ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
A NEW STRONGYLOID FROM MONKEYS IN HIMACHAL PRADESH, INDIA
UN NUEVO ESTRÓNGILO DE MONOS EN HIMACHAL PRADESH, INDIA
Department of Biosciences. Himachal Pradesh University, Shimla, India- 171005
*Corresponding Author: rakesh67chandel@gmail.com
Rakesh Chandel*; Somesh Sharma & Deepak C. Kalia
ABSTRACT
Key words: Strongyloid – Oesophagostomum (Conoweberia) mandiensis n.sp. – Macaca mulatta
Oesophagostomum (Conoweberia) mandiensis n.sp. recovered from the stomach of male monkey,
Macaca mulatta (Zimmermann, 1780) at Narla (Drang) district Mandi of Himachal Pradesh, India is
described. This species differs from the other 15 known species of the genus in having an apical triangular
lancet on each of the three denticulated oesophageal walls.
Neotropical Helminthology
349
Neotropical Helminthology, 2017, 11(2), jul-dic: 349-348
RESUMEN
Palabras clave: Estrongiloideo – Oesophagostomum (Conoweberia) mandiensis sp. n. – Macaca mulatta
Oesophagostomum (Conoweberia) mandiensis sp. n. recuperada del estómago del mono macho, Macaca
mulatta (Zimmermann, 1780) en el distrito de Narla (Drang) Mandi de Himachal Pradesh, India es
descrita. Esta especie difiere de las otras 15 especies conocidas del género al tener una lanceta triangular
apical en cada una de las tres paredes esofágicas denticuladas.
INTRODUCTION of which found along the roadside at village Narla
(Drang) district Mandi of Himachal Pradesh, India
(Zimmermann, 1780). This species has been
described and discussed in the light of 15 already
known species of the subgenus Oesophagostomum
(Conoweberia) Ihle, 1922 and has been found to be
new to science.
During the survey of nematode parasites from
monkey host, 15 specimens of the present species
were recovered from the stomach of male host,
Macaca mulatta (Zimmermann, 1780), the carcass
MATERIAL AND METHODS
350
from the anterior extremity (Fig.1A); bursa
symmetrical, with weakly differentiated dorsal
lobe, each lateral lobe with an anterior and a
median papilla (1C, 1D, 2N, 2O); ventral rays
parallel, adjoining and extend to bursal margin;
externo-lateral rays slightly divergent not
extending to the bursal margin; medio-lateral and
postero-lateral rays parallel, extending to the bursal
margin, externo-dorsal rays arising from the
common stem with dorsal; dorsal bifurcated in its
distal half, each with a small external accessory
branch (Fig.1C, 1D); spicules 0.90-1.008 mm long,
equal, alate, with fused tips, spicular termination as
ostrich claw-shaped (Fig.1E); gubernaculum
0.081-0.13 mm long and inverted tinner-shaped
hammer(Fig.1F); genital cone oblong, with two
small, rounded, lateral papillae (Fig. 1D).
Female: Body 10.35-15.21 mm long,0.33-0.45
mm in maximum thickness; oesophagus 0.56-0.59
mm long; oesophageal funnel 0.045×0.065 mm;
nerve ring 0.18-0.20 mm, excretory pore 0.22-0.27
mm from anterior extremity; tail 0.19-0.22 mm
long and conical (Fig. 1G, 2P); vulva 0.31-0.45 mm
from posterior extremity; ovejector 0.20-0.22 mm
long and 0.09-0.12 mm wide; eggs 0.045-0.060×
0.044-0.060 mm in size (Fig. 1G).
Taxonomic summary
Type Host: Macaca mulatta (Zimmermann, 1780)
Location: Stomach
Type Locality: Narla (Drang) district Mandi
Himachal Pradesh, India
Specimens deposited: Holotype, Cat. PCPL 001
(one male); Paratypes, Cat. PCPL 010 (two males
and five females).
Etymology: The specific epithet refers to the
locality of collection of host.
Differential diagnosis: Each oesophageal funnel
with an apical triangular lancet; spicular
termination as ostrich claw-shaped; gubernaculum
0.0831-0.13mm long and an inverted tinner-
shaped hammer.
Specific diagnosis: Each oesophageal funnel with
an apical triangular lancet; each lateral lobe of
caudal bursa with an anterior and a median papilla;
spicules 0.90-1.008 mm long, equal, alate, alae
ending in small swelling just in front of spicule tip,
spicular termination as ostrich claw-shaped;
gubernaculum 0.0831-0.13mm long and inverted
tinner-shaped hammer.
Specimens of Oesophagostomum (Conoweberia)
mandiensis n.sp. were recovered from its host at
village Narla (Drang), India in May, 2015. The
worms were killed and fixed in 3- 4% formalin and
bulk cleared in lactophenol for microscopic
examination, as per ethical approval of Department
of Biosciences, Himachal Pradesh University,
Shimla. The sketches incorporated were made with
the help of camera lucida and measurements were
taken with the help of ocular and stage micrometers
and photomicrographs were taken with the help of
Leica microscope DML S2 Camera DFC 320 and
scanning micrographs JEOL-2601. All the
specimens (Holotype and Paratypes) were
deposited in Parasite collection of the Parasitology
laboratory (PCPL), Department of Biosciences,
HPU Shimla, India.
Oesophagostomum (Conoweberia) mandiensis n.
sp.
(Figs. 1-3)
Description: (Based on 15 specimen (6 males and 9
females): Body stout, whitish when alive, cuticle
with thick striations, having external leaf crown
only with 12 elements; cephalic vesicle present;
excretory pore at the level of cervical groove,
mouth directed straight forward; submedian
cephalic papillae 4 and 1 pair of lateral amphids
(Fig. 1A, 1B, 2M); buccal capsule closed, shallow,
wider posteriorly, without transverse processes
internally; oesophagus club- shaped, muscular,
with an anterior oesophageal funnel, 0.045-0.063
mm deep, consisting of three denticulated concave
walls and each wall provided with an apical
triangular lancet (Fig. 1B); cervical papillae at
about middle of oesophagus; prebursal papillae
and lateral bursal papillae present (Fig.1D, 2N,
2O).
Male: Body 9.36-11.61 mm long, 0.27-0.40 mm in
maximum thickness; oesophagus 0.54-0.57 mm
long; nerve ring 0.15-0.16 mm; excretory pore
0.22-0.23 mm and cervical papillae 0.22-0.28 mm
Neotropical Helminthology, 2017, 11(2), jul-dic
RESULTS
Chandel et al.
351
3-(12): Oesophageal funnel lancets having
chitinized.
4-(7): Oesophageal funnel lancets simple and
conical.
5-(6): Oesophageal funnel with its cuticular lining
forming 3 alae projecting into the lumen. Spicules
0.832 mm long (from Sus scrofa in India).
………. O. (C.) maplestonei (Schwartz, 1931)
emend Schwartz, 1932
6-(5): Oesophageal funnel lancets arising from its
wall near the base and directed anteriad, having
broad bases and pointed tips. Spicules 1.6 mm long
(from Semnopithecus obscurus in India).
……… O. (C.) tridentatum Maplestone, 1932
7-(4): Oesophageal funnel lancets otherwise.
8-(9): Oesophageal funnel lancets hook-shaped.
Oesophageal funnel having three slightly hook-
shaped lancets (teeth) with their tips directed
inwards and somewhat posteraid. (from Simia
satyrus; Papio hamadryas in Switzerland and East
Africa).
……… O. (C.) brumpti Railliet and Henry, 1905
9-(8): Oesophageal funnel lancets varying in
shape.
10-(11): Oesophageal funnel with 3 winding
contours at its anterior margin, each carrying a
dentiform processes. Spicules 1.29 mm long. (from
Xerus setosus in London zoo from South African
rodents).
……… O. (C.) xeri Ortlepp, 1922
11-(10): Oesophageal funnel having 3 chitinized
sharply curved sickle-shaped elements connected
at their edges, and each one provided with a conoid
projection at its base, directed inwards. Spicules
0.062 mm long (male 5.0-5.55 mm long). (from
Papio maimon in Hamburg zoo).
……... O. (C.) zukowskyi Travassos and
Vogelsang, 1931.
12-(3): Oesophageal funnel lancets normally
chitinized.
13-(14): Oesophageal funnel having 3 lancets
consisting of thickened chitin membrane. Spicules
1.44 mm long. (from Cercopithecus sabaeus; C.
nictitans; C. ruber; C. callitrichus in Tropical
Africa).
…….. O. (C.) pachycephalum Molin, 1861
Remarks
The species in having the characterstics, viz.,
external elements; buccal capsule ring-like,
without transverse processes internally and the
width considerably exceeding its length;
oesophagus club-shaped; cephalic vesicle
separated from remaining body by ventral groove
has been assigned to genus Oesophagostomum
Molin, 1861 and its corona radiata with 12 (10-15)
elements; buccal capsule wide posteriorly; large
oesophageal funnel with three concave walls, each
with tooth and cervical papillae anterior to
o e s o p h a g e a l s w e l l i n g t o s u b g e n u s
Oesophagostomum (Conoweberia) Ihle, 1922 (in
agreement with Lichtenfels, 1980; Gibbons, 2010).
The already known species of the subgenus
Oesophagostomum (Conoweberia) can be grouped
on the basis of presence or absence of
lancets/denticles on the walls of oesophageal
funnel (Molin, 1861; Ihle, 1922; Travassos, 1930;
Lichtenfels, 1980; Gibbons, 2010). Phylogenetic
tree of species of O e s o p h a g o s t o m u m
(Conoweberia) is indicated by Brooks et al.
(2005).
Oesophagostomum (Conoweberia) mandiensis n.
sp. closely resembles Oesophagostomum
(Conoweberia) zukowskyi Travassos & Vogelsang,
1931 having three lancets on the walls of
oesophageal funnel; gubernaculum consisting of
strongly chitinized portion, which when viewed
laterally has two ends; spicules 0.062mm long;
O.(C.) kherai Kalia, 1985 having 4 lancets on walls
of oesophageal funnel; spicules 1.516 mm long,
equal, alate, alae ending in a small tuberculated
swellings just in front of the spicule tip;
gubernaculum 0.15 mm long, lamina shaped and
O. (C.) amarpurense Chandel & Kalia, 1995,
oesophageal funnel walls with nine lancets;
spicules 1.377mm long, alate; gubernaculum 0.12-
0.15mm long. The differences between the 15
species of the subgenus are in the Key to species of
sub genus Oesophagostomum (Conoweberia)
included below (Kalia, 1985; Chandel & Kalia,
1995).
Key to species of sub genus Oesophagostomum
(Conoweberia)
1-(20): Oesophageal funnel with lancets/denticles.
2-(15): Oesophageal funnel with 3 lancets.
Neotropical Helminthology, 2017, 11(2), jul-dic A new strongyloid from monkey
352
Figure 1. Oesophagostomum (Conowevberia) mandiense n.sp.
A. Anterior region, lateral view
B. Anterior region (enlarged), lateral view
C. Posterior region of male, lateral view
D. Posterior region of male, ventral view
E. Spicule tip (enlarged), lateral view
F. Gubernaculum (enlarged)
G. Posterior region of female, lateral view
Neotropical Helminthology, 2017, 11(2), jul-dic Chandel et al.
H
I
J
K
Figure 2. Oesophagostomum (Conowevberia) mandiense n.sp.
A. Cephalic view
B. Posterior region of male, dorsal view
C. Posterior region of male, ventral view
D. Posterior region of female
17-(18): Oesophageal funnel with 4 lancets, each
latero-ventral walls forms with a median bifid one
and dorsal wall with two conical ones. Spicules
1.516 mm long. (from Presbytis entellus in India).
……….O. (C.) kherai Kalia, 1985
18-(17): Oesophageal funnel lined with chitin
membrane which forms 6 large lancets with
slightly pointed tips directed upwards and inwards.
Spicules 1.32-1.47 mm long, non-alate.(from Felis
sp. in Brazil).
14-(13): Oesophageal funnel with one dorsal and
two sub-ventral thin pointed and slightly curved
lancets. Spicules 2.00 mm long. (from Hylobates
syndactilus; H. agilis; H. mulleri; H. hoolock in
Africa, Jawa, Borneo and Sumatra).
…….. O. (C.) Ovatum (Linstow, 1906) Railliet et
Henry, 1912
15-(2): Oesophageal funnel having more than 3
lancets.
16-(19): Oesophageal funnel upto 6 lancets.
Neotropical Helminthology, 2017, 11(2), jul-dic A new strongyloid from monkey
353
Hylobates hoolock in Indo-China, Jawa and
Borneo).
………. O. (C.) raillieti Travassos and Vogelsang,
1932
29-(16) Oesophageal funnel with less than nine
lancets.
30-(20) Oesophageal funnel wall denticulated,
each wall beset with an apical triangular lancet;
spicules equal, 0.90-10.8 mm long with fused tips,
spicular termination as ostrich claw-shaped.
………. O. (C.) mandiense n.sp.
The species under discussion differs from all the
known species of this group in its each oesophageal
wall with an apical triangular lancet, spicular
termination as ostrich claw-shaped; gubernaculum
0.0831-0.13mm long and inverted tinner-shaped
hammer. Hence, in view of the above differences,
this species has been considered new to the science
and named after the locality of the host (Railliet,
1916; Travassos & Vogelsang, 1931; Skryabin et
al., 1952). However, identification of all species of
Oesophagostomum using DNA sequence analysis
is required (Ota et al., 2015).
……… O. (C.) ventri Thornton,1924
19-(16): Oesophageal funnel with 9 lancets.
Oesophageal funnel beset with three lancets (teeth)
on each wall, which become progressively larger in
size towards the base of the wall. Spicules equal,
1.377-1.567 mm long. (from Presbytis entellus in
India).
……… O. (C.) amarpurense Chandel and Kalia,
1995
20-(1): oesophageal funnel without lancets.
21-(26): Externo-dorsal having common stem with
dorsal ray.
22-(25): Spicules helically coiled.
23-(24): Dorsal ray bifurcated twice, each of which
giving of very small external processes with
outwardly bent convex surfaces. Spicules 0.83-
1.14 mm long, gubernaculum boat-shaped in
lateral view with rounded proximal and pointed
distal ends. (from Cercopithecus ruber; Papio
procarius; P. sphinx; P. cynocephalus; P.
hamadryas, P. maimon, P. langheldi;Macacus
rhesus; M. murus; Anthropopitecus troglodytes;
man, in Africa and South Asia).
……… O. (C.) bifurcum (Creplin, 1849)
24-(23): Dorsal rays bifurcated twice, secondary
external trunk short and curved. Spicules long,
with alae extend from cloaca. Gubernaculum
groove-shaped, strongly chitinized. (from
Macacus cynomolgus; M. nemestrinus; Cebus
capucinus; C. sinicus in Indo-China, Jawa and
Borneo).
……… O. (C.) aculeatum ( Linstow, 1879)
25-(22): Spicules not helically coiled. Dorsal ray
bifurcated twice, secondary external trunk bent in
an elbow-like manner. Spicules 1.3-1.4 mm long,
free portion of spicules with veins. (from Simia
satyrus; Hylobates hoolock in Indo-China, Jawa
and Borneo).
……… O. (C.) blanchardi Railliet et Henry. 1912
26-(21) Externo-dorsal arising separately from
dorsal ray.
27-(28) Parasites of rodents. (from Pedetes cafer in
South Africa)
………. O. (C.) susannae Le Roux,1929
28-(27) Parasites of Primates. External leaf crown
with 14 petals. Spicules 1.98 mm long. (from
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subgenus. Journal of Parasitology and
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