Observations on two Procamallanus (Spirocamallanus) species (Nematoda: Camallanidae) from freshwater fishes in Argentina, including description of Procamallanus (Spirocamallanus) juana sp. nov.
Author
Ailán-Choke, Lorena Gisela
text
Zootaxa
2017
2017-09-21
4323
2
286
294
journal article
32034
10.11646/zootaxa.4323.2.12
352a8612-76b6-48f4-b3f9-50107c119980
1175-5326
898866
07F176A4-Fc26-4A3E-8Dde-B03E29Dab799
Procamallanus
(
Spirocamallanus
)
juana
sp. nov.
(
Figs 1–2
)
Type material.
Holotype: female CH-N-FML #07729; allotype: male CH-N-FML #07730; paratypes (four females, five males) CH-N-FML #07731.
Type host.
Pimelodus albicans
Valenciennes
(
Siluriformes
,
Pimelodidae
), Ichthyology Collection CI-FML #6467, collected
30 May 2013
.
Additional host
:
Pimelodella gracilis
(Valenciennes)
(
Siluriformes
, Heptateridae), Ichthyology Collection CI- FML #6519, collected
30 May 2013
.
Type
locality
.
Salado River
,
Añatuya
,
General Taboada Department
, Province of
Santiago del Estero
(
28° 48’42”S
,
62°39’0.9”W
), Northwest
Argentina
.
Etymology.
The new species is named in honor of the memory of Juana Rosa Bennasar de Herrera (“Ms. Monona”), colleague, friend and for years Director of Zoology Area, FML.
Site of infection
.Intestine.
Infection parameters
. For
P. albicans
, prevalence: 75% (3/4); media intensity: 3.3 nematodes per fish and for
P. gracilis
, 75% (3/4); 4 nematodes per fish, respectively.
Measurements.
Table 1
.
TABLE 1.
Measurements of
Procamallanus
(
Spirocamallanus
)
juana
sp. nov.
Given in mm, mean ± SD (minimum value–maximum value). (* Measurement of total length of tail, including the spike).
| Character |
Holotype |
Allotype |
Paratypes |
| ♀ 1 |
♂1 |
♀4 |
♂5 |
| Total body length |
22,23 |
10.28 |
21.19±4.31 (15.46–24.25) |
10.69±1.51 (8.35–12.00) |
| Body width |
0.35 |
0.16 |
0.31±0.05 (0.27–0.37) |
0.17± 0.02(0.15–0.20) |
| Buccal capsule length |
0.06 |
0.053 |
0.06±0.00 (0.06) |
0.05±0.00 (0.05) |
| Buccal capsule width |
0.06 |
0.05 |
0.06±0.00 (0.06) |
0.05±0.00 (0.05–0.06) |
| Cephalic ring length |
0.013 |
0.01 |
0.01±0.00 (0.01) |
0.01±0.00 (0.01) |
| Cephalic ring width |
0.033 |
0.033 |
0.03±0.00 (0.03–0.04) |
0.03±0.00 (0.02–0.03) |
| Muscular esophagus total length |
0.63 |
0.35 |
0.60±0.03 (0.56–0.63) |
0.54±0.02 (0.51–0.56) |
| Muscular esophagus total width |
0.07 |
0.06 |
0.07±0.00 (0.07) |
0.06±0.00 (0.05–0.06) |
| Glandular esophagus total length |
0.94 |
0.87 |
0.84±0.11 (0.70–0.93) |
0.82±0.11 (0.70–0.93) |
| Glandular esophagus total width |
0.06 |
0.05 |
0.06±0.00(0.06) |
0.05±0.00 (0.04–0.05) |
| Nerve ring—anterior end |
0.23 |
0.24 |
0.26±0.01 (0.25–0.26) |
0.23±0.01 (0.22–0.23) |
| Excretory pore—anterior end |
0.3 |
0.49 |
0.37±0.04 (0.32–0.40) |
0.42±0.07 (0.35–0.49) |
| Deirids |
- |
0.1 |
- |
0.12±0.03 (0.10–0.18) |
| Vulva—anterior end |
15.00 |
14.79±2.86 (10.50–16.36) |
- |
| Right spicule |
- |
0.75 |
- |
0.79±0.02 (075–0.80) |
| Left spicule |
- |
0.27 |
0.27±0.01 (0.26–0.28) |
| Caudal alae length |
- |
0.32 |
- |
0.34±0.04 (0.30–0.40) |
| Tail length* |
0.12 |
0,14 |
0.12±0.01 (0.11–0.12) |
0.14±0.03 (0.12–0.20) |
| Spike length |
0.02 |
- |
0.02±0.00 (0.02) |
- |
| Larvae length |
0.26 |
- |
0.28±0.06 (0.20–0.32) |
- |
General description.
Medium-sized nematodes with finely, transversely striated cuticle. Mouth aperture rounded, provided and surrounded by six visible pores, fourteen submedian cephalic papillae arranged in three circles, two circlets (medium and external) with four papillae each; and the inner circlet with six larger papillae. Pair of medium amphids present (
Fig. 1D
,
2A
). Buccal capsule orange-brown, thick-walled, barrel-shaped, slightly longer than wide, with simple well developed basal cephalic ring; wall of middle part of capsule strengthened by conspicuous thickenings appearing in lateral view as drop-shaped, extending anteriorly to anterior margin of capsule. In both sexes, inner surface of capsule provided with several spiral ridges, which may be complete and incomplete (not extending from one lateral margin of capsule to other) (
Figs. 1A, B, C
). Muscular esophagus somewhat shorter than glandular esophagus; both parts of esophagus slightly expanded near their posterior ends (
Figs. 1A, C
). Intestine narrow. Deirids, observed only in males; small, simple, with rounded end situated at about mid-way between posterior end of buccal capsule and nerve ring (
Figs. 2B, C
). Excretory pore located approximately in the middle of the muscular esophagus(
Figs. 1A, C
). Tail of females pointed and of males conical (
Figs. 1F, G
).
Adult female (five gravid specimens): Buccal capsule with 5–7 inner spiral ridges (
Figs. 1C
). Deirids absent. Vulva pre-equatorial with conspicuous lips (
Fig. 1E
,
2E
). Vagina muscular, directed posteriorly from vulva. Uterus containing larvae (
Figs. 1E
). Tail pointed with terminal spike (
Figs. 1F
,
2F
).
Adult Male (six specimens): Buccal capsule with 5–7 inner spiral ridges (
Fig. 1B
). Deirids present (
Figs. 2B, C
). Spicules of similar shape, but very unequal in length, right spicule larger than left, both with pointed distal ends (
Fig 1G
). Six pairs of sessile caudal papillae: three pairs preanal and three pairs postanal (
Figs. 1G
,
2D
). Gubernaculum absent. Posterior end of body ventrally bent, provided with narrow caudal alae. (
Figs. 1G
,
2D
). Tail conical (
Fig 1G
).
Remarks
. The new species belongs to the genus
Procamallanus
Baylis, 1923
, which is characterized by the presence of a solid buccal capsule continuous with the inner surface smooth or with spiral ridges,spicules usually unequal, and caudal alae and gubernaculum present or absent in males. Three subgenera occur in Neotropical freshwater fishes. The new species herein described belongs to the subgenus
Spirocamallanus
Olsen, 1952
, because both males and females present spiral thickenings (ridges) in the buccal capsule and the base of the male capsule without teeth (
Moravec 1998
).Between the species of
Procamallanus
(
Spirocamallanus
)
recorded for the Neotropical Region, it is possibly distinguished as a morphological group that present caudal alae and unequal spicules, represented by
P.
(
S
.)
rarus
,
P.
(
S.
)
solani
Pinto, Fabio, Noronha & Rolas
,
P.
(
S.
)
paraguayensis
(Petter)
,
P.
(
S.
)
freitasi
(Moreira, Oliveira & Costas)
,
P.
(
S.
)
pimelodus
Pinto, Fábio, Noronha & Rolas
,
P.
(
S.
)
dessetae
(Petter, Golvan & Tcheprakoff)
,
P.
(
S.
)
rebecae
(Andrade-Salas, Pineda-Lopez & Garcias-Magaña)
and the new species herein described.
The general morphology of the new species is very similar to
P.
(
S.
)
pimelodus
; both species are characterized by possessing three pairs of preanal papillae and caudal alae in males, the right spicule exceeds
0.70 mm
and the vulva is pre-equatorial. However, both species differ in the number of cephalic papillae (14 vs. 8); the presence or absence of pores around the mouth aperture; the number of pairs of postanal papillae (3 vs. 8) and the shape of the female tail (pointed with a spike vs. conical without spike). By the presence of caudal alae in males, the new species also resembles
P.
(
S.
)
rarus
.
Moreover both species were found in freshwater catfishes from
Argentina
. However, these species differ in that,
P.
(
S.
)
juana
sp. nov.
has sessile caudal papillae, while those of
P.
(
S
.)
rarus
are pedunculated; the vulva in the new species is pre-equatorial while in
P.
(
S.
)
rarus
it is equatorial, and the spicules are simple in
P.
(
S.
)
juana
sp. nov.
While
P.
(
S.
)
rarus
has unequal and dissimilar spicules, the large spicule with a small ventral outgrowth and the small spicule simple.
The presence of a digit-like projection provided with one or more small terminal cuticular spikes on the female tail, is a feature that the new species shares with some species of
Procamallanus
(
Spirocamallanus
)
, parasites of freshwater and marine fishes (
Moravec
et al.
2000
). In the Neotropical Realm some species have this character. These include
P
. (
S.
)
rebecae
;
P.
(
S.
)
solani
;
P.
(S.)
penneri
(Fusco & Brooks);
P.
(
S.
)
gobiomori
Moravec
, Salgado- Maldonado &
Caspeta-Mandujano, 2000
; and
P.
(
S.
)
jaliscensis
Moravec, Salgado-Maldonado
& Caspeta- Mandujano, 2000; all of them are parasites of freshwater fishes (
Moravec 1998
;
Moravec
et al.
2000
). These species can be distinguished from
P.
(
S.
)
juana
sp.nov.
by a series of morphological features (such as the number of spiral thickenings in the buccal capsule and the length of right spicule) and the geographical distribution.
Most of the species of
Procamallanus
(
Spirocamallanus
)
have eight cephalic papillae arranged in two circlets. Nevertheless, the new species is the first in presenting fourteen cephalic papillae organized in three circlets, the external and median circlet formed by four papillae and the inner by six papillae, the papillae of the inner circlet distinctly large.
Procamallanus
(
Spirocamallanus
)
halitrophus
(Fusco & Overstreet)
,
P
. (
S
.)
rebecae
,
P
.(
S
.)
rigbyi
Yooyen, Moravec & Wongsawad
and
P.
(
S.
)
similis
Yooyen, Moravec & Wongsawad
also have numerous cephalic papillae, all present 12 papillae organized in three circlets formed by four papillae each and the papillae of the external circlet are distinctly large (
Cardenas & Lanfredi, 2005
;
Yooyen
et al.
2011
). Nevertheless these species differ mainly in the host range and the geographical distribution. The first two species were recorded in the Neotropical Realm.
Procamallanus
(
Spirocamallanus
)
halitrophus
was record in marine fishes from the northern Gulf of
Mexico
and the coasts of
Rio de Janeiro
,
Brasil
; while
P.
(
S.
)
rebecae
was found in cichlid freshwater fishes from southern
Mexico
(
Moravec, 1998
). In contrast to
P
. (
S.
)
rigbyi
and
P.
(
S.
)
similis
that were recorded in marine perciform fishes from the Gulf of
Thailand
(
Yooyen
et al.
2011
).
By the presence of pores surrounding the margin of the oral opening,
P.
(
S.
)
juana
sp. nov.
resemble
P.
(
S.
)
daleneae
(Boomker)
,
P.
(
S.
)
spiralis
Baylis
and
P.
(
S.
)
serranochromis
Moravec & Van As. The
first two present six pores, which coincides with the new species; while
P.
(
S.
)
serranochromis
has four pores in the cephalic end. Nevertheless, these species can be distinguished mainly from
P.
(
S.
)
juana
sp. nov.
by the geographical distribution.
Procamallanus
(
S.
)
daleneae
and
P.
(
S.
)
serranochromis
were only recorded in African freshwater fishes. While,
Procamallanus
(
S.
)
spiralis
was also found in Africa and in different species of marine fishes in the Gulf of Suez, off the Atlantic and Pacific coasts of
Mexico
, in Philippine and Indonesian waters (off the Celebes), and in the Indian Ocean off the coast of
Pakistan
and
India
(
Moravec & Van As 2015
).
Procamallanus
(S.)
juana
sp. nov
.
can be distinguished from all congeners, by possessing 14 cephalic papillae arranged in three circlets (one of six papillae and two remaining with four papillae); six pores distinctly surrounding the mouth aperture; a buccal capsule with 5–7 spiral ridges; three pairs of preanal and three pairs of postanal papillae in males and a terminal cuticular spike on the female tail. Thus in this paper, we propose the erection of the new species of
Procamallanus
(
Spirocamallanus
)
, which is the 30th species of this genus for Neotropical Realm and the sixth for
Argentina
.
FIGURE 1.
Procamallanus
(
Spirocamallanus
)
juana
sp. nov.
(A) Male, anterior end, lateral view. (B) Male, head, lateral view. (C) Female, anterior end, lateral view. (D) Female, apical view. (E) Female, vulva, lateral view. (F) Female, tail, lateral view. (G) Male, posterior end with spicules and papillae, ventral view.
FIGURE 2.
Procamallanus
(
Spirocamallanus
)
juana
sp. nov.
(SEM micrographs) (A) Male, cephalic end. Six pores (white arrows), amphids (black arrows). Scale=10µm. (B) Anterior end of male, sublateral view. Deirid (white arrow). Scale= 10µm. (C) Detail deirid. Scale=1µm. (D) Posterior end of male, ventral view. Preanal papillae (white arrows). Scale=10µm. (E) Female, vulva, subventral view. Scale=10µm. (F). Female, posterior end, lateral view. Scale=10µm.
Procamallanus
(
Spirocamallanus
)
hilarii
Vaz & Pereira, 1934
Specimens
examined.
Six
males and one female CH-N-FML #7732 isolated from
Hyphessobrycon anisitsi
(Eigenmann, 1907)
(CI-FML #6429) from
Salado River
,
Añatuya
,
General Taboada Department
, Province of
Santiago del Estero
(
28° 48’42”S
,
62°39’0.9”W
)
,
Northwest
Argentina
.
Infection parameters.
Prevalence: 57% (4/7), mean intensity 1.75 nematodes per fish.
Diagnosis.
Medium nematodes with transversely striated cuticle. Buccal capsule with 13–18 spiral thickenings, basal ring well development. Muscular esophagus claviform, much shorter than glandular esophagus. Male with three pairs of preanal, 1–2 pairs adanal and three pairs of postanal papillae. Gubernaculum absent. Spicules short and subequal. Larger spicule 0.070–0.082, small spicule 0.050–0.062.Tail conical.In females, vulva in middle of body; uterus containing larvae. Tail rounded with terminal caudal appendix.
Remarks.
The morphological and morphometric analyses of the specimens analyzed by light microscopy, allowed the identification of
Procamallanus
(
Spirocamallanus
)
hilarii
, agreeing with the original description.
Procamallanus
(
S.
)
hilarii
belongs to a morphological group of species without caudal alae and with short and similar spicules in males, represented by
P.
(
S.
)
chimusensis
(Freitas & Ibañez)
,
P.
(
S.
)
inopinatus
Travassos, Artigas & Pereira
,
P.
(
S.
)
krameri
(Petter)
,
P.
(
S.
)
neocaballeroi
(Caballero-Deloya)
,
P.
(
S.
)
paraensis
Pinto & Noronha
,
P.
(
S
.)
pintoi
(Khon & Fernandes)
and
P
. (
S.
)
saofranciscencis
(Moreira, Oliveira & Costas)
(
Moravec
et al.
2004
).
By the general morphology,
Procamallanus
(
S.
)
hilarii
is most closely related with P.
(
S.
)
neocaballeroi
. Both species present numerous spiral ridges (13–19) occupying the whole inner surface of the buccal capsule and a glandular esophagus at least three times longer than muscular esophagus.
Procamallanus
(
S.
)
neocaballeroi
can be readily distinguished from
Procamallanus
(
S.
)
hilarii
by possessing equal spicules and four pairs of preanal papillae and six pairs of postanal papillae. Moreover these species differ in the geographical distribution in the Neotropical Region.
Procamallanus
(
S.
)
hilarii
was recorded for
Brazil
,
Perú
and
Argentina
; while
P.
(
S
.)
neocaballeroi
has only been recorded in
Mexico
(
Moravec 1998
).
Discussion.
The genus
Procamallanus
Baylis, 1923
comprises numerous species described in a broad variety of host and geographical regions, in both marine and freshwater fishes. Although, many authors (Andrade–Salas
et al.
1994) consider
Spirocamallanus
Olsen, 1952
as a distinct genus,
Moravec & Sey (1988)
consider
Spirocamallanus
a subgenus of
Procamallanus
to accommodate the species where both males and females have the buccal capsule with spiral ridges. Nevertheless, it is clear that this taxonomic system based on the morphology of the buccal capsule is more or less artificial and does not reflect the phylogenetic relationships (
Moravec & Thatcher 1997
).
Andrade-Salas
et al.
(1994)
proposed an alphabetic list with all nominal species grouped according to the geographical zones. However, this list is outdated, because later new species of
Procamallanus
were described. With respect to the Neotropical Realm, species of
Procamallanus
(
Spirocamallanus
)
occur both in marine and continental water systems. To date, there are 29 species recorded from freshwater fishes, and they are widely distributed for the Neotropical Realm; mainly in
Mexico
, Lesser Antilles,
Venezuela
,
Brasil
,
Paraguay
,
Perú
and
Argentina
.
In
Argentina
, there are five species of
Procamallanus
(
Spirocamallanus
)
(
P.
(
S.
)
inopinatus
,
P.
(
S.
)
rarus
,
P.
(
S.
)
huacraensis
,
P
.(
S.
)
hilarii
and
P.
(
S.
)
pintoi
) recorded from characiform and siluriform freshwater fishes, mainly distributed in the regions northwest and northeast of the country. In the province of
Corrientes
, northeast region, it was registered
P.
(
S.
)
inopinatus
in Totora
y Perez Lagoon, Riachuelo basin, and Riachuelo River Lagoon; and
P.
(S.)
rarus
in
Parana
River.
Procamallanus
(
S.
)
inopinatus
presents a wide host range. It was recorded from specimens of
Characiformes
(
Brycon orbignyanus
Valenciennes
,
Poptella paraguayensis
Eigemann
,
Leporinus maculatus
Müller & Troschel
,
Serrasalmus marginatus
Valenciennnes
,
S. spilopleura
Kner
,
Pygocentrus nattereri
Kner
) and
Siluriformes
(
Luciopimelodus pati
Valenciennes and
Pseudoplatysoma
corruscans
Spix & Agassiz). By contrast,
P.
(
S.
)
rarus
was only found in
P. albicans
(
Chemes & Takemoto 2011
)
. Moreover, there are many records of both species in
Brasil
.
Procamallanus
(
S.
)
inopinatus
is also recorded from
Paraguay
and
Venezuela
and
P.
(
S
.)
rarus
from
Perú
(
Moravec 1998
). The new species herein described is most closely related with
P. (S.) rarus
by the presence of caudal alae and both species were found in the same host,
P. albicans
.
With respect to the northwest region, there are three species recorded:
P.
(
S.
)
huacraensis
,
P.
(
S.
)
pintoi
and
P.
(
S.
)
hilarii
. The first two were found only in catfishes:
Trichomycterus corduvensis
and
T. spegazzini
respectively (All
Trichomycteridae
).
Procamallanus
.
(
S.
)
huacraensis
was registered from Huacra and Vis-Vis Rivers, and Dike Agua Fresca (
Catamarca Province
). While, there is a unique record of
P.
(
S.
)
pintoi
in irrigation ditch tributary of River Yacones (Vaqueros municipality,
Salta Province
).
Procamallanus
(
S.
)
hilarii
was recorded in a wide host spectrum:
Salminus brasiliensis
Cuvier
(=
S. maxillosus
Valenciennes
),
Megaleporinus obstusidens
Valenciennes
(=
Leporinus obstusidens
Valenciennes
),
Oligosarcus jenynsii
Günther
,
Hoplias malabaricus
Bloch,
A.
abramis
Jenyns,
A. lacustris
Lutken,
A. rutilus
Jenyns,
Piabina thomasi
Fowler
(all characids);
Pimelodus albicans
Valenciennes
(
Pimelodidae
,
Siluriformes
) and
Jenynsia alternimaculata
Fowler
(
Anablepidae
,
Cyprinodontiformes
). Its geographical distribution includes dam, rivers, streams and tributaries from several localities of the provinces of
Tucumán
,
Santiago del Estero
and
Salta
(
Northwest
Argentina
) (
Ailan
et al.
2014
;
Antelo
et al
. 2016
;
Ramallo 2008
).
Procamallanus (S.) juana
sp. nov.
was also found in
P. albicans
.
Thus both species (
P.
(
S.
)
juana
sp. nov.
and
P.
(
S.
)
hilarii
) share the same host species and present records in the province of
Santiago del Estero
. However, these species differ in their general morphology, mainly in the presence of caudal alae, the number of spiral ridges in the buccal capsule and the number of caudal papillae in males (
Moravec 1998
).
With the new finding, the number of species of
Procamallanus
(
Spirocamallanus
)
was extended for the Neotropical Realm. Moreover,
P.
(
S.
)
hilarii
extends its host range and geographical distribution.