The Life Cycle of Pseudosellacotyla lutzi (Digenea: Cryptogonimidae), in
Aylacostoma chloroticum (Prosobranchia: Thiaridae), and Hoplias malabaricus
(Characiformes: Erythrinidae), in Argentina
Author(s): Manuel G. Quintana and Margarita Ostrowski de Núñez
Source: Journal of Parasitology, 100(6):805-811.
Published By: American Society of Parasitologists
DOI: http://dx.doi.org/10.1645/13-379.1
URL: http://www.bioone.org/doi/full/10.1645/13-379.1
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J. Parasitol., 100(6), 2014, pp. 805–811
Ó American Society of Parasitologists 2014
THE LIFE CYCLE OF PSEUDOSELLACOTYLA LUTZI (DIGENEA: CRYPTOGONIMIDAE), IN
AYLACOSTOMA CHLOROTICUM (PROSOBRANCHIA: THIARIDAE), AND HOPLIAS
MALABARICUS (CHARACIFORMES: ERYTHRINIDAE), IN ARGENTINA
Manuel G. Quintana and Margarita Ostrowski de Núñez*
Museo Argentino de Ciencias Naturales ‘‘Bernardino Rivadavia’’, Av. Angel Gallardo 470, C1405 DJR, Buenos Aires, Argentina. Correspondence should be
sent to: ostrowskimargarita@gmail.com
ABSTRACT:
Pseudosellacotyla lutzi (Freitas, 1941), at present included in the Faustulidae, is redescribed, and its life cycle was
resolved experimentally. The prosobranch snail Aylacostoma chloroticum Hylton Scott (Thiaridae), collected in the Yacyretá Dam,
Province of Misiones, Argentina, was found naturally infected with cercariae that lacked pigmented eyespots, and possessed 7 pairs
of penetration glands, 8 pairs of flame cells, and a V-shaped excretory vesicle. The cercariae developed in oval cysts, which were
found on fin rays, vertebrae, and spines of poeciliid and tetragonopterid fish species. Adults were obtained experimentally from
Hoplias malabaricus (Erythrinidae) infected with metacercariae from albino Gymnocorymbus ternetzi (Tetragonopteridae), which
had been exposed to emerging cercariae. Adults were also found in naturally infected H. malabaricus collected in the Yacyretá
Dam. The morphology of the cercariae, and the characteristics of the life cycle show that P. lutzi should be included in the
Cryptogonimidae.
MATERIALS AND METHODS
Snails of the genus Aylacostoma Spix, 1827 (Prosobranchia,
Thiaridae) are distributed in freshwater habitats of tropical and
subtropical areas of Central and South America. At their
southernmost distributional limit in Brazil, Paraguay, and
Argentina, they occur exclusively in the Paraná River and a
few major tributaries (von Ihering, 1902, 1909; Hylton Scott,
1953, 1954; Quintana and Mercado Laczkó, 1997; Simone,
2006).
Aylacostoma chloroticum Hylton Scott, 1954 is the only species
of the genus in Paraguay and Argentina surviving in the wild after
the construction of the Yacyretá hydroelectric power plant.
However, it is now seriously threatened by the alteration of its
original habitat, the rapids of the Paraná River.
During a parasite survey of the last 2 remaining relictual
populations at the upstream section of the reservoir, we observed
6 different cercariae emerging from the snails, of which 4 were
opisthorchioid-like, and 2 belong to the Echinostomatoidea.
Recently, the life cycle of 1 of these, Stephanoprora aylacostoma
Ostrowski de Núñez et Quintana, 2008, has been elucidated
(Ostrowski de Núñez and Quintana, 2008).
In the present article we describe the life cycle of Pseudosellacotyla lutzi (Freitas, 1941), which proved to be the adult of 1 of
the ‘‘opisthorchioid’’ like cercariae. This species has been
included in different families along its history. It was originally
included in the Nanophyetidae, Dollfus, 1939 by Freitas (1941),
considered to have affinities to the Heterophyidae, in the
Heterophyidae by Yamaguti (1953), in the Microphallidae by
Yamaguti (1958), in the Fellodistomidae (Baccigerinae) by
Yamaguti (1971), and finally, in the Faustulidae by Bray
(2008). Pseudosellacotyla lutzi was reported several times from
Brazil and Colombia, always from the same fish host, Hoplias
malabaricus (Bloch, 1794), by Kohn et al. (1985), Kohn and
Fernandes (1987), Kohn et al. (2011), and Lenis Velez et al.
(2010). We include P. lutzi in Cryptogonimidae, based on its
morphological characteristics and the pattern of its life history.
Specimens of A. chloroticum up to 37 mm in total shell length (TSL)
were collected by hand by scuba diving in flooded areas of the Paraná
River. Sampling dates and locations were as follows: September 2008 in
the Heller Peninsula (27820 0 S, 55855 0 W) near Posadas City, and January
2010 in the Heller Peninsula and Candelaria, (27827 0 S, 55845 0 W), Province
of Misiones. Snails were kept individually in vials with 50 ml of tap water
and examined daily for the emergence of cercariae. Some snails were
dissected to check for intramolluscan stages. Laboratory-raised Poecilia
reticulata Peters, 1859, Cnesterodon decemmaculatus (Jenyns, 1842), and
albino Gymnocorymbus ternetzi (Boulenger, 1895) were exposed to
emerging cercariae. After identifying the infection site and morphology
of the metacercariae, fishes belonging to the Tetragonopteridae, Moenckhausia dichroura (Kner, 1858), and Hyphessobrycon eques (Steindachner,
1882) were sampled at different sites along the dam to identify the natural
second intermediate host. These fish were not used in experimental
infections.
Two albino G. ternetzi with cysts aged 20 days or older were offered alive
or in pieces to individual presumptive definitive fish hosts every other day
for 15 days; fishes used were 4 Pimelodus maculatus Lacepède, 1803, 2
Pimelodus albicans (Valenciennes, 1840), 4 Callichthys callichthys (Linnaeus,
1758), 4 Oxydoras eigenmanni Boulenger, 1895, 1 Luciopimelodus pati
(Valenciennes, 1836), 6 Crenicichla lepidota Heckel, 1840, 10 Crenicichla
vittata Heckel, 1840, 8 Oligosarcus jenynsii (Günther, 1864) and 17 juvenile
(ca. 12 cm standard length, SL) H. malabaricus (9 exposed, 8 controls). They
were obtained from local dealers, held in aerated aquaria and starved for
several days prior to the experiments, to ensure that they would eat infected
intermediate hosts. Following cold narcosis, fishes were killed and dissected
at different times from day 2 postexposure (PE) onward; their feces were
examined for parasite eggs from day 15 PE onward.
In an attempt to determine the natural definitive hosts, piscivorous
fishes common in the area were captured and examined; to this aim, the
following fishes were collected from Candelaria in November 2012,
January and March 2013: 4 H. malabaricus, 21 C. vittata, 2 Gymnogeophagus balzanii (Perugia, 1891), 42 Acestrorhynchus pantaneiro (Menezes,
1992), 3 Serrasalmus maculatus (Kner, 1858), 6 Galeocharax humeralis
(Valenciennes, 1834), 1 Gymnotus inaequilabiatus (Valenciennes, 1839), 4
Roeboides sp., 18 Astyanax sp., and 22 M. dichroura.
Rediae, cercariae, and metacercariae were studied alive or fixed in
nearly boiling 4% formalin, cleared in lactophenol, and then mounted in
glycerine jelly or formalin without applying pressure for measurements.
Metacercariae were mechanically freed from cysts. Adults and some
metacercariae freed from cysts were fixed in 4% formalin, stained with
Semichon’s carmine or hematoxylin, and sometimes counterstained with
light green or eosin, respectively. Then, the specimens were dehydrated in
an ethanol series, cleared in creosote, and mounted in Canada balsam. For
histological studies, pieces of pyloric ceca containing 1–4 parasites were
embedded in paraffin wax, cut at 3 lm, and stained with Harris
hematoxylin and eosin. Photographs were taken with an Olympus DP10 digital camera (Olympus, Tokyo, Japan), drawings were made with a
Received 21 August 2013; revised 14 June 2014; accepted 16 June 2014.
* Departamento de Biodiversidad y Biologı́a Experimental, Facultad
de Ciencias Exactas y Naturales, Universidad de Buenos Aires,
Ciudad Universitaria, Pabellón II, 1428 Buenos Aires, Argentina.
DOI: 10.1645/13-379.1
805
806
THE JOURNAL OF PARASITOLOGY, VOL. 100, NO. 6, DECEMBER 2014
drawing tube attached to an Olympus BH2-NIC microscope (Olympus),
and details were added freehand.
Some naturally infected snails and experimentally obtained adults were
fixed in 96% ethanol for later possible molecular analysis. All
measurements are given in micrometers, with the range followed by the
mean and number (n) of specimens measured in parentheses. Specimens
were deposited in the Parasitological Collection of the Museo Argentino
de Ciencias Naturales ‘‘Bernardino Rivadavia,’’ Buenos Aires, Argentina
(MACN-PA).
REDESCRIPTION
Pseudosellacotyla lutzi (Freitas, 1941) Yamaguti, 1953
(Figs. 1–17)
Adult (Figs. 1–4, 15–17): Based on 90 mounted and several living
specimens 13, 20, 48, and 54 days PE, and on 20 specimens obtained from
natural infections. Measurements based on egg-bearing specimens 20 days
PE in text and on other specimens in Table I. Body squat to oval, slightly
longer than wide, 302–447 (395; n ¼ 21) 3 233–340 (307; n ¼ 20) at level of
testes; width/length ratio 1:1.1–1.5 (1.3; n ¼ 20), with rounded posterior
extremity. Forebody c. 41% of body length. Body spines of same length,
8–10 long, extend to posterior extremity, except around excretory pore.
Oral sucker subterminal, 43–64 (54) 3 53–80 (66; n ¼ 21), without crown of
spines. Ventral sucker in middle of body, smaller than oral sucker, 24–48
(38) 3 29–54 (42; n ¼ 17), embedded in tegument; ventral sucker to oral
sucker width ratio 1:1.2–2.0 (1.6; n ¼ 17). Prepharynx short, generally
indistinguishable, sometimes up to 14 (3; n ¼ 21) long; pharynx well
developed, 30–56 (43) 3 32–48 (43; n ¼ 19); esophagus short, 0–24 (13; n ¼
18), bifurcates short distance anterior to ventral sucker in 2 wide, short
blind ceca, reaching level of ventral sucker.
Testes 2, oval to spherical, nearly equal in size, symmetrical, in
posterior half of body, left testis 109–152 (124) 3 77–112 (89; n ¼ 17); right
testis 96–149 (125) 3 72–117 (91; n ¼ 17). Vasa efferentia fuse to form
tubulosaccular seminal vesicle, occupying intertesticular space in immature specimens (Fig. 2); subsequently its proximal end develops into larger
saccular vesicle, sometimes appearing bipartite, lying posterolaterally or
posteromedially to ventral sucker. Pars prostatica and hermaphroditic
duct very short, discernible only in histological sections and in living
pressed specimens (Fig. 3). Genital pore medial, immediately anterior to
ventral sucker. Gonotyl and ventrogenital sac absent.
Ovary oval or irregular in shape, 43–91 (73) 3 40–88 (57; n ¼ 16),
compact, between testes, near right testis (38 %), left testis (53 %), or
middle line (9 %) (n ¼ 78) and near ventral sucker, sometimes
overlapping. Canalicular seminal receptacle large, posterior to ovary.
Laurer’s canal present, opening dorsally near posterior end of body (Fig.
4). Vitelline follicles oval to spherical, 14–48 (27) 3 16–51 (30; n ¼ 52)
arranged in single group on each side of body at level of pharynx,
extending to anterior level of testis. Uterus forms loops filling posterior
half of body, with distal end opening into hermaphroditic duct. Eggs
small, numerous, 32–40 (36) 3 14–21 (18; n ¼ 67), contain developed
miracidium (Fig. 17). Excretory vesicle V-shaped, arms reach to
posterior border of testes.
Metacercariae (Figs. 5, 12, 13, 14): Cysts (n ¼ 28): 129–176 (157) 3
107–164 (137), in fin rays, vertebrae, and spines. Freed metacercariae
similar in morphology to adult, except for development of vitelline follicles
and absence of eggs. Body (n ¼ 3) 196 (144–256) 3 127 (109–160),
tegumental spines conspicuous, oral sucker 35 (29–45) 3 40 (35–45),
pharynx 32 3 32, ventral sucker 27 3 29 (26–32), short ceca, and testes
symmetrical, at level of excretory vesicle.
Cercariae (Figs. 6, 7, 10, 11): Body small, pigmented (n ¼ 20) 198 (183–
214) 3 61 (57–69), covered by tegumental spines on dorsal and ventral
surface and fine sensory hairs; oral sucker 29 (26–32) 3 26 (22–29), 7 pairs
of finely grained penetration glands, their ducts running forward to open
into 4 sets of 3–4–4–3 pores at anterior extremity. Pigmented eyespots
absent. Small pharynx 10 in diameter; esophagus and 2 short ceca
observed in 1 pressed living specimen. Ventral sucker consisting of
conspicuous cluster of cells. Presence of genital anlagen represented by
small group of cells posterior to ventral sucker. Excretory vesicle Vshaped. Flame cells probably 4 groups of 2 flame cells each. Tail 322 (296–
340) 3 28 (25–38), with dorsoventral finfold (Fig. 11); inconspicuous short
excretory canal sometimes observed in proximal 1/8; bifurcation or
excretory pores not detected. Swimming behavior and resting position in
water similar to those of other opisthorchioid species.
Rediae (Figs. 8, 9): Occur as tangled masses, making it difficult to
separate individual rediae. Rediae have elongate, slender yellow-brownish
pigmented bodies of variable width (n ¼ 20) 426 (284–554) 3 52 (32–107),
depending on development of germinal masses; pharynx small 24 (22–29)
3 22 (19–26); cecum short 70–122 (90), reaching 14–35% (24%) of body
length. Rediae may contain 1–2 fully developed cercariae and numerous
developing germ balls. Old rediae with bodies of variable width and
several constrictions. Small living rediae (Fig. 9) with elongate body
tapering at posterior end, without developing germ balls, 95–150 (128; n ¼
10) 3 28–47 (36), pharynx 17–37 (27; n ¼ 10) 3 19–25 (22), with relatively
longer cecum, reaching 50–75% of body length. Mother redia and
sporocyst not detected.
Taxonomic summary
Type host and experimental definitive host: Hoplias malabaricus (Bloch,
1794) (Characiformes, Erythrinidae).
Site of infection: Intestine and pyloric ceca.
Prevalence: Two of 4 H. malabaricus (November 2012 and March
2013).
Intensity: Fourteen and 12, respectively.
First intermediate host: Aylacostoma chloroticum Hylton Scott, 1954
(Thiaridae).
Prevalence: Forty-eight of 444 examined.
Second intermediate host: Moenckhausia dichroura (Kner, 1858), H.
eques (Steindachner, 1882) (Tetragonopteridae) (natural); P. reticulata
Peters, 1859, C. decemmaculatus (Jenyns, 1842), (Poecilidae), albino G.
ternetzi (Boulenger, 1895) (Tetragonopteridae) (experimental).
Locality: Yacyretá Dam [Heller Peninsula (27820 0 S, 55855 0 W); Candelaria, (27827 0 S, 55845 0 W)], Paraná River, Province of Misiones, Argentina.
Deposition of specimens: MACN-PA 565/1: metacercariae; 565/2–5:
adults 13 days PE; MACN-PA 565/6–9: adults 20 days PE; MACN-PA
565/10–12: adults 48 days PE, MACN-PA 565/13: adults 54 days PE;
MACN-PA 565/14–15: adults from natural infection.
Remarks
Forty-eight of 444 snails examined were found infected with cercariae
of P. lutzi, and none of them showed dual or multiple infections with other
digeneans. Sporocysts and mother rediae were absent, probably because of
the age of infection. All laboratory-raised fish species exposed to cercariae
became infected, with the longest survival of metacercariae being recorded
for albino G. ternetzi individuals (up to 270 days PE, at the end of the
experiments).
None of the fish species used as presumptive definitive hosts became
infected with P. lutzi after ingestion of metacercariae, except for the 9
exposed juvenile H. malabaricus; the remaining 8 used as controls were
negative. As fish were obtained from local dealers, captured in localities
far away from Yacyretá Dam, all of them were infected with at least 1 of
the following parasites: cestodes and metacestodes, larvae of acanthocephalans, nematodes, digenean metacercariae, and digenean species
different from P. lutzi.
In the 9 exposed H. malabaricus, parasites were located in the
proximal part of the intestine in 4 cases, of which 1 had 12 immature
specimens at day 2 PE, and 3 had 15, 70, and 80 ovigerous specimens at
days 11, 12, and 13 PE, respectively. In the other 4 cases, parasites were
located exclusively in the pyloric ceca, which contained more than 100,
10, 70, and 20 specimens at days 20, 22, 48, and 54 PE, respectively. It is
interesting to note that specimens were located in the intestine lumen of
H. malabaricus juveniles before 13 days PE but in their pyloric ceca
afterwards. Finally, 1 of the fish was kept alive in order to obtain
parasite eggs, but only dead specimens without eggs could be recovered
from its feces. When dissected on day 41 PE, the pyloric ceca and body
cavity appeared to be heavily infected with larvae of cestodes and
acanthocephalans, and a single specimen of P. lutzi filled with eggs was
found in a pyloric cecum. This heavy infection with cestodes and
acanthocephalans may account for the slight experimental infection by
P. lutzi. Among the fishes collected from Candelaria, only 2 of the 4 H.
malabaricus were parasitized with P. lutzi; these fish measured 200 and
234 mm SL and harbored 12 and 14 gravid specimens, respectively, in
their pyloric ceca.
QUINTANA AND OSTROWSKI DE NÚÑEZ—LIFE CYCLE OF PSEUDOSELLACOTYLA LUTZI
807
FIGURES 1–8. Pseudosellacotyla lutzi (Freitas, 1941): (1) Adult experimentally from Hoplias malabaricus 20 days postexposure (PE) (most eggs in
central body area omitted). (2) Adult 13 days PE (without eggs), showing position of seminal vesicle. (3) Terminal genitalia. (4) Female genitalia (Figs. 3
and 4 reconstructed from living specimens). (5) Excysted metacercaria. (6) Cercaria, body with tail. (7) Body of cercaria, dark triangles: observed flame
cells, open triangle: suspected position of missing flame cell. (8) Redia, fully developed, with 2 mature cercariae. Scale bars ¼ 100 lm.
808
THE JOURNAL OF PARASITOLOGY, VOL. 100, NO. 6, DECEMBER 2014
FIGURES 9–17. Pseudosellacotyla lutzi (Freitas, 1941): (9) Young redia. (10) Cercaria body. (11) Cercaria tail. (12) Metacercaria encysted on
vertebrae (dark arrow). (13) Metacercaria encysted on spines. (14) Metacercaria freed from cyst. (15) Adult experimentally from H. malabaricus, 13 days
postexposure, ventral view; vs: embedded ventral sucker. (16) Tegument of adult specimen. (17) Eggs. Scale bars ¼ 25 lm (Figs. 16, 17); 50 lm (Figs. 9,
10); 100 lm (Figs. 11, 14, 15); 200 lm (Fig. 13); 250 lm (Fig. 12). Figs. 9–14, 16–17 from living specimens, Fig. 15 from specimen mounted in glycerine
jelly.
QUINTANA AND OSTROWSKI DE NÚÑEZ—LIFE CYCLE OF PSEUDOSELLACOTYLA LUTZI
809
TABLE I. Pseudosellacotyla lutzi (Freitas, 1941). Values are shown in micrometer as min-max with the mean and number of specimens measured in
parentheses. L: length, W: width, os: oral sucker, vs: ventral sucker.
Measurements (lm)
Body L
Body W (testes level)
Forebody
% forebody/L
Oral sucker L
Oral sucker W
Prepharynx
Pharynx L
Pharynx W
Ventral sucker L
Ventral sucker W
Ovary L
Ovary W
Left testis L
Left testis W
Right testis L
Right testis W
Vitelline follicles L
Vitelline follicles W
Egg L
Egg W
vs:os width ratio
Body L/body W
13 days PE
163–278
128–224
64–122
37–45
24–48
38–59
0–16
27–42
21–35
22–37
22–38
32–64
19–40
48–104
35–72
61–104
46–66
16–32
10–19
29–40
14–21
0.5–0.9
1.2–1.5
(244, 16)
(191, 16)
(102, 14)
(41, 14)
(38, 15)
(49, 15)
(4, 15)
(34, 12)
(29, 12)
(30, 13)
(32, 13)
(43, 12)
(33, 11)
(73, 12)
(57, 12)
(76, 12)
(58, 12)
(20, 19)
(16, 19)
(33, 29)
(17, 29)
(0.7, 13)
(1.3, 16)
48–54 days PE
265–410
183–315
96–160
33–46
42–64
50–72
0–21
32–51
29–48
32–48
30–43
48–72
29–64
72–112
56–88
80–112
48–88
13–32
10–35
32–37
14–21
0.5–0.8
1.1–1.5
(330, 33)
(266, 33)
(131, 28)
(40, 27)
(51, 28)
(60, 28)
(6, 21)
(45, 25)
(37, 25)
(36, 26)
(36, 25)
(57, 13)
(44, 13)
(93, 12)
(75, 12)
(96, 12)
(74, 11)
(21, 51)
(20, 51)
(34, 52)
(17, 52)
(0.6, 25)
(1.2, 32)
Natural infection
372–466
271–384
128–192
33–46
48–64
64–80
0–16
32–48
38–51
27–48
27–48
56–96
37–72
96–144
83–128
112–136
83–120
16–48
19–42
32–38
16–21
0.4–0.7
1.1–1.4
(407, 15)
(320, 15)
(158, 12)
(38, 12)
(56, 14)
(71, 14)
(9, 14)
(39, 14)
(45, 14)
(39, 9)
(40, 9)
(79, 12)
(50, 12)
(123, 14)
(99, 14)
(120, 14)
(100, 14)
(29, 42)
(27, 42)
(36, 46)
(18, 46)
(0.6, 9)
(1.3, 15)
Freitas (1941)
Kohn et al. (1985)
340–590
240–444
510–650
370–480
50–59
59–63
75–89
75–99
46–50
34–42
38–42*
50–60
50–60
47–52
47–52
67–120
70–94
90–210†
70–140
42–105
42–80
67–105†
50–63
34–38
17
33–38
16–19
1:530–650
* Diameter.
† Include both testes.
Body shape, body spination, and the position of gonads were identical
in experimental metacercariae, adults from experimental infections, and
adults from naturally infected H. malabaricus.
The fact that Hyphessobrycon eques (from Heller Peninsula) and M.
dichroura (from Candelaria) were parasitized with mature metacercariae
that had been identified with those of P. lutzi from experimental infections
for comparison strongly indicates that both fish species serve as second
intermediate hosts of this parasite in the Paraná River.
Adults at 13 days PE were smaller, 163–278 (244) 3 128–224 (191, n ¼
16) produced fewer eggs and had a more prominent seminal vesicle than
those at 20 days PE. After 48 days PE, specimens were larger than those at
13 days PE, 265–410 (330) 3 183–315 (266, n ¼ 33) (Table I), but smaller
than those at 20 days PE, 302–447 (395) 3 233–340 (307, n ¼ 20). The latter
were filled with eggs obscuring the internal organs, except for the
conspicuous seminal vesicle. The specimens from natural infections, 372–
466 (407) 3 271–384 (320, n ¼ 15), were larger than those from
experimental infections (Table I).
DISCUSSION
This is the second report of Aylacostoma chloroticum infected
with larval stages belonging to a digenean species whose life cycle
was experimentally established. The experimentally and naturally
obtained adults are morphologically indistinguishable from P.
lutzi, and were considered identical to this species, included in the
Faustulidae by Bray (2008).
The family Faustulidae is a member of the superfamily
Microphalloidea, which consists of 18 families, from which 8
are known to present xiphidiocercariae (Microphallidae, Prosthogonimidae, Lecithodendriidae, Leyogonimidae, Phaneropsolidae, Stomylotrematidae, Zoogonidae), 2 presumably present
xiphidiocercariae as they are parasites of bats (Anenterotrematidae) or have odonates as second intermediate hosts (Eumegacetidae), from 6 the life cycle is not known (Diplangidae,
Exotidendriidae, Gyrapsidae, Pachypsolidae, Renschetrematidae,
Taiwantrematidae) (Bray, 2008), 1 presents at least some species
with xiphidiocercariae (Renicolidae), and the remaining 1
gymnocephalous cercariae (Faustulidae).
Bray (2008) recorded 14 genera in the Faustulidae, of which 2
(Pseudobacciger Nahhas and Cable, 1954 represented by 3 marine
species and Pseudosellacotyla, represented by a single freshwater
species) lack a cirrus sac, present in the others. In the life cycle of
Pseudobacciger harengulae a marine clam acts as first, and
crustaceans as second, intermediate host. The cercaria is of the
trichocercous type, which emerged from sporocysts; definitive
hosts are different marine fish (Kim and Chun, 1984; Dimitrov et
al., 1999). On the other hand, the life cycle of Pseudosellacotyla
lutzi presents cercariae of the ‘‘opisthorchioid’’ type, which
originate in rediae, and emerge from a gastropod of the
superfamily Cerithioidea, as do most of the opisthorchioid species
(Cribb et al., 2001). Pseudosellacotyla lutzi has a V-shaped
excretory vesicle with short arms, not reaching the testes,
although in Faustulidae the arms reach into the forebody, but
both share the overall position of organs, and the opening of the
Laurer’s canal near the posterior extremity. These characteristics
are also seen in heterophyids, and some cryptogonimids, as in
Acanthostomum brauni Mañe Garzon and Gil, 1961, where the
Laurer’s canal opens at the level of the anterior testis (Ostrowski
de Núñez, 1987), and probably in other species of Acanthostomum
Looss, 1899, where genitalia lie in the posterior extremity of the
body. On the other hand, P. lutzi possesses an embedded ventral
sucker, a characteristic of Cryptogonimidae, Heterophyidae, and
some Opisthorchiidae, absent in Faustulidae. Yamaguti (1953)
considered probable from the figures of Freitas (1941) ‘‘that the
acetabulum is embedded in the body parenchyma, and the genital
810
THE JOURNAL OF PARASITOLOGY, VOL. 100, NO. 6, DECEMBER 2014
pore opens to the outside over the acetabulum,’’ and if this
assumption be justified, ‘‘there would be no question to include
Pseudosellacotyla in the Heterophyidae.’’ In the living pressed
specimens, in whole mounts, and in histological sections no
ventrogenital sac could be detected; therefore the inclusion in
Heterophyidae as proposed by Yamaguti (1953) is excluded. The
marked difference in the larval stages of P. lutzi (with
opisthorchioid cercariae developing in rediae in gastropods) in
comparison to the faustulid P. harengulae (with trichocercous
cercariae developing in sporocyst in a marine clam), the
embedded condition of the ventral sucker, and the similarity in
the terminal genitalia, lead to the conclusion that P. lutzi is not a
faustulid, and should be included in the Cryptogonimidae.
Indeed, recent molecular studies of another species included in
the Faustulidae show relationship with the Gymnophalloidea,
and suggest the polyphyletic character of the Faustulidae (Sun et
al., 2014).
Miller and Cribb (2008) recognized 68 valid genera in the
Cryptogonimidae, most of which show a Y-shaped excretory
vesicle with a long stem, and arms reaching to the pharynx. The
single exception is Acanthostomoides apophalliformis Szidat, 1956,
with the arms of the Y-shaped excretory vesicle extending to the
ovary. Although Miller and Cribb (2008) mentioned a V-shaped
excretory vesicle in some squat species, its arms would be placed
anterior to the midbody. Pseudosellacotyla mainly differs from all
other genera in the family by its V-shaped excretory vesicle, with
the arms reaching to posterior border of testes. However, the
genera Gonacanthella Sogandares-Bernal, 1959; Caecincola Marshall and Gilbert, 1905; Tabascotrema Lamothe-Argumedo and
Pineda-López; Campechetrema Lamothe-Argumedo, SalgadoMaldonado and Pineda-López, 1997; Paleocryptogonimus Szidat,
1954 Exorchis Kobayashi, 1921; and Metadena Linton, 1910
resemble Pseudosellacotyla in their body shape and in having
symmetrical testes, vitelline follicles in two groups and in the
absence of a gonotyl (Miller and Cribb, 2008), but they differ
from it at least in 1 of the following characters: extension of ceca,
position of seminal vesicle, intestinal bifurcation, vitelline
follicles, elongate body, funnel-shaped oral sucker, shape and
position of ovary.
Gonacanthella and Metadena are parasites of marine fishes,
whereas Caecincola, Tabascotrema, Campechetrema, and Paleocryptogonimus (all of which occur in America) and Exorchis
parasitize freshwater fishes.
Miller and Cribb (2008) mentioned that there are at least 25
known life cycles of Cryptogonimidae with typical ‘‘opisthorchioid’’ cercariae, which commonly lack body pigmentation and
have 8 pairs of flame cells. Cribb (1986) suggested that cercariae
with pigmented body and numerous flame cells may belong to
Heterophyidae. Notwithstanding this, studies on the life cycles of
A. brauni, Acanthostomum gnerii Szidat, 1954, and A. apophalliformis have revealed that species of Cryptogonimidae also possess
cercariae with these features (Ostrowski de Núñez, 1987;
Ostrowski de Núñez and Gil de Pertierra, 1991; Ostrowski de
Núñez et al., 1999). On the other hand, colorless cercariae with 8
pairs of flame cells have been observed to occur in heterophyids
(e.g., Euhaplorchis californiensis Martin, 1950, Ascocotyle gemina
Font, Overstreed and Heard, 1984; Ascocotyle secunda, Ostrowski
de Núñez, 2001; A. tertia Ostrowski de Núñez, 2001; see Martin,
1950; Font et al., 1984; Ostrowski de Núñez, 2001).
The cercaria of P. lutzi fits that described for cryptogonimids
and heterophyids, except for the lack of pigmented eyespots,
unusual in opisthorchioid cercariae, but is shared by the
heterophyid species Eurihelmis monorchis Ameel, 1938, which
penetrates in amphibians (Yamaguti, 1975). The presence of
intestinal ceca is rare, however, has been mentioned for the
cryptogonimid Pseudexorchis major (Hasegawa, 1934), and for
species of the heterophyid Apophallus Lühe, 1909 (Odening, 1970,
1973; Yamaguti, 1975). The rediae of P. lutzi are morphologically
similar to those of both groups but may contain fully developed
cercariae, as opposed to those of the other 3 Argentine
cryptogonimid species (A. brauni, A. gneri, A. apophalliformis).
With the exception of the man-introduced genera Melanoides
Olivier, 1804 and Tarebia H. Adams and A. Adams, 1854,
molluscs of the Thiaridae are distributed in tropical and
subtropical areas of Africa, Asia, Australia, Central, and South
America. It is striking that all thiarid intermediate hosts of
opisthorchioid life cycles were found in Asia, especially the
numerous human heterophyid parasites, which were studied
beginning in the first half of 20th century (Yamaguti, 1975). In
tropical and subtropical areas of South America life cycle studies
were scarce, and thiarids were seldom included. Actually, the
present life cycle is the first of a cryptogonimid that involves a
thiarid intermediate host in South America. In contrast, the
Hydrobiidae were mainly distributed in template and cold areas
of the world, and were extensively studied for digenean life cycles,
which included several cryptogonimid species (Yamaguti, 1975).
The Cochliopidae, well distributed in South America and more
recently studied, presented a rich fauna of cryptogonimid and
heterophyid species (Ostrowski de Núñez and Gil de Pertierra,
2004). As research on life cycles in South America increases, more
thiarids should be found to be involved. In actual fact 3 other
cercariae of the Opisthorchioidea were observed emerging from
A. chloroticum, one of them lacking body pigment, and eyespots
(unpubl. data).
ACKNOWLEDGMENTS
We are indebted to Lic. D. C. Pérez (Entidad Binacional Yacyretá) for
his kind help in snail collection by diving, and to the ichthyologists of the
Universidad Nacional de Misiones, Lic. D. R. Aichino, Lic. M. F. Benitez,
and A. S. Masin for their effort to capture fishes in the dam with the use of
different fishing gear. Special thanks go to Dr. C. Ituarte and his staff for
laboratory facilities for histological sections, to Lic. A. C. Mercado
Laczkó for helping in the preparation of figures, to Dr. V. Ivanov for
helping with some photographs, and to 2 anonymous referees, whose
comments improved the manuscript, and 1 of which helped with the
correct identification of the present species, and provided us with recent
literature. Funds and facilities for this work were provided by EBY
(Yacyretá Binational Entity). The authors are sincerely grateful for the
continued support of the Aylacostoma Conservation Program in Yacyretá.
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