ilies and genera of the order Primates. The subfamily Entero- 
biinae was erected for oxyurids from primates (Hugot et al. 
1996), and the monophyly of this subfamily was later con­
firmed by cladistic analysis (Hugot 1999). Primates of the sub­
order Strepsirrhini are parasitized by species of the genus 
Lemuricola Chabaud et Petter, 1959 (Enterobiinae).
Several authors have studied the possible co evolutionary re­
lationships among groups of primates and their oxyurid para­
sites (e.g. Cameron 1929, Sandosham 1950, Inglis 1961, Brooks 
and Glen 1982, Hugot 1999). Among these, Hugot (1999) pro­
vides evidence supporting the existence of coevolution with 
cospeciation between hosts in Strepsirrhini and species of 
Lemuricola. Several occurrences of parasites specific to partic­
ular hosts were observed, and for this reason it is probable that 
the speciation of the parasites parallels very closely the specia­
tion of the hosts (Hugot 1999). However, these studies are based 
on relatively few host species. To date, Lemuricola spp. have 
been recorded from only 10 of 88 host species of Strepsirrhini 
belonging to 7 of 23 genera and 4 of 7 families.
On the basis of cephalic and caudal papillae as well as 
characteristics of the lips, oesophagus and tip of the tail of 
males, three subgenera of Lemuricola have been defined 
(Chabaud and Petter 1959, Inglis 1961, Chabaud et al. 1965). 
To date, 9 species have been described: L. nycticebi (Baylis, 
1928) and L. malayensis Inglis et Dunn, 1963 belong to the 
subgenus Protenterobius Inglis, 1961; L. contagiosus Chabaud 
et Petter, 1959 and L. microcebi Hugot, Morand et Gardner, 
1995 belong to the subgenus Lemuricola Chabaud et Petter, 
1965; and lemuris (Baer, 1935), L. vauceli Chabaud, Bry­
goo et Petter, 1965, L. baltazardi Chabaud, Brygoo et Petter, 
1965, L. bauchoti Chabaud, Brygoo et Petter, 1965 and 
L. daubentoniae Petter, Chabaud, Delavenay et Brygoo, 1972 
belong to the subgenus Madoxyuris Chabaud, Brygoo et Pet­
ter, 1965. Based on cladistic studies, Hugot and Baylac (2007) 
question the placement of L. daubentoniae in the subgenus 
Madoxyuris, suggesting that it is more closely related to the 
subgenus Lemuricola.
The males of each genus and subgenus of Enterobiinae 
have been observed to share a particular pattern of distribu­
tion of preanal and postanal papillae (Hugot and Baylac 2007). 
These caudal papillae as well as other features of the tail are 
very difficult to observe with light microscopy. Only two stud­
ies on Enterobiinae have studied these features with scanning 
electron microscopy (SEM) (Tenora et al. 1981, Baros et al. 
2007).
Lemuricola (Madoxyuris) bauchoti Chabaud, Brygoo et 
Petter, 1965 was described on the basis of specimens recov-
*Corresponding author: rosario@cepave.edu.ar
Unauthenticated
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Redescription of Lemuricola (M) bauchoti from L. catta in Madagascar 271
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Til Maria del Rosario Robles et al.
ered fcoraHapalemur spp. In this previous work, some charac­
teristics were not mentioned, the drawings of the posterior end 
were not very clear and a correct differentiation from other 
species was not provided.
No species of Enterobiinae have been previously recorded 
from the ring-tailed lemur, Lemur catta Linneaus, 1758. The 
aim of this paper is to redescribe Lemuricola (Madoxyuris) 
bauchoti on the basis of new specimens recovered from this 
host from southwest Madagascar.
Materials and methods
The nematodes studied here were collected on 17 December 
2005 from the feces of a ring-tailed lemur, Lemur catta, from 
the Beza Mahafaly Special Reserve in Madagascar (23°30'S, 
44°40'E). The feces were collected immediately after observ­
ing the individual defecating during the morning hours (07-10 
a.m.) and preserved in polyvinyl alcohol. Nematodes were 
studied in temporary mounts of lactophenol. Drawings were
Figs 1-7. Lemuricola (Madoxyuris) bauchoti: 1 - male, complete specimen; 2 - ventral view of posterior extremity, detail of caudal papillae, 
spicule and area rugosa; 3 - posterior extremity, lateral view; 4 -detail of spicule; 5 - female, complete specimen; 6 - detail of vulva; 7 - egg
Unauthenticated
Download Date | 8/26/19 8:03 PM
Redescription ofLemuricola (M.) bauchoti from L. catta in Madagascar 273
made with the aid of a drawing tube. Some specimens were 
dried using the critical point method, examined under SEM 
(Jeol 6360 LV), and photographed.
All measurements are in micrometers unless otherwise 
stated (Table I).
The type specimen of Lemuricola (Madoxyuris) bauchoti 
from Hapalemur spp. was studied (1 female allotype, MNHN 
634 F Muséum National d’Histoire Naturelle, Paris, France - 
this is the only type material existent of this species).
Figs 8-17. SEM micrographs of Lemuricola (Madoxyuris) bauchoti: 8 - female, buccal aperture surrounded by lips, four cephalic papillae 
and amphids, apical view; 9 - female, lateral view of anterior extremity, detail of cephalic papillae and amphids; 10 - male, lateral view of 
anterior extremity, detail of lateral alae; 11 - male, complete specimen; 12 - female, lateral view of anterior extremity, detail of lateral alae; 
13 - female, complete specimen, detail of lateral alae; 14 - male, detail of area rugosa; 15 - male, ventral view of posterior extremity and 
area rugosa; 16 - male, 2 pairs of pedunculate papillae, 2 pairs of sessile papillae, and 1 pair of amphids; 17 - male, detail of sessile papillae 
and amphids
Unauthenticated 
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Z1A Maria del Rosario Robles et al.
Redescription
Lenturicola (Madoxyuris) bauchoti Chabaud, Brygoo et 
Petter, 1965 (Figs 1-17, Table I)
General: Buccal aperture surrounded by three lips. Lips de­
fined, with cuticular edges around triangular opening (Figs 8 
and 9). Four cephalic papillae visible and ventral papillae very 
close to the amphids (Figs 8 and 9). Lateral alae symmetrical 
and with sexual dimorphism. In males, the alae are single ex­
pansions (one crest) of the cuticle and extend from approxi­
mately 350-420 mm from the posterior end to approximately 
3/4 of the body length (Figs 10 and 11); in females, the alae are 
double expansions (two crests) reaching the end of the body 
(Figs 12 and 13).
Male: Body length 1.2-2.1 mm. Body width 80-210. Total 
oesophagus 280-310 long, oesophageal bulb 50-80 long. 
Nerve-ring 70-120, and excretory pore 350-550 from ante­
rior end (Fig. 1). Spicule 50-70 long (Figs 2-4). Tail spike ab­
sent (Figs 2 and 3).
Area rugosa present as a large round inflated cuticle pos­
terior to the excretory pore, in the region between the second 
and third portion of body (Figs 1-3; 14 and 15).
Four pairs of caudal papillae: 1 preanal pedunculate pair, 
2 postanal sessile pairs, and 1 large postanal pedunculate pair 
supporting the bursa (Figs 2 and 3, 15 and 16). The 2 sessile 
pairs are very close to each other and form a square cuticular- 
ized sheet connected with a small pitchfork ornamentation that 
longitudinally flanks the posterior edge of the cloaca (Figs 16 
and 17). The phasmids are lateral to the first papillae and lie 
between the two pedunculate papillae (Fig. 17).
Female: Body length 2.14-3.47 mm. Body width 150-280. 
Total oesophagus 320—480 long, oesophageal bulb 70-90 long 
(Fig. 5). Nerve-ring 80-170, excretory pore 350-620, and 
vulva 550-1300 from anterior end (Figs 5 and 6). Tail rela­
tively long, 550-890. Eggs elliptical and with large opercu­
lum, 45-60 x 20-30 (Fig. 7).
Type host: Hapalemur spp.
New host: Lemur catta Linnaeus, 1758 (Lemuridae). 
Type locality: Ambavaniasy, east-central Madagascar. 
New locality: Beza Mahafaly Special Reserve in Mada­
gascar (23°30'S, 44°40'E).
Site of infection: Presumptively caecum. Found in feces.
Specimens deposited: Helminthological Collection of the 
Museo de La Plata CHMLP, no. is MLP 6146.
Remarks: The general morphology and measurements of 
the specimens of L. (AL.) bauchoti from L. catta examined in 
the present study agree with specimens from Hapalemur 
spp. described by Chabaud et al. (1965) and the observations 
made here on the allotype specimen with a few exceptions. 
The minor discrepancies include small differences in the 
measurements of the excretory pore in both sexes and the total 
length of the oesophagus in the females (Table I).
The principal character which places these specimens in 
the subgenus Madoxyuris is the absence of a tail spike in the 
males. They can be differentiated from the other 4 species in 
the subgenus by their shorter oesophageal and spicule lengths. 
In addition, the males differ from L. (M.) daubentoniae, 
L. (M.) vauceli, and L. (M.) baltazardi by lacking caudal alae 
and by a more anterior excretory pore. The shorter distance 
from the vulva to the anterior end distinguishes the females 
from L. (M.) lemuris, L. (AL.) vauceli, and L. (AL.) baltazardi. 
Although the males are somewhat longer than the original de­
scription and there are other minor differences in measure­
ments, we believe they most closely fit L. (M.) bauchoti.
Discussion
This is the first record of Lemuricola (Madoxyuris) bauchoti 
from Lemur catta and the first record of any oxyurid from this 
host. Structures such as the cephalic papillae, details and dis­
tribution of the caudal papillae and amphids, fine points of the 
cervical alae, and the area rugosa, poorly visualized under 
light microscopy, were observed here with the SEM for the 
first time.
Using light microscopy, Chabaud et al. (1965) described 
3 pairs of pedunculate papillae, 2 pairs of sessile papillae, and 
1 pair of amphids in L. (AL.) bauchoti as well as L. (AL.) 
vauceli and L. (M.) baltazardi. Only 2 pairs of pedunculate 
and 2 pairs of sessile papillae were observed here using SEM. 
There is no small pair of pedunculate papillae lateral to the 
anus as described by Chabaud et al., although there is a small 
ridge in this area (Fig. 15). Since the number of observed 
papillae in the Enterobiinae is constant, this feature should 
be re-examined in the species L. (M.) vauceli and L. (M.) bal­
tazardi.
To date, all species in the subgenus Madoxyuris have been 
recorded from the family Lemuridae and each species has 
been described from a different species of host (Hugot and 
Baylac 2007). Chabaud et al. (1965) list the type host of 
L. bauchoti only as Hapalemur spp., but Hugot and Baylac 
(2007) give the type host as Hapalemur sirnus without any fur­
ther explanation. In any case, ours is the first record of a 
species of Lemuricola from a host genus different from the 
original, which contradicts the coevolutionary theories of a 
number of authors (Cameron 1929, Sandosham 1950, Inglis 
1961, Brooks and Glen 1982, Hugot 1999). However, a num­
ber of studies support a close phyletic affinity between Lemur 
catta and the genus Hapalemur (e.g. Crovella and Rumpier 
1992, Macedonia and Stanger 1994, Yoder and Irwin 1999, 
Delpero et al. 2001), agreeing in part with the theories about 
a possible association by descent between Lemuricola and 
species of Strepsirrhini.
Future records of Enterobiinae in lemurs will reduce the 
gaps in their host distribution, and will prove or disprove the 
degree of correspondence between parasite and host phy­
logeny.
Acknowledgments. This research was supported by a grant from the 
National Science Foundation (BSC 0525109). We thank the follow-
Unauthenticated 
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Redescription ofLemuricola (M.) bauchoti from L. catta in Madagascar 275
ing people for supporting this research: Jeannin Ranaivonasy, Andry 
Randrianandrasana, Joel Ratsirarson, Jeatmicq Randrianarisoa, and 
Youssouf Jacky Ibrahim. This research was supported by the Asso­
ciation Nationale pour la Gestion des Aires Protégées, the body gov­
erning research in Madagascar’s protected areas, and the Départe­
ment des Eaux et Forêts, Ecole Supérieure des Sciences Agrono­
miques. We thank Dana Whitelaw and members of the Beza Ma- 
hafaly Ecological Monitoring Team, especially Elahavelo and Enafa 
Efitroaromy. Special thanks to Jean Pierre Hugot for important sug­
gestions on taxonomy. We also thank Maria Cristina Estivariz 
(CEPAVE-CCT-CONICET) for the drawings; and to Patricia Sar­
miento (MLP-UNLP) for the SEM photographs.
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(Accepted May 14, 2010)
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Redescription of Lemuricola (Madoxyuris) bauchoti (Nematoda, Oxyuridae) from Lemur catta in Madagascar

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Redescription of Lemuricola (Madoxyuris) bauchoti (Nematoda, Oxyuridae) from Lemur catta in Madagascar

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