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Redescriptions of the Nematodes Litomosoides patersoni (Mazza, 1928) (Onchocercidae) and Stilestrongylus stilesi Freitas, Lent, And Almeida, 1937 (Heligmonellidae) Parasites of Holochilus chacarius (Rodentia, Cricetidae) From Salta, Argentina

Authors:
  • National Council of Scientific and Technical Research -CONICET- Argentina
  • Universidad Nacional de Villa Mercedes (UNVIME)

Abstract and Figures

Two nematode species are redescribed from the type host species Holochilus chacarius Thomas (Rodentia, Cricetidae, Sigmodontinae) and from the type locality of 1 of them, i.e., Ingenio San Martín de Tabacal, Salta Province, Argentina. Rodents were deposited at the Colección Mamíferos Lillo, Tucumán, Argentina. Litomosoides patersoni (Mazza, 1928) (Onchocercidae) possesses a buccal capsule with irregular external walls, a buccal cavity smooth, becoming thinner near the oral opening, a complete set of head papillae, 3-6 pairs of cloacal papillae, and the " sigmodontis " type of spicules. Filarioids were found in 3 of 17 examined hosts. Stilestrongylus stilesi Freitas, Lent, and Almeida, 1937 (Heligmonellidae), whose description was based on male specimens, was found in all 17 of the examined hosts. Here, we describe the female and the synlophe of both sexes. Females are characterized by a short uterus with less than 25 eggs, short ovejector, short and conical tail, and the posterior extremity strongly invaginated in a cuticular expansion usually harboring 1 to several eggs. The synlophe is characterized by 29-31 sub-equal cuticular ridges at the mid-body, with single (in males) or double (in females) axis of orientation of the ridges. The present work validates and enlarges the original descriptions of both species and assigns the specimens from L. patersoni, recovered from the type locality and the type host species, as neotypes.
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REDESCRIPTIONS OF THE NEMATODES LITOMOSOIDES PATERSONI (MAZZA, 1928)
(ONCHOCERCIDAE) AND STILESTRONGYLUS STILESI FREITAS, LENT, AND ALMEIDA,
1937 (HELIGMONELLIDAE) PARASITES OF HOLOCHILUS CHACARIUS (RODENTIA,
CRICETIDAE) FROM SALTA, ARGENTINA
Juliana Notarnicola, Marı
´a Celina Digiani*, and Pablo Martı
´nLo´ pezÀ
Centro de Estudios Parasitolo´gicos y de Vectores–CEPAVE–CCT La Plata-CONICET, Calle 2 #584 (1900) La Plata, Argentina.
e-mail: julinota@yahoo.com.ar
ABSTRACT: Two nematode species are redescribed from the type host species Holochilus chacarius Thomas (Rodentia, Cricetidae,
Sigmodontinae) and from the type locality of 1 of them, i.e., Ingenio San Martı
´n de Tabacal, Salta Province, Argentina. Rodents were
deposited at the Coleccio´n Mamı
´feros Lillo, Tucuma´n, Argentina. Litomosoides patersoni (Mazza, 1928) (Onchocercidae) possesses a
buccal capsule with irregular external walls, a buccal cavity smooth, becoming thinner near the oral opening, a complete set of head
papillae, 3–6 pairs of cloacal papillae, and the ‘‘sigmodontis’’ type of spicules. Filarioids were found in 3 of 17 examined hosts.
Stilestrongylus stilesi Freitas, Lent, and Almeida, 1937 (Heligmonellidae), whose description was based on male specimens, was found
in all 17 of the examined hosts. Here, we describe the female and the synlophe of both sexes. Females are characterized by a short
uterus with less than 25 eggs, short ovejector, short and conical tail, and the posterior extremity strongly invaginated in a cuticular
expansion usually harboring 1 to several eggs. The synlophe is characterized by 29–31 sub-equal cuticular ridges at the mid-body, with
single (in males) or double (in females) axis of orientation of the ridges. The present work validates and enlarges the original
descriptions of both species and assigns the specimens from L. patersoni, recovered from the type locality and the type host species, as
neotypes.
In 1928, Mazza described a new filarioid species, Filaria
patersoni, from several chacoan marsh rats, Holochilus chacarius
Thomas, 1906 (originally regarded as H. vulpinus Brants, 1827)
from the Ingenio San Martı
´n de Tabacal, a sugar cane plantation
in Salta Province, Argentina (Mazza, 1928). The systematic
position of this species was complex and synonymyzed several
times (Vogel and Gabaldon, 1932; Chitwood, 1933; Vaz, 1934;
Esslinger, 1973; Bain et al., 1989). It was considered as
Vestibulosetaria patersoni (Mazza, 1928) by Vogel and Gabaldon
(1932) within a set of filarioid specimens parasitizing Rattus
norvegicus (Berkenhout, 1769) from Caracas, Venezuela (Vogel
and Gabaldon, 1932) and Sigmodon hispidus (Say and Ord, 1825)
from Jalisco and Michoacan, Mexico (Ochoterena and Caballero,
1932); as Litomosoides patersoni (Mazza, 1928) by Chitwood
(1933), who validated the genus Litomosoides Chandler, 1931; and
as L. carinii (Travassos, 1919) by Vaz (1934) and Esslinger (1973)
within a set of filarioids from Nectomys squamipes (Brants, 1827)
from Sao Pablo, Brazil (Vaz, 1934), and Melanomys caliginosus
(Tomes, 1860) from Valle, Colombia (Esslinger, 1973). Bain et al.
(1989) reexamined the material of most of these sets, with the
exception of that from Mazza, which is lost, and clarified the
systematic position from L. carinii and L. sigmodontis Chandler,
1931; they also created a new species based on the material of Vaz
(1934), i.e., L. kohnae (Vaz, 1934), and considered L. patersoni a
valid species.
In 1934, Mazza sent some specimens of the chacoan marsh rat
to Dr. F. Werneck of the Instituto Oswaldo Cruz, Brazil, who
kindly gave the intestines to Dr J. F. T. Freitas. Years later,
Freitas et al. (1937) described a new genus and species of
heligmonellid nematode from the intestines of these hosts, i.e.,
Stilestrongylus stilesi Freitas, Lent, and Almeida, 1937, plus 3
other new species, i.e., Hassalstrongylus argentinus (Freitas, Lent,
and Almeida, 1937) (5Longistriata argentina), Hassalstrongylus
mazzai (Freitas, Lent, and Almeida, 1937) (5Heligmonoides
mazzai), and Longistriata fortuita Freitas, Lent, and Almeida,
1937 (Heligmosomoidea); all were reported from a single H.
chacarius (syn. Holochilus balnearum Thomas, 1906) from Salta.
The original descriptions of most of these nematodes are
incomplete, particularly the Heligmosomoidea, for which the
publications prior to 1964 do not include the synlophe;
additionally, females were typically poorly described. Currently,
Stilestrongylus includes 24 species, and the synlophe of 21 of them
is known, but that of the nominal species, S. stilesi, remains
undescribed. The type material of S. stilesi is available from the
Helminthological Collection of the Instituto Oswaldo Cruz
(CHIOC), Rio de Janeiro, Brazil. However, its state of
preservation precludes making a correct redescription of the
species (M. C. Durette-Desset, pers. comm.). In contrast,
specimens from L. patersoni were not deposited in any collection.
In the present paper, we provide redescriptions of L. patersoni
and S. stilesi, based on specimens colleted in H. chacarius from
the Ingenio San Martı
´n de Tabacal, and designate neotypes for
the filarioid species, considering that the type material is lost.
MATERIALS AND METHODS
Seventeen H. chacarius Thomas, deposited in the Coleccio´n Mamı
´feros
Lillo (CML), Tucuma´n, Argentina, were examined for parasites. They
were captured in the Ingenio San Martı
´n de Tabacal, Departamento Ora´n,
Salta Province, in August and September 1990. Rodents were fixed in 10%
formalin and stored in 70%ethanol.
Filarial worms were recovered from the abdominal cavity and
heligmonellids from the small intestine. Nematodes were preserved in
70%ethanol. A transverse section posterior to the vulva was made in a
filarioid female, and microfilariae were isolated (Notarnicola et al., 2000).
Synlophe was studied, following the method of Durette-Desset (1985).
Measurements are given in micrometers, except otherwise stated, as the
range followed by the mean in parentheses. Classification used above the
family Heligmonellidae level follows Durette-Desset and Chabaud (1993).
The nomenclature and synonymy of the host species follows Wilson and
Reeder (2005). Parasites were deposited in the Helminthological Collec-
tions of the Museo de La Plata, La Plata, Argentina (CHMLP), and of the
Muse´um national d’Histoire naturelle, Paris, France (MNHN).
Received 3 February 2010; revised 8 June 2010; accepted 11 June 2010.
*Divisio´n Zoologı
´a Invertebrados, Museo de La Plata and CONICET.
Paseo del Bosque s/n (1900) La Plata, Argentina.
{Facultad de Ciencias Naturales y Museo, Universidad Nacional de La
Plata. Av. 60 y 122, 1900 La Plata, Argentina.
DOI: 10.1645/GE-2448.1
J. Parasitol., 96(5), 2010, pp. 993–1001
FAmerican Society of Parasitologists 2010
993
RESULTS
REDESCRIPTIONS
Litomosoides patersoni (Mazza, 1928)
(Figs. 1–21; Tables I, II)
General: Males about 2.5 times shorter than females. Cephalic
extremity attenuated. Mouth small. Four minute cephalic papillae
placed in rectangle stretched laterally; 4 labial papillae surround
oral opening (Fig. 4); amphids lateral, not salient. Buccal capsule
embedded in esophagus, with irregular external walls (Figs. 2, 3);
buccal cavity smooth, becoming thinner near oral opening.
Esophagus muscular, slightly glandular posteriorly. Tail attenu-
ated. Measurements given in Tables I and II.
Males (based on 4 specimens): Posterior region coiled. Left
spicule with handle shorter than blade; blade constituted by
membranous folded ala and terminal filament (Fig. 14). Right
spicule with poorly cuticularized heel (Fig. 15). Number of cloacal
papillae variable, from 3 to 6 pairs. One male with 1 pair of
adcloacal, 1 pair of lateral postcloacal papillae, and 1 papilla in
median ventral line (Fig. 18); other male with 1 precloacal pair, 1
adcloacal pair, and 4 postcloacal pairs (Figs. 19–21). Area rugosa
composed of transverse ridges of small longitudinal crests,
extending through coiled region (Figs. 16, 17).
Females (based on 4 specimens): Vulva far away from
esophagus-intestine junction. Vagina globular, ovejector muscular
directed posteriad (Fig. 1). Small divergent phasmids. In cross
section, at mid-body, lateral chords flattened and expanded
laterally; internal cuticular ridges square-shaped (Fig. 5).
Microfilariae: Body fusiform. Stout microfilariae. Anterior
extremity with small visible hook, tail attenuated with nuclei near
the tip tail. Sheath not visible (Fig. 9). Measurements based on
uterine microfilariae from female 2: 35 36mm; 44 36mm.
Taxonomic summary
Host: Three H. chacarius Thomas (Rodentia, Cricetidae)
deposited at Coleccio´n Mamı
´feros Lillo, numbers CML 5810,
CML 5813, CML 5825.
Material studied: Three males, 4 female anterior extremities,
and 1 posterior extremity deposited at CHMLP, numbers 5995
and 6007; 1 male deposited at MNHN, number 591 MQ.
Site of infection: Body cavity, between the intestinal mesentery
and testis. In host CML 5810, 1 male in small intestine.
Locality: Ingenio San Martı
´n de Tabacal (23u169S, 64u159W),
lote Milagros, Departamento Ora´n, Salta, Argentina.
Prevalence and mean intensity: Three of 17 hosts infected
(17.6%); 2.6 (1–5) worms per host.
Remarks
Litomosoides patersoni belongs to the ‘‘sigmodontis’’ group of
species (Bain et al., 1989; Notarnicola et al., 2000; Bain et al.,
2003) based on the morphological characteristics of both spicules.
The left spicule has a handle shorter than the blade and the blade
is divided in anterior membranous folded ala, with a terminal
filament; heel of right spicule not heavily cuticularized. Mazza
(1928) reported smaller length for the spicules; moreover,
Figure 4 in his paper clearly shows the ‘‘sigmodontis’’ type of
spicules. One of the males described herein possesses a similar
arrangement of the cloacal papillae as stated by Mazza (1928), but
others display a greater number of papillae (see Figs. 18–21).
Microfilariae are shorter and more stout compared with other
species of Litomosoides, which was also reported by Mazza (1928)
for microfilariae from blood smears.
Litomosoides patersoni can be differentiated from L. navonae
Notarnicola, 2005, a parasite of H. chacarius from Chaco and
Formosa Provinces, Argentina, by the shape of the buccal
capsule, the number and disposition of the cloacal and the head
papillae (Notarnicola, 2005). The 4 postcloacal papillae in L.
patersoni are mostly symmetrical, while in L. navonae there are 5–
6 asymmetric papillae. Moreover, the microfilariae in L. patersoni
are shorter (35–44 36mm vs. 70 33.8 mm) and the sheaths are
not visible as in L. navonae (Notarnicola, 2005). Moreover, L.
patersoni can be differentiated from other species of Litomosoides
from cricetid rodents because of the shape of the buccal capsule,
the stout microfilariae, and the complete presence of the head
papillae.
Stilestrongylus stilesi Freitas, Lent, and Almeida, 1937
(Figs. 22–34)
General: Medium-sized nematodes, usually coiled sinistrally
along ventral side, in different degrees. Coiling varying from
tightly and completely coiled in up to 6 spirals, partly coiled with
up to 3 spirals in anterior half, loosely coiled with 1–2 spirals at
anterior end, or uncoiled. Excretory pore within 74–81%of
esophagus length in males; 65–78%in females. Deirids small,
situated at level of excretory pore or slightly posterior (Fig. 22).
Ratio uterus length/body length 10–20%. Cephalic vesicle present.
In apical view, triangular buccal opening surrounded by thin ring.
Two amphids, 6 externo-labial papillae, and 4 submedian cephalic
papillae (Fig. 23).
Synlophe (2 males and 2 females): In both sexes, cuticle with
longitudinal, uninterrupted ridges appearing mainly on left side
posterior to cephalic vesicle, disappearing just anterior to caudal
bursa in males and extending up to end of terminal cuticular
dilatation in female. At level of esophagus-intestinal junction: 24
ridges in male, 25 in female (Fig. 24); 29–31 ridges in both sexes at
mid-body; unequal in size, ridges on ventral right quadrant,
smaller. In female, double axis of orientation, right axis inclined
at 60uto sagittal axis, left axis sub-frontal. In males, right axis
inclined at 63u, left axis at 54uto sagittal axis (Figs. 25, 27).
Within distal third of body length; in male, 29 ridges at 150 mm
anterior to caudal bursa, in female, 26 ridges at mid-length of
uterus (Figs. 26–28); ridges sub-equal in size in both sexes. Most
ridges with similar orientation than at mid-body.
Males (20 specimens, except otherwise stated): 2.62–3.73 (3.12)
mm long and 80–130 (100) wide at mid-body. Cephalic vesicle 50–
62 (57) long and 22–32 (28) wide. Nerve ring not observed.
Excretory pore situated at 200–270 (228) from apex (n 59).
Deirids, when observed (n 54), at same level than excretory pore.
Esophagus 260–310 (263) long (n 510).
Caudal bursa asymmetrical, with right lobe more developed
than left (Figs. 29, 30). Prebursal papillae not observed. Right
lobe: pattern of type 2–3; rays 2 and 3 joined proximally,
diverging at half of their length, stout and of similar length; rays
4–6 with long common trunk; ray 5 stout, with strongly reinforced
margins; rays 4 and 6 thinner, divergent from ray 5 at distal and
proximal third of its length, respectively (Fig. 29). Left lobe:
pattern of type 2-2-1; rays 2 and 3 joined proximally, diverging at
distal third of their length, stout and of similar length; rays 4 and
994 THE JOURNAL OF PARASITOLOGY, VOL. 96, NO. 5, OCTOBER 2010
FIGURES 1–9. Litomosoides patersoni (Mazza, 1928) female. (1) Anterior extremity. (2–4) Cephalic end, lateral, median, and apical views from female
2. (5) Transverse section posterior to the vulva. (6, 7) Tail, lateral and ventral views. (8) Tip of tail with phasmids. (9) Uterine microfilaria.
NOTARNICOLA ET AL.—REDESCRIPTION OF TWO NEMATODE SPECIES 995
FIGURES 10–17. Litomosoides patersoni (Mazza, 1928) male. (10) Anterior extremity. (11, 12) Cephalic end, lateral and median views from male 1.
(13) Cephalic end from male 2. (14, 15) Left and right spicule, lateral view from male 1. (16) Area rugosa at mid-length. (17) Posterior extremity showing
the extension of the area rugosa.
996 THE JOURNAL OF PARASITOLOGY, VOL. 96, NO. 5, OCTOBER 2010
FIGURES 18–21. Litomosoides patersoni (Mazza, 1928) male. (18) Posterior end showing the spicules and papillae from male 1. (19–21) Tail from male
2, lateral views from left and right sides and ventral view, respectively.
TABLE I. Measurements of males of Litomosoides patersoni (Mazza, 1928).
Measurements
CML5813 CML5810
M1 M2 M3 M4*
Body length 19.305 mm 15.85 mm 17.3 mm 12 mm
Maximum width 120 120 135 85
Buccal capsule (L 3W) 18 37.5 22 3819371739
Esophagus length 510 580 540 425
Nerve ring 340 360 340
Tail length 275 180 146 195
Left spicule 246 247 265
Handle/lamina 100/146 107/140 115/150
Right spicule 80 87 84 80
Area rugosa length 1,150 1,740 1,500 400
Area rugosa beginning at 500–1700 from
tip of tail 550–1,700 760–2,500 770–2,270 260–660
* Specimen found in the small intestine of the host.
TABLE II. Measurements of females of Litomosoides patersoni (Mazza, 1928).
Measurements
CML5813 CML5825
F1 ae +Tail F2 ae F3* F4 ae
Length of pieces 28.71 +15.345 mm ,31.6 mm
Maximum width 250 300 160 260
Width at vulva 170 200 150 175
Buccal capsule (L 3W) 24 3924392639 26.5 310
Esophagus length 780 650 700 690
Nerve ring 490 260 470 600
Tail length 500
Vulva to apex 1,520 2,050 1,350 1,600
Vulva to e-i junction{720 1,400 610 1,000
ae, anterior extremity.
* Female with the tail broken.
{Distance of the vulva to the esophagus-intestine junction.
NOTARNICOLA ET AL.—REDESCRIPTION OF TWO NEMATODE SPECIES 997
5 divergent at extremities; ray 6 short and thin, diverging from
common trunk at same level than the group formed by rays 2–3
(Fig. 30). Rays 8 thin, arising asymmetrically from proximal third
of dorsal ray. Dorsal ray divided at about distal third into 2
branches. These branches are not bifurcated at their distal end,
indicating that rays 9 and 10 probably are merged (Fig. 31).
Genital cone well developed, markedly conical, 100–140 (122)
long by 50–60 (58) wide at base (n 510). Papillae on genital cone
not observed. Spicules subequal, alate, ending in simple, pointed
tips. Length of spicules 740–970 (865), representing 23.3–33%of
body length. Gubernaculum quadrangular, 20–50 (36) long and
15–30 (23) wide (Fig. 29).
Females (14 specimens, except otherwise stated): 3.08–5.10
(3.83) mm long and 80–120 (98) wide at mid-body. Cephalic
vesicle 55–70 (60) long and 25–35 (29) wide. Nerve ring, excretory
pore, and deirids situated at 125–160 (141) (n 55), 190–260 (231)
(n 57), and 200–270 (240) (n 54) from apex, respectively.
Esophagus 280–400 (325) long (n 510). Monodelphic. Vulva
situated at 65–70 from caudal extremity (n 57). Vagina vera 25–
35 (31) long (n 58), vestibule 55–90 (68) long (n 511), sphincter
40–50 (44) long and 35–55 (46) wide, infundibulum 60–120 (82) (n
511). Uterus 400–750 (560) long, taking up 9.8–20.5%(14.8%)of
body length, containing 7–24 (16) eggs. Eggs at 2–8 blastomeres
stage, 55–80 long and 30–45 wide. Tail 20 (n 55) long. Posterior
FIGURES 22–28. Stilestrongylus stilesi Freitas, Lent and Almeida, 1937. (22) Female, anterior extremity, right lateral view. (23) Female, head, apical
view. (24–28) Transverse sections of the body. (24) Female at esophageal level (220 mm from apex). (25) Female, at mid-body (53%of body length). (26)
Female at mid-length of uterus (400 mm from posterior end). (27) Male at mid-body (50%of body length). (28) Male at 150 mm anterior to caudal bursa.
Abbreviations: R, right; V, ventral.
998 THE JOURNAL OF PARASITOLOGY, VOL. 96, NO. 5, OCTOBER 2010
FIGURES 29–34. Stilestrongylus stilesi Freitas, Lent and Almeida, 1937. (29–31) Male, caudal bursa. (29) Entire bursa, ventral view. (30) Detail of left
lobe, ventral view (spicules omitted). (31) Detail of dorsal lobe, ventral view. (32–34) Female, posterior extremity in 3 different specimens. (32, 33) Right
lateral view. (34) Left lateral view, showing eggs within cuticular dilatation.
NOTARNICOLA ET AL.—REDESCRIPTION OF TWO NEMATODE SPECIES 999
extremity, from vestibular level, invaginated into a cuticular
dilatation, 155–310 (187) long. Seven of 20 females harbored 1–8
eggs within this cuticular dilatation (Figs. 32–34).
Taxonomic summary
Host: Seventeen H. chacarius Thomas (Rodentia, Cricetidae)
deposited at Coleccio´n Mamı
´feros Lillo (numbers CML 5810–
5826).
Material studied: Males and females deposited as CHMLP
numbers 5993, 5994, 5996–6006, 6008, 6009, and 6096; males and
females deposited at MNHN (numbers 592 MQ to 594 MQ).
Site of infection: Small intestine.
Locality: Ingenio San Martı
´n de Tabacal (23u169S, 64u159W),
lote Milagros, Departamento Ora´n, Salta, Argentina.
Prevalence and mean intensity: Seventeen hosts examined (100%
infected); 108 (4–826) worms per host.
Remarks
Freitas et al. (1937) based their description of S. stilesi, the
nominal species, on an unspecified number of males, plus 1 female
in the same work. The illustrations of the male (caudal bursa,
spicules, and gubernaculum) made by Freitas et al. (1937) are very
accurate, allowing confirmation of our specimens as S. stilesi. The
preservation of type material, available from CHIOC, precludes a
redescription of the species because some specimens are mounted
on slides and others preserved in ethanol are too fragile to permit
a description of the synlophe (M. C. Durette-Desset, pers.
comm.). The finding of voucher specimens parasitizing the same
host species, and probably from the same locality, permitted us to
make a complete description of S. stilesi.
Stilestrongylus was originally defined based mainly on the
characters of the caudal bursa, which is markedly asymmetrical
(Freitas et al., 1937). However, Durette-Desset (1971) redefined
the genus based on 5 species with known synlophe (Stilestrongy-
lus barusi Durette-Desset, 1970; S. dessetae Yoyotte-Vado, 1972;
S. freitasi Durette-Desset, 1968; S. inexpectatus Durette-Desset
and Tche´prakoff, 1969; and S. renaudae Durette-Desset, 1970)
and 4 species with unknown synlophe (S. stilesi,S. aculeata
[Travassos, 1918], S. eta [Travassos, 1937], and S. riberoi
[Travassos, 1937]). She established Stilestrongylus as having a
strongly asymmetrical caudal bursa, a hypertrophied genital
cone, and synlophe with more than 24 cuticular ridges that are
small and sub-equal, with axis of orientation of ridges from right
ventral to left dorsal quadrant. Since the synlophe observed in the
present specimens is coincident with the described characters, this
redescription also validates the redefinition of the genus by
Durette-Desset (1971).
In the material studied herein, some internal structures of the
anterior extremity are difficult to observe; in females, the caudal
structures are frequently hidden by the folds of the posterior
cuticular dilatation or the presence of eggs within it. The
inclination of the left axis of orientation differs between males
and females, but this should not be interpreted as a specific
character. The inclination of the axis on the left side is difficult to
evaluate, due to the opacity of the cuticle (orientation of ridges
unclear) and the frequent deformation of the cuticle on this side of
the body. Despite these minor constraints, the most important
characters can be observed and interpreted for both sexes. We
clarify in this work the asymmetry of the caudal bursa in having
the right lobe more developed than the left one, in contrast to the
affirmation by Freitas et al. (1937) where the left lobe is the most
developed.
DISCUSSION
Both species, L. patersoni and S. stilesi, are redescribed herein
with new morphological data. Currently, specimens of the
chacoan marsh rat distributed in the Yungas of Salta are referred
to H. chacarius Thomas, 1906 (Cirignoli et al., 2006). Mazza
(1928) misidentified the specimens from Salta, which he assigned
to H. vulpinus, a synonym of H. brasiliensis (Desmarest, 1819)
distributed in eastern Argentina (Pardin˜as and Galliari, 1998a,
1998b). However, Freitas at al. (1937) were correct in that the
hosts were H. balnearum, which is a subspecies of H. chacarius
(Cirignoli et al., 2006).
The site of infection for Litomosoides spp. is typically the
thoracic and/or abdominal cavity of the host. The present finding
of 1 male of L. patersoni in the intestine is unusual. However,
other authors have reported living filarioids in the intestine of
their host, i.e., Litomosa filaria (van Beneden) in bats (Desportes,
1946). Considering that this male worm was smaller than the
other collected in the body cavity, the intestine could be a
transitory organ in the migratory route.
Since the type specimens of L. patersoni have been lost, we
assigned the specimens from this survey (recovered from the type
locality and the type host species) as neotypes, according with the
Articles 75.3.4, 75.3.5, and 75.3.6 from the International Code of
Zoological Nomenclature (ICZN, 1999). For the heligmosomoid
S. stilesi, we validated and completed the description from Freitas
et al. (1937) and provided voucher specimens.
ACKNOWLEDGMENTS
We thank Dr. R. Barquez, curator of the Coleccio´n Mamı
´feros Lillo,
and Dr. M. M. Dı
´az, both from Tucuma´n, Argentina, who kindly made
the rodents available for parasitological examination; we also thank Dr.
M.C. Durette-Desset from MNHN, Paris, France, for helpful comments
on the manuscript, and Marı
´a Cristina Estivariz from CEPAVE for the
drawings. Funds came from Project N11/541 from SeCyT (UNLP,
Argentina). J. Notarnicola and M.C. Digiani are members of CONICET.
LITERATURE CITED
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2003. Examination of type material of two species of Litomosoides
(Filarioidea: Onchocercidae), parasites from bats; taxonomic conse-
quences. Parasite 210: 211–218.
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NOTARNICOLA ET AL.—REDESCRIPTION OF TWO NEMATODE SPECIES 1001
... In stark contrast with the importance of these filarioids as a model to understand basic aspects of parasitism and filarial disease in humans and animals, knowledge of their phylogeny and the study of their evolution has received only sporadic attention (Bain et al., 1989;Bain and Philipp, 1991;Brant and Gardner, 2000;Guerrero et al., 2006;Notarnicola et al., 2010aNotarnicola et al., , 2010bNotarnicola et al., , 2012. Both exhaustive taxon sampling and detailed accounts of the distribution of the parasites in their hosts are important because most tests of events of cospeciation require well-resolved phylogenies and an estimation of the level of host specificity or the host spectrum of the parasites (Light and Hafner, 2008;de Vienne et al., 2013). ...
... Both groups include species parasitizing bats, cricetid rodents, and marsupials. However, in the last 2 decades, several new species were described, and others were re-described or synonymized (Guerrero et al., 2002;Notarnicola et al., 2010aNotarnicola et al., , 2010bNotarnicola et al., , 2012Notarnicola and de la Sancha, 2015;Oviedo et al., 2016); thus, some of the Litomosoides species were re-assigned to either one or another group, and, as a result, some of them do not fit with the original definition of the ''carinii'' or ''sigmodontis'' groups. Examination of specimens deposited in helminthological collections as well as material obtained from our collecting efforts suggest there may be a third type of spicule, which may be typified by the structure present in Litomosoides hamletti Sandground, 1934. ...
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The genus Litomosoides Chandler, 1931, includes species that as adults occur in the thoracic and abdominal cavity of mammalian hosts and are presumably vectored by mites. The vertebrate hosts include a variety of Neotropical mammals such as phyllostomid and mormoopid bats; cricetid, sciurid, and hystricognath rodents; and didelphid marsupials. It has been suggested that Litomosoides is not a monophyletic group and that rampant horizontal transfer explains their presence in disparate groups of mammals. Herein we present a phylogenetic reconstruction including mitochondrial genes of 13 vouchered species. This phylogeny is used to reconstruct the evolutionary history of these parasites and the ancestral states of key characters used in species classification, namely, the configuration of the spicules. The historical association of these filarioids with 6 groups of mammals, as well as their ancestral geographic distributions, were reconstructed using Bayesian statistical approaches comparing alternative models of biogeography and evolution and fossil states in selected nodes of the phylogeny. The optimal reconstruction suggests a model of dispersal, extinction, and cladogenesis (DEC) driving the evolution of Litomosoides; the results suggest an origin of Litomosoides in South America and association of ancestors with phyllostomids, and strong evidence of at least 2 host-switching events: 1 of these involving cricetid rodents and the other mormoopid bats. The latter event included a simultaneous geographic expansion of the parasite lineage across South and North America. The host-switching event from phyllostomid bats into cricetid rodents occurred once these rodents diversified across South America; subsequent diversification of the latter clade resulted in 2 branches, each showing expansion of the parasites back into North America. This result suggests that both parasites and cricetid rodents established an association in South America, underwent diversification, and then dispersed into North America. Further, this clade of cricetid-dwelling species includes parasites featuring the "sigmodontis" spicule type. The identification of a single host-switching event involving the disparate lineages of Chiroptera and Rodentia offers a framework to reconstruct the gene evolution and diversification of this lineage after the host-switching event. This will help in predicting the ability of these parasites to infect sympatric mammals.
... Freitas, Lent and Almeida, 1937 Description. The morphological characters observed in the specimens mostly agree with the original description and subsequent redescription given by Notarnicola et al. (2010), i.e., synlophe with 29-31 subequal ridges; males with bursa dissymmetrical with right lobe larger, bursal pattern of type 2-3 on the right lobe and 2-2-1 on the left lobe, particular morphology of right ray 5 hypertrophied and with reinforced margins, genital cone characteristically curved and hypertrophied 137.8 × 58 ± 19.1 µm, spicules 740-970 µm long, and gubernaculum 37 ± 7 µm long and 23.3 ± 6.1 µm wide, females monodelphic, with vulva situated at 78.7 ± 16 µm from caudal extremity, tail 50.5 ± 12.3 µm long, and eggs 57.8 ± 8.5 µm long and 32.3 ± 3.5 µm wide. ...
... Stilestrongylus stilesi is the type species of the genus Stilestrongylus Freitas, Lent & Almeida 1937, and was originally described parasitizing Holochilus chacarius from the locality of San Martín de Tabacal, in the Orán Departament, Salta province, Argentina, and was redescribed by Notarnicola et al. (2010) on material from the same host species and locality. This is the first record of S. stilesi in Akodon azarae and Necromys lasiurus and for Humid Chaco ecoregion, enlarging the host and geographical range of the species. ...
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The aims of this paper were to list the helminths from sympatric rodent species (Muroidea, Cricetidae) in Corrientes city, Humid Chaco ecoregion, Argentina and summarise the record and ecological data on six host species. Fourteen species of helminths were found in 6 rodent assemblages. Five new hosts and 12 new geographical reports from Humid Chaco ecoregion are provided. The higher prevalence values corresponded to Stilestrongylus stilesi, Hassalstrongylus mazzai, H. argentinus and Mazzanema fortuita, and the higher mean abundance and mean intensity values corresponded to S. stilesi from Necromys lasiurus. Nippostrongylinae was the dominant group within each host species. The ecological descriptors of component communities are given. The highest value of richness index was observed for N. lasiurus (S = 6). The diversity index reached values between the range 1.11 in Holochilus chacarius and 0.16 in Akodon azarae. The equitability index shows the highest values for Oligoryzomys flavescens (0.96) and H. chacarius (0.81). The highest value index of dominance of Berger-Parker was observed for A. azarae (0.96) followed by N. lasiurus (0.86). This study contributes to the taxonomic and ecological of the parasite-host relationships, providing substantial information to one of the ecoregions most affected by anthropic actions in Argentina.
... There are numerous contributions in this country based on descriptions of helminths species poorly known in sigmodontine rodents and most of them correspond to nematodes (e.g. Sutton 1974Sutton , 1983Sutton , 1994Suriano & Navone 1992, 1994Notarnicola et al. 2000, Robles & Navone 2007b;2010;Notarnicola et al. 2010;Notarnicola & Navone 2011;Robles et al. 2008;Digiani et al. 2012;Notarnicola et al. 2012;Digiani & Kinsella 2014;Digiani et al. 2015;Robles et al. 2016). ...
... CAMB, RVSU and PPU Comments. The genus Stilestrongylus was defined by having a markedly asymmetrical caudal bursa, a hypertrophied genital cone and a synlophe with more than 24 cuticular ridges, small and subequal in size (Notarnicola et al. 2010). Among the 26 species of Stilestrongylus described to date, 25 have been described from Sigmodontinae rodents and 1from a spiny rat (Echimyidae) (Souza et al. 2009;Simões et al. 2014). ...
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Taxonomic and ecological aspects of the helminths found in the assemblage of sigmodontine rodents (Cricetidae-Muroidea) of the Atlantic Forest in Argentina are studied in this paper. The following species Akodon montensis, Brucepattersonius sp. and Thaptomys nigrita (Tribe Akodontini), as well as, Euryoryzomys russatus, Nectomys squamipes, Oligoryzomys nigripes, and Sooretamys angouya (Tribe Oryzomyini) are analyzed. A complete taxonomic list with a total of 25 species of helminths, including Digenea (Dicrocoeliidae), Cestoda (Hymenolepididae) and Nematoda (Trichuridae, Capillariidae, Cooperidae, Helligmonellidae, Oxyuridae, and Onchocercidae) is provided. Twenty new host and locality records for Misiones, Argentina, are reported and the results of the ecological descriptors of component communities are given. The highest value of richness was observed for A. montensis (S=8) and E. russatus (S=7). The diversity index (H´) reached values between 1.03 and 1.39 in all rodents, with the exception of N. squamipes that reached 0.75. The equitability indeces with highest value were observed for T. nigrita and E. russatus. The Berger-Parker index of dominance was similar for all host species. The highest prevalence, mean abundance and mean intensity values corresponded to Nippostrongylinae, followed by Syphacinii. This survey constitutes the report with the most diverse parasitic assemblage of rodents described for the Atlantic Forest ecoregion and for Argentina.
... Host: Peromyscus yucatanicus Locality: Paraíso Prevalence and mean intensity (range): 20% (1/5) and 1 (1) Specimens deposited: MLP-He 7439 Comments: Infected mouse harbored one non-gravid female specimen. The characteristics of the synlophe (24 small and subequal ridges with oblique axis of orientation), and morphology of the posterior end (monodelphic, with invaginated tail) evoke clearly the females of the genus Stilestrongylus (Notarnicola et al. 2010). However, more material, particularly males, should be collected to identify this taxon at species level. ...
Article
In this survey, 19 species of helminths including Cestoda (Davaineidae, Hymenolepididae, and Taeniidae), Acanthocephala (Oligacanthorhynchidae), and Nematoda (Trichuridae, Ornithostrongylidae, Heligmonellidae, Oxyuridae, and Gongylonematidae) from Rattus rattus, Mus musculus, Sigmodon toltecus, Heteromys gaumeri, and Peromyscus yucatanicus in two Mayan villages in Yucatán, México, were recorded. Ten species of helminths were collected in both localities. The highest species richness was recorded in R. rattus from Xkalakdzonot (6 taxa). Twelve species are new records for Yucatán and two are registered for the first time in México. This survey constitutes the first checklist of helminth parasites in small rodents in the south-southeast of México.
... Stilestrongylus azarai was present in the three habitats, with low values of prevalence (25-32.1%) and mean abundance (2.1-29.2) compared with another study carried out in a natural environment (95% and 81.6, respectively, in A. azarae from marshlands; Navone et al., 2009), and with other species of Stilestrongylus (100% and more than 69.4 for S. flavescens (Navone et al., 2009); 100% for S. stilesi (Notarnicola et al., 2010)). In the present study, both abundance and infection prevalence were higher on the poultry farms than in the other two habitats, and they were associated with A. azarae females on farms during the season of high abundance of rodents. ...
Article
In the Pampa region of Argentina, farming activities have been performed since the beginning of the 20th century, but in the 1990s, land-use patterns rapidly changed towards intensive agriculture and poultry breeding. This study compares the helminth community of Akodon azarae (Rodentia) among three habitats with different land use in pampean agroecosystems: poultry farms, mono-cultivated fields and abandoned fields (not used for 35 years), under the prediction that there will be greater helminth richness and diversity in mice from abandoned fields compared to those from the other habitats. Nevertheless, the highest abundance of A. azarae occurred on poultry farms, the habitat most disturbed by human activity, while cultivated fields showed the lowest. Helminth richness and diversity were significantly higher on poultry farms than in the other habitats, due to the presence of Trichuris laevitestis , Protospirura numidica criceticola and cysts of Taenia taeniaeformis . We suggest that the helminth fauna of A. azarae can survive on poultry farms despite disturbance from farming activities, because rodents can move and get shelter within farm perimeter fences, where dense and high vegetation grows. This farm area could offer good conditions for geohelminth development, while chicken sheds could attract insects that are intermediate hosts of helminths with indirect life cycles. On the contrary, agrochemicals applied in cultivated fields would negatively influence helminth diversity and composition, by decreasing host populations (arthropods and rodents) and affecting free larval stages of geohelminths.
... The range in Argentina includes a narrow band in the provinces of Jujuy, Salta, Santiago del Estero, and Tucuman, and a second, wider region in the Humid Chaco from south Formosa province to northeastern Buenos Aires (D'Elía and Pardiñas, 2015). Different species of nematodes have been recorded in H. chacarius from different provinces in Argentina (Salta, Chaco and Formosa) (Notarnicola, 2005;Notarnicola et al., 2010;Digiani et al., 2013Digiani et al., , 2015. Nevertheless, any survey of Trichuris species has been recorded in this host species. ...
Article
A new Trichuris species isolated from Holochilus chacarius (Cricetidae: Sigmodontinae) from the Chaco ecoregion in Argentina is described based on morphological characteristics and mitochondrial (cox1, cob) and nuclear (ITS2) markers. The new species is distinguished from 27 species of Trichuris from North and South American rodents based on morphological and biometrical features, such as the absence of a spicular tube, presence of a cylindrical spicular sheath, non-protrusive vulva, length of spicule, and proximal and distal cloacal tube. In addition, the results based on three molecular markers of the new species and three Trichuris species previously analysed from sigmodontine rodents: Trichuris pardinasi, Trichuris navonae and Trichuris bainae confirmed that the specimens here studied belong to a different species. Molecular data are further used to discuss the phylogenetic relationships among the Trichuris species of rodents from Argentina. The combined analysis of mitochondrial genes (cox1 and cob) revealed four clades corresponding with four different species of Trichuris. T. navonae (Akodontini rodents) and T. massoiai n. sp. as a sister group related to T. bainae (Oryzomyini rodents) and separated of T. pardinasi (Phyllotini rodents).
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Filaria lorenzo n. sp. is described in the Lesser Grison, Galictis cuja from northern Patagonia, Argentina. The new species can be differentiated from the eight species of Filaria from the Old World by the shape of the sclerotized preesophageal ring. The four remaining species of the genus parasitize American Mephitidae and/or Mustelidae. Filaria carvalhoi from Brazil and F. texensis from USA lack a preesophageal ring, whereas F. taxideae from USA and F. conepati from Argentina share with our specimens a preesophageal ring mostly mushroom shaped. Our specimens differ from F. taxideae by lacking lateral alae, by a different ornamentation of the female tail and by the male lacking adcloacal papillae. The new species also differs from F. conepati by the shape of the preesophageal ring and by the shape of the eggs. The indirect examination of the types of F. conepati and F. carvalhoi, corroborated the existence of differences between these two species, allowing us to refute their synonymy, as proposed by some authors. Our results extend the taxonomy of Filaria to 13 species and comprise the first report of a filarioid nematode for an Argentinean mustelid, and the first report for Patagonia.
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Two species of Hassalstrongylus Durette-Desset, 1971 coparasitic in Holochilus chacarius Thomas (Rodentia, Cricetidae), not recorded since their original description in 1937, were newly found in their type host and locality. Hassalstrongylus mazzai (Freitas, Lent and Almeida, 1937) and Hassalstrongylus argentinus (Freitas, Lent and Almeida, 1937) were obtained from Holochilus chacarius from two different populations: one from Salta Province (northwest Argentina) and another from Chaco Province (northeast Argentina). The species described as Heligmonoides mazzai Freitas, Lent and Almeida, 1937 had been transferred to Hassalstrongylus even though its synlophe had never been studied. We provide the first descriptions and illustrations of the synlophe of males and females of H. mazzai and the female of H. argentinus, and account for morphological and metrical variability. We confirm, through the study of the synlophe, the placement of H. mazzai in the genus Hassalstrongylus, and designate neotypes for the species since the type material deposited by the authors could not be found. Females of both species were morphologically very similar and a Principal Components Analysis performed on some morphometrical characters showed that the body length, uterus length, and an unexpected character as the eggs number were useful characters in the discrimination of both species.
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Paraguay is a small landlocked country whose mammalian fauna is among the least studied in South America, as well as their parasites. As a result of a study of the effects of habitat fragmentation on small mammal biodiversity in eastern Paraguay, we have collected some parasites of cricetid rodents. Herein, we describe a new species of Litomosoides Chandler, 1931 parasitising the body cavity of the tuft-toed rice rat Sooretamys angouya (Fischer) and Litomosoides esslingeri Bain, Petit & Diagne, 1989 parasitising Oligoryzomys nigripes (Olfers), thus expanding its geographical distribution into Paraguay. Litomosoides ysoguazu n. sp. is characterised by the large size of the females (92.2–117.6 mm long) and by having buccal capsule with an anterior widening with rounded edges on the chitinous segment and a rounded widening at the base; male tail with a single pair of adcloacal papillae, three to five pairs of asymmetrical postcloacal papillae, and one or two unpaired papillae in the median ventral line; spicules corresponding to the ‘‘sigmodontis’’ species group; and microfilaria with a sheath stuck to the body and visible in the anterior extremity. We also describe a fourth-stage female larva. Oligoryzomys nigripes is a new host record of L. esslingeri; this enlarges the host record to eight species highlighting the low specificity of this species.
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A catalogue of type specimens of the Helminthological Collection of the División Zoología Invertebrados, of Museo de La Plata (FCNyM-UNLP), Argentina, is presented. It includes Platyhelmithes, Nematoda, Nematomorpha and Acan-thocephala. The collection comprises type lots for 217 species: 90 nematodes, 50 digeneans, 28 Nematomorpha, 19 mono-geneans, 17 turbellarians, 8 cestodes and 5 acanthocephalans. Specific names are listed systematically, followed by type host, type locality, specimens, collection number and bibliographic reference.