Orientatractis brycini sp. nov. (Nematoda: Atractidae) from characiform freshwater fishes in Gabon, Africa
Author
David González-Solís
Author
Jean Mariaux
text
Revue suisse de Zoologie
2017
124
1
1
8
journal article
33322
10.5281/zenodo.322659
70c2f9d7-3d55-4226-8d02-1385064e8076
0035-418
322659
Orientatractis brycini
sp. nov.
Figs 1-3
Deposition of specimens:
Holotype
(MHNG- INVE-91071),
allotype
(MHNG-INVE-91072) and
paratypes
(MHNG-INVE-91073) in the Muséum d’histoire naturelle, Geneva. –
Paratypes
in the Helminthological Collection of the Institute of Parasitology, Biology Centre, Czech Academy of Sciences,
Č
eské Bud
ĕ
jovice (Cat. No. N-1072).
Type
host:
Brycinus macrolepidotus
Valenciennes
(
Alestidae
,
Characiformes
) (Body length
21.4 cm
).
Other host:
Xenocharax spilurus
Günther
(
Distichodontidae
,
Characiformes
) (Body length
15.5-20.2 cm
).
Site of infection:
Intestine.
Type
locality:
Bridge
on
Ogooué River
,
Haut-Ogooué
,
Gabon
(
01°38’24”S
;
13°31’48”E
; elev.
300 m
), collected on
28/11/2010
.
Other
localities:
Mpassa River
, near
Hotel Poubara
,
Franceville
,
Haut-Ogooué
,
Gabon
(
01°37’12”S
;
13°36’00”E
; elev.
300 m
),
30/11/2010
.
Prevalence and intensity:
Brycinus macrolepidotus
: prevalence 25% (1 fish infected/4 examined), mean intensity 24 nematodes (range 24).
Xenocharax spilurus
: 43% (3/7), 4.3 (2-8).
Etymology:
The specific name relates to the generic name of the fish host (i.e.,
Brycinus
).
Description
General
: Whitish, small-sized nematodes, with cuticle finely transversely striated. Anterior end rounded, posterior end with very slender, long, pointed tail (
Fig. 1
A, E). Oral opening rhomboid or quadrangular, with 2 lateral and 4 submedian poorly-developed lips (
Figs 1
D, 2A, B). Each submedian lip bearing one large spherical papilla and external pair of well-sclerotized, recurved, pointed spines joined at the base and a single large median spine. Lateral lips supporting large amphids; two small spines posterior to each amphidial pore present (
Figs 1
D, 2A-D). Lateral grooves extending from first third of esophagus to posterior end of body, but not reaching tail tip (
Figs 1
E, G, 2F). Esophagus divided in a cylindrical corpus, elongated isthmus, and posterior, well-developed, valved bulb (
Fig. 1
A, B). Nerve ring surrounding isthmus at its anterior end. Deirids small, knob-like, somewhat anterior or at level of nerve ring (
Figs 1
A, B, 2E). Excretory pore anterior to esophageal bulb (
Fig. 1
A, B). Intestine straight. Rectum a hyaline tube.
Male
(
22 specimens
, measurements of
holotype
in parentheses): Length of body 2.58-3.07 (3.04) mm, maximum width 52-93 (72). Length of corpus 130- 163 (150), of isthmus 289-346 (305); entire esophagus 436-507 (455). Width of esophageal bulb 33-47 (43). Nerve ring, excretory pore, and deirids 162-226 (178), 294-350 (310), and 175-199 (189), respectively, from anterior end of body. Eight pairs of caudal papillae: 1 subventral precloacal pair, 3 subventral adcloacal pairs, close to each other (one pair anterior to cloacal opening, one at same level and one posterior to it), 4 postcloacal pairs (first pair of postcloacals lateral, second and third pairs subventral and close to each other, fourth pair subdorsal) (
Figs 1
G, 3A). Pair of small, lateral outlets (probably representing phasmids) between pairs 3 and 4 of postcloacals (
Fig. 3
A, E). Single left-shifted papilla on anterior cloacal lip weakly-developed (
Fig. 3
C, D). Spicules unequal, similar, well-sclerotized. Left and right spicules 130-158 (148) and 75-90 (83) long, respectively. Both spicules with transverse striations along their lengths; proximal ends slightly expanded, distal ends sharply pointed (
Fig. 1
G, H). Gubernaculum 29-39 (37) long, well-sclerotized, proximal end rounded, with deep depression; distal end pointed and slightly ventrally curved (
Fig. 1
F). Tail 207-257 (229) long, with dorsal groove-like structure (
Fig. 3
B).
Fig. 1.
Orientatractis brycini
sp. nov.
(A) Whole body of male, lateral view. (B, C) Anterior end of body, lateral views. (D) Cephalic end, apical view. (E) Posterior end of female, lateral view. (F) Gubernaculum, lateral view. (G) Posterior end of male, lateral view. (H) Spicules, lateral view.
Fig. 2.
Orientatractis brycini
sp. nov.
, SEM micrographs. (A, B) Cephalic end, subapical and apical views, respectively (asterisks indicate single median spine). (C) Detail of lateral lip, amphid and lateral spines, apical view. (D) Cephalic end, sublateral view (asterisks indicate single median spine). (E) Deirid. (F) Anterior end of body (arrow indicates groove-like lateral ala). Abbreviations: a
‒
amphid, b
‒
cephalic submedian papilla, ls
‒
lateral paired spine, ss
‒
submedian paired spine.
Female
(13 gravid specimens; measurements of
allotype
in parentheses): Length of body 2.50-3.61 (3.30) mm, maximum width 60-129 (109). Length of corpus 126-170 (161), of isthmus 294-355 (318); entire esophagus 443- 509 (479). Width of esophageal bulb 34-50 (43). Nerve ring, excretory pore, and deirids 158-221 (217), 292-347 (331), and 196-205 (-), respectively, from anterior end of body. Vulva with anterior lip slightly elevated, near the posterior end of body, 2.19-3.18 (2.91) mm from anterior end of body, somewhat anterior to anal opening (
Figs 1
E, 3F). Distance anus-vulva 39-72 (44). Vagina muscular, anteriorly directed. Uterus containing fully developed larvae 673-1 176 (927) long; some females with developing eggs 236-305 × 93-110 (236-242 × 93- 94). Tail 270-388 (348) long, with pore-like phasmids between first and second thirds of tail length (
Fig. 1
E).
Remarks
Petter (1966)
erected the genus
Orientatractis
to allocate nematodes with a particular structure of the oral opening, specifically the presence of symmetrical groups of 3 sclerotized posteriorly directed spines surrounding mouth. Currently, this genus includes 7 valid species, namely:
O
.
asymmetrica
Gibbons & Platt,
2006
in
Rhinoclemmys pulcherrima
Gray (Testudines)
from
Costa Rica
,
O
.
campechensis
González-Solís & Moravec,
2004
in
Paraneetroplus bifasciatus
(Steindachner)
(reported as
Vieja bifasciata
) and
Cichlasoma pearsei
(Hubbs)
(both
Perciformes
) from Southern
Mexico
,
O
.
chiapasensis
González-Solís & Moravec,
2004
in
Theraps intermedius
(Günther)
(reported as
Vieja intermedia
) and
Tomocichla tuba
(Meek)
(both
Perciformes
) from Southern
Mexico
,
O
.
hamabatrachos
Bursey, Goldberg & Kraus,
2014
in
Austrochaperina basipalmata
(van Kampen) (Anura)
from New
Guinea
,
O
.
levanhoai
(
type
species) in
Indotestudo elongata
(Blyth)
(reported as
Testudo elongata
) (
Testudines
) from
Vietnam
,
O
.
leiperi
Buckley,
1969
in
Podocnemis vogli
Müller (Testudines)
from
Colombia
, and
O
.
mekongensis
Moravec, Kamchoo & Pachanawan,
2015
in
Pangasius bocourti
Sauvage (Siluriformes)
from
Thailand
(
Petter, 1966
;
Buckley, 1969
;
González-Solís & Moravec, 2004
;
Gibbons & Platt, 2006
;
Bursey
et al.,
2014
;
Moravec
et al.,
2015
). Even though the
type
species of the genus was not reviewed, we decided to emend the generic diagnosis, based on the already described species and present data, since several important features were not included in the original description (see
Petter, 1966
). Morphological features as the structure of the oral opening, presence of deirids, among others, were incorporated to the diagnosis for making it easier to distinguish
Orientatractis
from closely related genera (e.g.,
Klossinemella
and
Paraorientatractis
) within the
Atractidae
. Thus,
Orientatractis
and
Paraorientractis
have four bicornate submedian structures surrounding mouth, whereas
Klossinemella
shows eight pairs; the two first genera differ in the number of lips (6
vs.
4) and presence of ornamentations on the dorsal surface of body in
Paraorientatractis
. These changes do not modify the systematic position of the genus.
The four bicornate structures along with a pair of spines posterior to amphidial pore are only present in
O
.
brycini
sp. nov.
,
O
.
hamabatrachos
, and
O
.
leiperi
; while in
O
.
asymmetrica
,
O
.
campechensis
,
O
.
chiapasensis
,
O
.
levanhoai
,
O
.
mekongensis
are lacking.
Orientatractis brycini
sp. nov.
shows similar body length to that of
O
.
chiapasensis
, and is near the lower size range of
O
.
campechensis
,
O
.
leiperi
and
O
.
levanhoai
, whereas the remaining three species (
O
.
asymmetrica
,
O
.
hamabatrachos
,
O
.
mekongensis
) have larger bodies. However,
O
.
brycini
sp. nov.
differs from all species within the genus in the size of both spicules (except in
O
.
hamabatrachos
), gubernaculum and number and distribution of caudal papillae (see
Table 1
).
The new species shares some similarities with
Paraorientatractis semiannulata
Gibbons, Khalil & Marinkelle, 1997
, a nematode of
Podocnemis unifilis
Troschel (Testudines)
in
Brazil
(
Gibbons
et al.,
1997
). Both species harbour identical shape and structures surrounding mouth, such as each submedian lip with a pair of recurved pointed spines and single median spine near their distal margin, along with a pair of smaller spines posterior to amphidial pores. Moreover, both have two unequal, striated spicules, similar gubernaculum and number of caudal papillae. However, they differ in the ornamentations on the dorsal surface of body and striated, broad, well-developed lateral alae in
P
.
semiannulata
.
Caballero-Rodríguez
(1971)
described
Proatractis parvicapiticoronata
from the tortoise
Staurotypus triporcatus
in
Veracruz
,
Mexico
.
Later
, this species was transferred to
Klossinemella
as
K
.
parvicapiticoronata
by
Moravec
&
Thatcher
(1997)
.
González-Solís
&
Moravec
(2004)
stated that it probably belongs to
Orientatractis
according to the shape of spicules, number and distribution of caudal papillae and structure of the anterior end, but until the
type
material of
K
.
parviticoronata
is re-examined, it should be retained within the genus
Klossinemella
.
Fig. 3.
Orientatractis brycini
sp. nov.
, SEM micrographs. (A) Posterior end of male, sublateral view (arrows indicate caudal papillae). (B) Dorsal surface of male tail. (C, D) Region of cloaca, ventral views (arrow indicates left-shifted unpaired papilla). (E) Posterior end of male, lateral view (arrowhead indicates phasmids). (F) Region of anus and vulva, lateral view. Abbreviations: c
‒
anus, g
‒
groove-like dorsal structure, v
‒
vulva.
Table 1. Comparison of some selected measurements of the valid species of
Orientatractis
around the world; measurements are in micrometers, unless otherwise stated.
| Body length |
(mm) |
Spicule |
length |
Gubernaculum length |
Caudal papillae* |
| male |
female |
right |
left |
|
O
.
asymmetrica
|
4.1-4.3 |
3.7-5.5 |
86-104 |
220-239 |
56-66 |
4: 2: 3 + 1 |
|
O
.
brycini
sp. nov.
|
2.6-3.1 |
2.5-3.6 |
75-90 |
130-158 |
29-39 |
1: 3: 4 |
|
O
.
campechensis
|
3.0-3.5 |
3.3-4.3 |
84-106 |
430-506 |
62-74 |
0: 5: 4 + 1 |
|
O
.
chiapasensis
|
2.7-3.0 |
2.0-3.8 |
60-68 |
204-238 |
44-49 |
0: 5: 4 + 1 |
|
O
.
hamabatrachos
|
3.2-4.3 |
3.4-4.9 |
79-98 |
146-165 |
55-67 |
2: 1: 5 + 1 |
|
O
.
leiperi
|
3.0-3.9 |
2.7-4.3 |
160 |
470 |
76 |
3: 1: 5 + 1 |
|
O
.
levanhoai
|
3.3 |
3.4 |
90 |
170 |
40 |
3: 0: 5 |
|
O
.
mekongensis
|
5.3-6.6 |
7.7-8.9 |
90-105 |
306-384 |
33-51 |
2: 1: 5 |
* pairs of caudal papillae (without considering phasmids): precloacal: adcloacal: postcloacal + single median papilla (left-shifted in
O
.
brycini
sp. nov.
)
Interestingly,
O
.
brycini
sp. nov.
was found in two fish species of the order
Characiformes
, but from different families (
Alestidae
and
Distichodontidae
) and sampling localities (Ogooue and Mpassa). Despite this, there were no differences in the morphology and biometrical values among the nematodes from both hosts, although certain morphometric variability always occurs intraspecifically. Such morphological and biometrical variability which might be associated with local ecological conditions and physiological traits of host species is not uncommon (see
González-Solís & Moravec, 2004
).
Nothing is known about the life cycle of these nematodes, but as in other members of
Atractidae
, larvae develop to the third stage in uterus, thus auto-infection is possible (
Anderson, 2000
). Viviparity has greatly helped atractid nematodes to parasitize several unrelated vertebrates (i.e., turtles, fish, amphibians, grazing mammals) by venereal and oral transmission (
Baker, 1982
), and to be distributed in different zoogeographical regions (America and Indonesia). The present finding represents the eighth species in the genus
Orientatractis
and the fourth being reported from fish hosts, since other members were reported in tortoises (
O
.
levanhoai
,
O
.
leiperi
), frog (
O
.
hamabatrachos
), and turtle (
O
.
asymmetrica
). This is also the first record of a species of
Orientatractis
in Africa, which expands the geographical distribution of the genus, since it was previously reported from Costa Rica, Colombia, Mexico (American continent), Thailand,
Vietnam
(
Southeastern Asia
) and New Guinea (Melanesia).