ORIGINAL ARTICLE /ARTÍCULO ORIGINAL
NEW DATA ON TEREANCISTRUM PARVUS KRITSKY ET AL. AND T. PARANAENSIS
KARLING ET AL. (MONOGENEA: DACTYLOGYRIDAE) FROM LEPORINUS
OBTUSIDENS VALENCIENNES (CHARACIFORMES: ANOSTOMIDAE) FROM LAKE
GUAÍBA, SOUTHERN BRAZIL
NUEVOS DATOS ACERCA DE TEREANCISTRUM PARVUS KRITSKY ET AL. Y T.
PARANAENSIS KARLING ET AL. (MONOGENEA: DACTYLOGYRIDAE) DE
LEPORINUS OBTUSIDENS VALENCIENNES (CHARACIFORMES: ANOSTOMIDAE)
DEL LAGO GUAÍBA, REGIÓN SUR DE BRASIL
1 2 3
Emília Welter Wendt ; Cassandra Moraes Monteiro & Suzana B. Amato
1,3Laboratório de Helmintologia, Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do
Sul, Av. Bento Gonçalves 9500, Prédio 43435, sala 208, Bairro Agronomia, CEP 91501-970, Porto Alegre, RS, Brasil
1 2 3
E-mail: wendtemi@gmail.com; cassimonteiro@hotmail.com; sbamato@ufrgs.br
Neotropical Helminthology, 2015, 9(2), jul-dec: 203-210.
ABSTRACT
Key words: gills - Leporinus - morphological structures - measurements - 'piava' - Tereancistrum.
Tereancistrum parvus Kritsky, Thatcher & Kayton, 1980 and T. paranaensis Karling, Lopes,
Takemoto & Pavanelli, 2014 are recorded for the first time on the gills of Leporinus obtusidens
Valenciennes from Lake Guaíba, State of Rio Grande do Sul, southern Brazil. The original
description of Tereancistrum paranaensis was altered in order to correct the position of vagina,
which was described as dextral, but it is actually sinistral; some morphometric data were revised.
The description of T. parvus is complemented with the drawings of a specimen mounted in toto,
with details of the vagina and gonads as well as with measurements of the internal structures of
specimens collected from the gills of 'piava', L. obtusidens from Lake Guaíba.
203
ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
RESUMO
Palavras-chave: brânquias - estruturas morfológicas – medidas - piava.
Terencistrum parvus Kritsky, Thatcher & Kayton, 1980 e T. paranaensis Karling, Lopes,
Takemoto & Pavanelli, 2014, são registrados pela primeira vez em brânquias de Leporinus
obtusidens Valenciennes, 1837 do Lago Guaíba, Rio Grande do Sul, região sul do Brasil.
Tereancistrum paranaensis teve sua descrição original alterada para corrigir a posição da vagina,
que foi descrita como dextra, quando na verdade é sinistra, além disso, alguns dados
morfométricos foram revisados. A descrição de T. parvus é complementada com desenhos de um
espécime montado in toto, detalhes da vagina e gônadas, bem como com medidas das estruturas
internas dos espécimes coletados em brânquias de piava, L. obtusidens do Lago Guaíba.
INTRODUCTION
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Tereancistrum Kritsky, Thatcher & Kayton,
1980 is a well characterized genus being
represented by several species, although the
description of one of them was based on few
specimens, thus preventing the authors to
observe and describe some important
characters. An example is Tereancistrum
parvus Kritsky, Thatcher & Kayton, 1980,
w h o s e des c r i p t i o n w a s base d on
morphological data from a single specimen
and the illustration of the body did not include
the position of the vagina and gonads. Thus,
some morphological characters of this species
were not well described and there are no ranges
of measurements for the characters. For these
reasons a complementation of the description
of T. parvus collected from the host Leporinus
obtusidens Valenciennes, 1837 of Lake Guaíba
is presented. Besides, in the description of
Tereancistrum paranaensis Karling, Lopes,
Takemoto & Pavanelli, 2014, the authors left
some doubts about the position of the vagina,
some structures of the haptor, anchors, bars,
and the male copulatory organ (MCO). In this
paper, we add new information on the
morphology, parasitic indices, and report for
the first time the occurrence of T. paranaensis
and T. parvus in Lake Guaíba, Brazil.
Sixty specimens of L. obtusidens were
collected by professional fishermen from Lake
Guaíba (30°01'S, 51°16'W), State of Rio
Grande do Sul, southern Brazil, in October of
2013. The fish studied were bought directly
from the fishermen as they were taken to the
local market, immediately after the catch. The
study was approved by the Universidade
Federal do Rio Grande do Sul (UFRGS) Ethics
Committee under the number 27531. After
fixation in formalin 5% (Amato et al., 1991),
the gills were removed and parasites collected
under a stereomicroscope. Some specimens
were stained with Gomori's Trichrome
(Humason, 1979) and mounted in Canada
balsam for study of the internal organs, while
other specimens were mounted in Gray and
Wess' medium (Humason, 1979) for the study
of the sclerotized structures. Measurements
are in micrometers (µm), ranges are followed,
between parentheses, by the mean, standard
deviation, and total number of individuals
measured when different than 19 (T.
paranaensis) and 34 (T. parvus), respectively.
The number of hooks was counted according
to Mizelle & Price (1963), and the description
of the male copulatory organ (MCO) followed
Kritsky et al. (1985). Voucher specimens were
deposited in the 'Coleção Helmintológica do
Instituto Oswaldo Cruz (CHIOC)', Rio de
Janeiro, Brazil. Ecological terms follow Bush
et al. (1997).
Tereancistrum paranaensis Karling, Lopes,
Takemoto & Pavanelli, 2014
(Fig. 1)
Description. Based on 19 specimens, 2 stained
in Gomori's Trichome and mounted in Canada
balsam, 17 mounted in Gray & Wess. Body
elongated, fusiform, 350-500 (421 ± 44; n =
15) long, 70-130 (88 ± 17; n = 18) wide.
Cephalic lobes poorly developed. Four pairs of
cephalic organs poorly developed. Cephalic
glands at level of pharynx. One pair of
eyespots, anterior to pharynx. Pharynx sub-
spherical, 25-35 (28 ± 3; n= 11) wide. Peduncle
elongated, distinct from the rest of the body.
Haptor sub-hexagonal, 55-68 (63 ± 3; n = 14)
long, 63-88 (75 ± 7; n = 16) width. Presence of
two haptoral muscles attached to the accessory
sclerites, probably to assist movement. Seven
pairs of hooks, 5 ventral, 2 dorsal. Hooks
similar in size and shape, 15-25 (23 ± 2; n = 12)
MATERIAL AND METHODS
RESULTS
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Neotropical Helminthology. Vol. 9, Nº2, jul-dec 2015
Figure 1: Tereancistrum paranaensis, composite drawing (ventral view). A: in toto; B: male copulatory organ; C: hook; D:
ventral anchor and accessory sclerite; E: dorsal anchor; F: ventral bar; G: dorsal bar; H: haptor. Scales: A = 80 µm; B = 5 µm; C =
20 µm; D = 20 µm; F = 20 µm; G = 20 µm; H = 15 µm; I = 30 µm.
Tereancistrum from Leporinus
long, well developed thumb, recurved shank,
with inflated proximal portion. Filamentous
hook loop (FH) reach inflated portion of the
shank. Ventral anchor 45-50 (46 ± 2; n = 18)
long, 14-20 (16 ± 2; n = 16) wide at base, deep
root indistinct, superficial root well developed,
shaft, and recurved point. Accessory sclerite,
short and spatuliform, 24-27 (25 ± 1; n = 15)
long, associated to superficial root of the
ventral anchor. Dorsal anchor well developed,
15-27 (25 ± 3; n = 17) long, 6-15 (10 ± 3; n = 6)
wide at base, with divergent roots, short shaft,
and straight point. Ventral bar rectangular, 48-
65 (56 ± 4; n = 15) long. Dorsal bar rectangular,
1019 (14 ± 3; n = 8) long. Gonads overlapping.
Testis dorsal to ovary, difficult to observe.
Ovary 8088 (84 ± 4; n = 4) long, 15-38 (24 ±
10; n = 4) wide. MCO is a coiled tube with 1 ½
to 2 ½ counterclockwise rings, proximal ring
diameter 15-22 (18 ± 2; n = 16). Accessory
piece 10-18 (14 ± 3; n = 5) long, non-
articulated with the MCO. Vagina sinistral,
slightly sclerotized, in the anterior portion of
the body. Vitelline glands posterior to pharynx,
extending to the end of intestinal ceca, except
in the region of male copulatory complex and
gonads.
Taxonomic summary.
Host: Leporinus obtusidens Valenciennes,
1837.
Site of infestation: gills.
Locality: Lake Guaíba, State of Rio Grande do
Sul (30°01'S, 51°16'W), southern Brazil.
Prevalence: 26.66%.
Mean intensity of infestation: 1.75
specimens/host.
Abundance of infestation: 0.46 specimen/host.
Range of infestation: 15 specimens/host.
Specimens deposited: CHIOC 38085; CHIOC
38086 (vouchers).
Specimens examined: T. paranaensis (CHIOC
37866; CHIOC 37867) paratypes deposited by
Karling et al. (2014).
Remarks.
The morphology of the haptoral structures,
anchors, bars, and MCO was revised. In the
original description of T. paranaensis, Karling
et al. (2014) characterized the vaginal opening
as dextral when it is sinistral. Furthermore, in
the original illustration the MCO was
represented as coiled clockwise, however,
after examining the specimens deposited in the
'Coleção Helmintológica do Instituto Oswaldo
Cruz (CHIOC)' and the specimens collected
from the gills of L. obtusidens of Lake Guaíba
it was seen that this structure is coiled
counterclockwise. An explanation for this
might be that the specimen was observed in
dorsal view, but described as ventral view,
which resulted in a misleading interpretation
between ventral and dorsal structures. The
morphometric data presented in the original
description of T. paranaensis are incompatible
with the scales presented together with the
illustrations. So, the morphometric data were
corrected based on the new specimens
available.
The peduncle of T. paranaensis is not short as
referred by Karling et al. (2014), instead, this
structure quite visible. In the original
description of T. pa r an a en s is the
measurements of the haptor were not included.
If we compare these structures in the
illustrations presented by the authors, the
haptor appears to be ¼ of total body length.
When the same structure is observed in the
specimens deposited in the CHIOC and in
those collected from L. obtusidens (present
work) it is possible to verify that its size is
closer to 1/7 of the body length. Karling et al.
(2014) did not mention the presence of
haptoral muscles connected to the accessory
sclerite, although these structures are present,
they are well developed, and probably related
to movement of the haptoral structures.
Finally, it should be noted that despite the
observations made in the present work, the
validity of T. paranaensis is preserved, and the
species is recorded for the first time on L.
obtusidens of Lake Guaíba, expanding the
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known geographic distribution and the list of
known hosts for this parasite.
Tereancistrum parvus Kritsky, Thatcher &
Kayton, 1980
(Fig. 2)
Description. Based on 34 specimens, eight
stained in Gomori's Trichome and 26 mounted
in Gray & Wess. Body slender, fusiform, 450-
650 (530 ± 55; n = 34) long, 60-120 (86 ±15; n
= 34) at maximum width. Cephalic lobes well
developed, one apical and two bilateral. Four
cephalic organs. Cephalic glands anterior to
pharynx. One pair of eyespots, immediately
anterior to pharynx; sub-spherical, granular,
and variable in size; granules are spread
throughout the body. Pharynx sub-ovate, 28-
40 (34 ± 4; n = 30) in diameter. Peduncle broad,
sub-hexagonal, 88-128 (113 ±11; n = 27) long,
143-225 (182 ± 20; n = 30) wide. Haptoral
muscles dense, connecting the accessory
sclerites. Seven pairs of hooks, five ventral and
two dorsal. Hooks similar in size and shape,
3040 (35 ± 2; n = 18) long, with erect thumb,
curved shaft, short point, and proximal portion
of shank dilated, FH loop with ¼ of shank
length. Ventral anchor 68-108 (91 ± 8; n = 30)
long, 13-28 (22 ± 4; n = 28) wide at base, with a
root deep and incipient, the other root
superficial and well developed, shaft and point
strongly recurved. Accessory sclerites
delicate, elongated, spatuliform, 88-135 (109
± 11; n = 32) long. Dorsal anchor 68-88 (79 ±
4; n = 30) long, 18-25 (20 ± 3; n = 25) wide at
base. Ventral bar V-shaped, elongated with
rounded, dilated ends, 100-138 (117 ± 10; n =
26) long. Dorsal bar 45-88 (68 ± 10; n = 27)
long. Gonads overlapping. Testis dorsal to
ovary. Ovary 63-100 (77 ± 11; n = 10) long, 13-
40 (22 ± 8; n = 11) wide. Male copulatory organ
is a coiled tube with 3 ½ counterclockwise
rings, proximal ring 13-16 (15 ± 1; n = 25) in
diameter. Accessory piece 25-36 (29 ± 3; n =
18) long, a tube with a ventral groove serving
as guide to the distal portion of the MCO.
Vagina sinistral, cone shaped, strongly
sclerotized, in the middle region of body.
Vitellarium distributed throughout the body
except anterior to pharynx and in the gonads
region.
Taxonomic summary.
Host: Leporinus obtusidens Valenciennes,
1837.
Site of infestation: gills.
Locality: Lake Guaíba, State of Rio Grande do
Sul (30°01'S, 51°16'W), Brazil.
Prevalence: 40%.
Mean intensity of infestation: 2.58
specimens/host.
Mean abundance of infestation: 1.03
specimens/host.
Range of infestation: 112 specimens/host.
Specimens deposited: CHIOC 38087; CHIOC
38088 (vouchers).
Specimens examined: T. parvus, (CHIOC
37863; CHIOC 37864; CHIOC 37865)
voucher specimens deposited by Karling et al.
(2014).
Remarks.
Tereancistrum parvus was described by
Kritsky et al. (1980) based on a single
specimen. Recently, a emended diagnosis of T.
parvus was proposed by Karling et al. (2014).
Thus, we present more morphological data
based on specimens collected in L. obtusidens
from Lake Guaíba, and reaffirm the validity of
T. parvus, when it was compared wth other
species grouped in Tereancistrum.
Tereancistrum parvus is considered valid
based on the morphology of the anchors, the
accessory sclerites and the copulatory
complex, which together form a set of
characteristics which separates this species
from the others placed in Tereancistrum
(Kritsky et al., 1980; Lizama et al., 2004;
Cohen et al., 2012; Cepeda et al., 2012).
However, the detailed study of the samples
revealed some morphological differences.
First, the vagina, strongly sclerotized, is
located in the middle region of the body and is
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Figure 2: Tereancistrum parvus, composite drawing (ventral view). A: in toto; B: male copulatory organ; C: dorsal anchor; D:
ventral anchor and accessory sclerite; E: hooks; F: ventral bar; G: dorsal bar. Scales: A = 96 µm; B = 20 µm; C = 20 µm; D = 10 µm;
E = 45 µm; G = 40 µm; H = 50 µm; I = 15 µm.
cone-shaped, divided into two chambers, one
distal tapered and the other connected to the
vaginal canal. The copulatory complex shows
two differences when compared with the
description of Kritsky et al. (1980): (1) the
male copulatory organ consists of three
counterclockwise rings, its terminal portion
goes inside the accessory piece and ends in a
round-shaped loop that rests on it; (2) the
accessory piece is elongated, has a ventral
groove that serves as a guide for the MCO, and
does not present the projection mentioned in
the original description.
Furthermore, with respect to haptor structures,
the ventral bar is nearly twice as large and
presents rounded and enlarged terminal
portions, which differ from the description
made by Kritsky et al. (1980). The hooks are
longer, thin with a slight dilation in the shank.
Kritsky et al. (1980) and Karling et al. (2014)
did not mention the presence of a haptoral
muscle in this species, although this structure
is present, it is ventral and well developed. The
morphology of the other structures are in
accordance with the original description,
although in ours specimens they are larger. The
differences in size of the structures can be
attributed to the study of a larger number of
specimens, or due to the influence of
development in different hosts.
According to Kritsky et al. (1980),
Tereancistrum is characterized by the presence
of an accessory sclerite articulated to the
ventral anchor and by having a typically
ancyrocephaline haptor (Mizelle, 1936), one
or two pairs of eyespots, and overlapping
gonads. Tereancistrum groups eight species
which parasitize the gill filaments of
Neotropical freshwater characiforms. Seven
species have been described in Brazil, the other
was described from specimens collected in
Colombia (Kritsky et al., 1980; Lizama et al.,
2004; Cohen et al., 2012; Cepeda et al., 2012;
Karling et al., 2014). In Brazil, species of
Tereancistrum have been recorded in the
following rivers: Amazonas, Paraná, and
Mogi Guaçu. The records of T. parvus and T.
paranaensis in L. obtusidens from Lake
Guaíba, State of Rio Grande do Sul extend the
known geographic distribution of these
species. The descriptions of our specimens of
T. paranaensis and of T. parvus presented here
improve those of the original authors.
We are thankful to the following people:
Marcelo Knoff, curator of the 'Coleção
Helmintológica do Instituto Oswaldo Cruz
(CHIOC)', for the loan of specimens of T.
parvus and T. paranaensis and for accepting
our representative specimens for deposit.
Emília Wendt thanks 'Conselho Nacional de
Desenvolvimento Científico e Tecnológico
(CNPq)' for the scholarship.
DISCUSSION
209
ACKNOWLEDGMENTS
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Received May 15, 2015.
Accepted June 30, 2015.
