Abstract
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
Resumen
TWO NEW SPECIES OF PAVANELLIELLA (MONOGENEA, DACTYLOGYRIDAE)
PARASITIC ON PIMELODID FISHES FROM MOGI GUAÇU RIVER, SOUTHEASTERN
BRAZIL, AND NOTES ON THE MORPHOLOGY OF P. PAVANELLII
DOS NUEVAS ESPECIES DE PAVANELLIELLA (MONOGENEA, DACTYLOGYRIDAE)
PARÁSITOS DE PECES PIMELÓDIDOS DEL RIO MOGI GUAÇU, SUDESTE DE
BRASIL Y NOTAS SOBRE LA MORFOLOGÍA DE P. PAVANELLII
1 2 3
Julio C. Aguiar , Paulo S. Ceccarelli & José L. Luque
1 Curso de Pós-Graduação em Ciências Veterinárias, Universidade Federal Rural do Rio de Janeiro, BR-465, Km 7, CEP.:
23.890–000, Caixa Postal 74.508, Seropédica, Rio de Janeiro, Brazil.
2 Centro Nacional de Pesquisa da Conservação de Peixes Continentais, Instituto Chico Mendes para Conservação da
Biodiversidade, Rodovia Pref. Euberto Nemésio Pereira de Godoy, Km 6,5, CEP 13.630-970, Caixa Postal: 64,
Pirassununga–SP, Brazil
3 Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro. E-mail: jlluque@ufrrj.br
Suggested citation: Aguiar, J.C., Ceccarelli, P.S. & Luque, J.L. 2011. Two new species of Pavanelliella (Monogenea,
Dactylogyridae) parasitic on pimelodid fishes from Mogi Guaçu river, southeastern Brazil, and notes on the morphology of P.
pavanellii. Neotropical Helminthology, vol 5, nº 2, pp. 213-224.
Key words: Ancyrocephalinae – Biodiversity - nasal parasites - Neotropical Region - Pavanelliella laertei sp. n. -
Pavanelliella takemotoi sp. n. - South America.
Dos nuevas especies de Pavanelliella (Dactylogyridae) fueron descritas y algunos detalles sobre la
morfología de Pavanelliella pavanellii Kritsky & Boeger, 1998 se han añadido sobre la base de
especímenes colectados en los peces pimelódidos del rio Mogi Guaçu, Brasil. Pavanelliella takemotoi
sp. n., colectado de las cavidades nasales de Pimelodus maculatus Lacepède, 1803 se diferencia de sus
congéneres por tener un órgano copulador masculino (OCM) con 2-5 anillos, canal vaginal sinuoso,
Neotrop. Helminthol., 5(2), 2011
2011 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
Versión Impresa: ISSN 2218-6425 / Versión Electrónica: ISSN 1995-1043
Two new species of Pavanelliella (Dactylogyridae) were described and some details about the
morphology of Pavanelliella pavanellii Kritsky & Boeger, 1998 were added based on specimens
collected from pimelodid fishes from Mogi Guaçu River, Brazil. Pavanelliella takemotoi sp. n.,
collected from nasal cavities of Pimelodus maculatus Lacepède, 1803 differs from its congeners by
having a male copulatory organ (MCO) with 2–5 rings, vaginal canal sinuous without loops in distal
portion of vaginal canal and anteriorly directed vagina containing five irregular rings around the
vestibule. Pavanelliella laertei sp. n. collected from P. heraldoi Azpelicueta, 2001 is separated from the
other species of the genus by lacking a vaginal vestibule and by distal end shape of accessory piece,
which resemble flames or is bifurcated with one flank hooked in P. laertei sp. n. The specimens of P.
pavanellii examined in this study showed morphological variations especially on MCO, vaginal canal
and vagina morphology with respect to the holotype and paratype and are noted in this paper.
Significant differences among the described species were confirmed on the light of multivariate
morphometric statistical analysis. Initially a Principal Component Analysis (PCA) showed the
multivariate distinction between the three species and after a Linear Discriminant Analysis (LDA)
revealed that the Maximum number of MCO ring and the MCO length fairly contributed to the
discrimination between all Pavanelliella species (Wilk´s lambda = 0.006; p<0.000). This is the first
record of Pavanelliella species in Mogi Guaçu River.
213
INTRODUCTION
pero nunca con lazos en la porción distal del canal vaginal y la vagina es dirigida anteriormente y tiene
cinco anillos irregulares alrededor del vestíbulo. Pavanelliella laertei sp. n. colectados de P. heraldoi
Azpelicueta, 2001 se diferencia de las otras especies del género por La falta de un vestíbulo vaginal y
por la forma de extremo distal de la pieza accesoria, que se asemeja a las llamas o se bifurca con un
flanco enganchado en P. laertei sp. n. las muestras de P. pavanellii examinadas en este estudio
mostraron variaciones morfológicas, especialmente en la morfología de OCM, canal vaginal y de la
vagina con respecto al holótipo y parátipo, y se discuten en esta investigación. Todas las diferencias
entre las especies estudiadas fueron confirmadas com el uso del análisis estadístico morfométrico
multivariada. Inicialmente, un Análisis de Componentes Principales (ACP) mostró la distinción
multivariado entre las tres especies y después un Análisis Discriminante Lineal (ADL) reveló que el
número máximo de anillos del OCM y la longitud del OCM contribuyeron bastante a la discriminación
de todas las especies de Pavanelliella (Wilk´s lambda = 0,006; p<0,000). Este es el primer registro de
especies de Pavanelliella en el río Mogi Guaçu.
Palabras clave: América del Sur Ancyrocephalinae Biodiversidad - parásitos nasales - Pavanelliella laertei sp. n.
- Pavanelliella takemotoi sp. n. - Región Neotropical.
Papers about monogeneans parasitic on Brazilian
pimelodids focused on descriptions of
dactylogyrid species infecting gills of the hosts
(Boeger & Vianna, 2006; Cohen & Kohn, 2008;
Monteiro et al., 2010). Kritsky & Boeger (1998)
proposed Pavanelliella Kritsky & Boeger 1998 to
include dactylogyrid species parasitic on nasal
cavities of pimelodid fishes, although later Kritsky
& Mendoza-Franco (2003) described another
Pavanelliella species parasitic on a heptaterid host.
Pavanelliella includes specimens with few
features compared to other ancyrocephalin
species, and this makes still more difficult the
distinction between the species. After a carefully
morphological examination, we separated three
putative species which shared based in their
morphological characteristics and performed to
multivariate analysis, to confirm statistically, the
differences between the species observed by us.
Here, two new species of Pavanelliella are
described and new morphological data are added to
P. pavanellii Kritsky & Boeger 1998 from
specimens collected from the nasal cavities of P.
maculatus Lacepède, 1803 and Pimelodus heraldoi
Azpelicueta, 2001 in São Paulo, Pirassununga,
southeastern Brazil.
MATERIAL AND METHODS
Host fish and parasites collection and
identification
One hundred-one fishes were collected between
February 2008 and March 2010 from Cachoeira de
Emas (21º 58'S, 47º 26' W) on Mogi Guaçu River,
Pirassununga, São Paulo. Samplings were carried
out with nets and cast nets. Were collected 57
individuals of P. maculatus (Mean of total length =
26.24 ± 6.14; mean of weight = 258.42 ± 191.85)
and 44 of P. heraldoi (Mean of total length = 12.03
± 2.21; mean of weight = 18.46 ± 12.61). The fishes
were identified according to Britski et al. (1999)
and Azpelicueta (2001). The fish nasal cavities
were disrupted with a probe and washed with
1:4000 formalin solutions. The parasites were
posteriorly fixed in 4% formalin. The parasites
were stained with Gomori's trichrome and mounted
in Canada balsam for visualization of soft tissues,
or mounted in Gray and Wess medium to study of
sclerotized structures (Kritsky et al., 1986), or even
stained with Gomori's trichrome and mounted in
Gray and Wess medium. The identification of the
parasites was carried out use of an optical
microscope with differential interference contrast
(DIC) Olympus BX 51. The illustrations were
made with a drawing tube attached to a phase
contrast microscope Opton™. The measurements
(in micrometers) are represented by the average,
with ranges in parentheses and followed by the
number (n) of specimens. All measurements were
taken as straight-line distance extending between
the two most distant parts of such structures, using
a calibrated eyepiece micrometer according to
Mizelle & Klucka (1953). The diagnosis of the
genus was based on Kritsky & Mendoza-Franco
(2003). The quantitative population descriptors
(prevalence, abundance and mean intensity of
infestation) are those suggested by Bush et al.
(1997). Type specimens were deposited in the
Helminthological Collection of the Institute
Oswaldo Cruz (CHIOC), Rio de Janeiro, Brazil.
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Two new species of Pavanelliella parasitic on pimelodid fishes Aguiar et al.
Statistical analysis
Morphological features measured were those in
accordance with Kritsky & Mendoza-Franco
(2003). However, the choice of variables for
morphometric analysis follows the parameters
suggested by Du-Preez & Maritz (2006) that are
those easily measurable, repeatable, not be
geometrically redundant, representative and non-
negative. So, an univariated analysis was
performed to verify the variance (Bartlett's test P
levels < 0,05) of the variables values and the
Shapiro-Wilk test (P levels < 0,05) were run for
evaluating normality of data (McGarigal et al.,
2000) using the MYSTAT 12 (2007) (SYSTAT 12
©) also utilized for Principal Component Analysis
(PCA) and a Linear Discriminant Analysis (LDA).
The variables who had significant variance and
non-normal distribution were log (x) transformed.
10
The measurement of the body (total length and
greatest wide), haptor, germarium and testis
(length and wide) weren't used because their values
can to suffer drastic variations as consequence of
deformation of the soft parts during the fixation and
mounting of the parasites (Strona et al., 2005;
Vignon & Sasal, 2010; Vignon, 2011). Only the
hard structures (male copulatory organ length,
proximal ring diameter and hooks length), the
pharynx diameter and accessory piece length
values were also used for morphometric
analysis, so, only five out 14 features measured
were selected. A Pearson's correlation
coefficient with 95 percent confidence interval
was performed from five selected variables
according to exposed above, since that the
redundancy of variables chosen is indicate by
high Pearson's values (Vignon & Sasal, 2010;
Vignon, 2011) indicating a multicollinearity.
Additionally, nine categorical variables alone
and in combination with continuous variables
were used in multivariate analysis (Table 1).
An ordination analysis (PCA) was conducted
in order to evidence the presence of
multivariate distinction between the three
species (Strona et al., 2005). A backward
stepwise LDA was run to describe how the
species grouping differ between their
(McGarigal et al., 2000) and to select the best
set of morphometric variables in order to
contribute for groupings distinction.
RESULTS
Descriptions
Family Dactylogyridae Bychowsky, 1933
Pavanelliella takemotoi sp. n. (Figs. 1–8)
Diagnosis (based on 48 specimens: 6 stained with
Gomori's trichrome and mounted in Canada
balsam, 5 stained with Gomori's trichrome and
mounted in Grey and Wess's medium, 37 mounted
in Grey and Wess's medium): Body 426 (246–580;
n = 19), long, fusiform, tapering posteriorly,
peduncle absent; greatest width of trunk 140
(86–240; n = 19) at level of copulatory complex.
Cephalic region with 2 pairs of poorly developed
cephalic lobes, each lobe with 3 head organs;
cephalic glands present. Eyes 4 subequal,
equidistant; accessory granules few in cephalic
region. Pharynx subspherical 23 (14–36; n = 22) in
diameter; esophagus moderately long; intestinal
caeca confluent in posterior trunk after the
germarium. Haptor 82 (51–122; n = 15) wide, 59
(46–69; n = 15) long, comprising delicate extension
of posterolateral trunk velum-like, with slightly
rounded tip. Hooks 16 (13–21; n = 96), with
terminally expanded protruding, slightly depressed
thumb, a delicate point; filamentous hook loop
reaching union of shank subunits. Testis 67
(42–104; n = 5) long, 20 (19–27; n = 5) wide,
elongate ovate, tapering posteriorly, posterodorsal
to germarium; seminal vesicle sigmoid, lying to left
of midline in anterior trunk, vas deferens observed
until looping left intestinal. Prostatic reservoir
saccate. Male copulatory organ (MCO) 35 (23–52;
n = 29) long, 19 (16–27; n = 29) proximal ring
diameter, delicate, tubular, coiled with 2–5 rings;
base with 4 flanges, 2 proximal and 2 distal, 3
variations of flanges are observed. Accessory piece
27 (21–40; n = 25) long, comprising sheath
enclosing medial or distal portion of MCO, distally
partite. Germarium elongate, posteriorly tapering,
64 (45–104; n = 7) long, 18 (6–30; n = 7) wide;
oviduct, ootype, not observed. Vagina
sinistroventral, distal sclerotized vestibule,
anteriorly directed, with 4–5 irregular rings around
it; vaginal canal slightly sclerotized, seminal
receptacle subspherical, overlapped germarium
partially. Vitellaria dense, absent in the region of
Taxonomic summary
Type host: Pimelodus maculatus Lacepède, 1803,
mandi amarelo (Siluriformes, Pimelodidae).
Site of infection: Nasal cavity.
Type locality: Cachoeira de Emas, Mogi Guaçu
215
Neotrop. Helminthol., 5(2), 2011
River, Pirassununga, State of São Paulo, Brazil
(21º 58'S; 47º 26' W).
Prevalence of infection: 35.1%.
Mean intensity of infection: 2.3.
Mean abundance of infection: 0.8.
Specimens deposited: Holotype (CHIOC 37567a),
paratypes (CHIOC 37568a-f, 37569, 37570a-b,
37571, 37572, 37573, 37574, 37575a-b, 37576a-b,
37577a - b , 37578, 37579a-b , 37567b ,
3758037582a-C).
Etymology: The specific name is in honor to
Ricardo Massato Takemoto in recognition to his
contribution to fish parasitology in Brazil.
Remarks
Pavanelliella takemotoi sp. n. is close to P.
pavanellii and P. scaphiocotylus because these
species have a vaginal vestibule. However, P.
takemotoi sp. n. differs from the latter two species
by the vagina shape, which in P. pavanellii is
represented by a simple vaginal vestibule without
ornamentations and a vaginal canal with 1–3 loops
in the distal portion. Pavanelliella scaphiocotylus
have a simple vestibule and a vaginal canal with
4–5 loops in the distal portion around the vestibule.
In P. takemotoi sp. n., the vagina is anteriorly
directed and apparently longest, besides having
4–5 irregular rings around of the vaginal vestibule
and lack the loops of the distal portion of vaginal
canal. Pavanelliella takemotoi sp. n. also differs of
P. pavanellii and P. scaphiocotylus by presenting 4
flanges (1–3 flanges in P. pavanellii; 2 flanges in P.
scaphiocotylus) on the bases of MCO; The number
of MCO rings of P. takemotoi sp. n. is usually 4, but
was found two specimens with 2 and 5 MCO rings,
differentiating it from P. pavanellii (1–2 MCO
rings) and P. scaphiocotylus (5–6 MCO rings).
Pavanelliella takemotoi sp. n. also differs from P.
scaphiocotylus because this last species haves a
prominent tissue ridge along anterodorsal haptoral
surface. Additionally P. takemotoi sp. n. has a more
larger MCO (35) than P. pavanellii (23) and a more
larger hook length (16) than P. pavanellii (12) and
P. scaphiocotylus (14).
Diagnosis (based on 2 specimens stained with
Gomori's trichrome and mounted in Grey and
Wess's medium and 5 specimens mounted in Grey
and Wess's medium): Body 334 (274–374; n = 7)
long, ellipsoid, peduncle absent and differentiated
haptor; greatest width of trunk 135 (92–159; n = 4)
Pavanelliella laertei sp. n.
(Figs. 9–15)
in posterior third of body. Cephalic margin
rounded, with 3 pairs of head organs; cephalic
glands present. Eyes 4 subequal with two anterior
more closely than posterior eyes, sometimes not
observed. Pharynx subspherical 25 (20–30; n = 5)
in diameter; esophagus short; intestinal caeca
confluent posterior to germarium. Haptor 70
(60–79; n = 2) wide, 51 (42 –66; n = 5) long,
comprising delicate extension of postero lateral
trunk velum-like, with rounded tip, differentiated
from trunk by a constriction anterior to seventh pair
of hooks. Hooks 14 (11–17; n = 23), with
terminally expanded protruding erected thumb, a
delicate point, proximal subunit of shank slightly
expanded; filamentous hook loop reaching union
of shank subunits. Testis 30 (20–43; n =3) long, 17
(8–29; n = 3) wide, mediodorsal to germarium; vas
deferens observed until looping left intestinal;
seminal vesicle not observed. Prostatic reservoir
saccate. MCO 43 (21–70; n = 5) long, 18 (17–20; n
= 6) first ring diameter, tubular, forming coils with
2–3 rings or sometimes with 2 anterior rings and 2
posterior rings in relation to accessory piece; base
with 2–4 flanges. Accessory piece 20 (18–21; n =
3) long, comprising sheath enclosing distal or
medial portion of MCO, with irregular distal end
flame-like or bifurcated with one of them hooked.
Germarium elongate 57 (38–86; n = 3) long, 18
(10–29; n =3) wide, oval; oviduct, ootype, not
observed. Vagina sinistroventral, vaginal vestibule
not observed; vaginal canal sclerotized, elongate,
sinuous with 2–3 loops in distal portion with a duct
inside; seminal receptacle partially overlapped to
germarium. Vitellaria dense, absent in the region of
the reproductive organs.
Taxonomic summary
Type host: Pimelodus heraldoi Azpelicueta, 2001,
mandi branco (Siluriformes, Pimelodidae).
Site of infection: Nasal cavity.
Type locality: Cachoeira de Emas, Mogi Guaçu
River, Pirassununga, State of São Paulo, Brazil (21º
58'S; 47º 26' W).
Prevalence of infection: 14%.
Mean intensity of infection: 1.5.
Mean abundance of infection: 0.2.
Specimens deposited: Holotype (CHIOC 37561),
paratypes (CHIOC 37562, 37563, 37564, 37565,
37566).
216
Two new species of Pavanelliella parasitic on pimelodid fishes Aguiar et al.
Etymology: The specific name is in honor to Laerte
Batista de Oliveira Alves by his contribution to fish
conservation studies in Brazilian waters.
Remarks
Pavanelliella laertei sp. n. is more close to P.
pavanellii and P. scaphiocotylus because these two
species share the presence of loops in distal portion
of vaginal canal (2–3 loops in P. laertei; 1–3 in P.
pavanellii; and 45 in P. scaphiocotylus).
However, the new species is different from all
congeneric species because Pavanelliella laertei
sp. n. lacking a vaginal vestibule. Moreover,
Pavanelliella laertei sp. n. has a larger hook (14)
and MCO length (43) than P. pavanellii (12 and 23,
respectively). But, the accessory piece length of P.
laertei sp. n. (20) is lower than P. pavanellii (27).
Although P. scaphiocotylus has the same hook
length (14) of P. laertei sp. n., the former species
has a prominent tissue ridge along anterodorsal
haptoral surface (absent in P. laertei sp. n.). The
shape of distal end of accessory piece can be single,
flame-like or bifurcated with one end hooked on P.
laertei sp. n. The single distal end of accessory
piece is present too on P. pavanellii, P.
scaphiocotylus and P. takemotoi sp. n., but the
flame-like and hooked distal ends never are present
on these last three species. Additionally, P. laertei
sp. n. was found in another host species, Pimelodus
heraldoi, which to date hadn't a parasitological
record.
Pavanelliella pavanellii Kritsky & Boeger, 1998
(Figs. 16–18)
Diagnosis (based on 9 specimens: 1 stained with
Gomori's trichrome and mounted in Grey and
Wess's medium, 8 mounted in Grey and Wess's
medium): Body 340 (250–451; n = 7) long; greatest
width of trunk 102 (69–126; n = 7). Pharynx
diameter 19 (13–26; n = 4). Haptor 88 (87–120; n =
7) wide, 60 (48–77; n = 7) long. Hooks 12 (8–14; n
= 7). Testis (35; 39; n = 2) long, (11; 14; n = 2) wide.
MCO 23 (11–34; n = 7) long, 19 (13–24; n = 7) first
ring diameter. Accessory piece 27 (18–48; n = 4)
long. Germarium 55 (40–77; n = 4) long, 16 (9–23;
n = 4) wide.
Taxonomic summary
Host: Pimelodus maculatus Lacepède, 1803,
mandi amarelo (Siluriformes, Pimelodidae).
Site of infection: Nasal cavity.
Locality: Cachoeira de Emas, Mogi Guaçu River,
Pirassununga, Brasil (21º 58'S e 47º 26' W)
(Marcho 2008; September 2010).
Prevalence of infection: 14%.
Mean intensity of infection: 1.25.
Mean abundance of infection: 0.2.
Specimens deposited: Voucher specimens (CHIOC
37554a, 37555, 37560, 37559, 37558, 37557,
37556, 37554b, 37553a, 37553b).
Other specimens studied: Holotype (INPA PLH
365), paratype (INPA PLH 366a).
Remarks
The specimens of P. pavanellii collected from
Mogi Guaçu River and examined on this study
showed morphological differences in MCO,
vaginal canal and vagina compared to the
descriptions and deposited material of Kritsky &
Boeger (1998). The accessory piece described by
Kritsky & Boeger (1998) has a proximal lobe. In
the specimens observed by us this proximal lobule
was less developed or even absent as the accessory
piece was more or less contracted, respectively. In
the holotype of P. pavanellii the accessory piece
cannot be observed, but in the paratype was quite
evident as it has been observed by the authors.
Kritsky & Boeger (1998) observed that the
proximal and distal margins of base of the MCO
were sclerotized, but they gave not any information
about the MCO base flanges existence. We
observed the presence of 3 sclerotized flanges in
our specimens, one proximal and 2 distal, and the
exam of the holotype and paratype described
above, revealed the presence of 2 miniature flanges
at distal margin of MCO of paratype and one in
each margin of holotype. The vagina of the
specimens examined by us shows a large vaginal
vestibule, only observed in the paratype. The
vaginal vestibule of the holotype is equal to the
Kritsky & Boeger (1998) illustration, ie, longer
than wide. The vaginal canal of P. pavanellii
according to Kritsky & Boeger (1998) is coiled and
has 1 loop in its distal portion (Kritsky & Mendoza-
Franco, 2003); however in our specimens we
observed of 1–3 loops and in the holotype we
observed 2 loops. It was also observed in our
specimens that the vaginal canal extends into the
vaginal vestibule reaching near the lateral end of
the vestibule. Kritsky & Boeger (1998) did not
observe this because in the holotype and paratype
the vaginal canal ends closest to the proximal
portion of vaginal vestibule. We had access to only
217
Neotrop. Helminthol., 5(2), 2011
the holotype and one paratype, and, although
morphological variations was observed in this
parasites examined, especially with respect to
vaginal morphology, we don't redescribe this
species, since, possibility has that the total type
series of P. pavanellii can show more
morphological diversity.
Statistical analysis
On the first PCA, with all variables, the three first
factors (Eingenvalues > 1) accounts for 79% of the
variance, with the first factor mainly represented
by the minimum number of vaginal canal; the
second, by the minimum number of MCO ring and
the third, by the presence of the accessory piece
with flame-like distal end. In this analysis the
categorical variables were those that contributed
for the longest variability of the total sample. Only
continuous variables were used on the second PCA
in which the first factor accounts for 35.8% of the
variance and the second, 23.6%. In this analysis the
hook length, and the accessory piece length were
that captured the almost of variance between
species groups (59%). The backward stepwise
LDA with the set of total variables revealed that six
out nineteen variables were the best set of
characters to explain the variability within groups
composed by three species. The predictor variables
selected by stepwise were pharynx diameter, hook
length, MCO length, proximal ring diameter,
maximum number of MCO ring, and accessory
piece length. The model was successfully
discriminating among the three species (Wilk´s
lambda = 0.006; p<0.000). The first canonical
variable captures most of the difference among the
groups, accounting for 99% (eigenvalue = 87.69)
of the total dispersion of the groups, whereas the
second canonical variables accounted for 0.84%
(0.75) (Table 2). The cross validated classification
showed that overall 100% of monogeneans were
correctly classified.
The scatter plot (Fig. 19) considering two
canonical variables showed that the first
(Maximum number of MCO ring) and the second
variable (MCO length) fairly contributed to
discriminated all Pavanelliella species.
DISCUSSION
The morphometrical analysis has been used to
distinguish monogeneans species (Vignon, 2011).
In many researches the data collinearity of
variables choice has been a condition to run the
multivariate analysis (Shinn et al., 2004; Du-Preez
& Maritz, 2006). Vignon & Sasal (2010) and
Vignon (2011) having stated that the data
collinearity of variables can not be useful for
morphometric multivariate analysis because it
contribute to the same direction in the species
discrimination. In present paper we used the non-
collinearity of data and this resulted on well species
distinctiveness.
Although the present research don't had as
objective to evaluate the phylogenetic relationships
between the Pavanelliella species, make some
general considerations could be important.
Specimens belong to Pavanelliella Kritsky and
Boeger, 1998 have a few morphological
characteristics and so, is necessary to look for
others characters, beyond of the MCO and
accessory piece morphology to support the
description of new species. The vaginal vestibule
when present or absent; the number of loops in
distal portion of vaginal canal or it absence, seems
reasonable morphological characters to contribute
on distinguishment of the Pavanelliella species.
Pavanelliella laertei sp. n. lacking the vaginal
vestibule, it was collected on Pimelodus heraldoi,
whereas Pavanelliella pavanellii and P. takemotoi
sp. n. have a vaginal vestibule and were both
collected on P. maculatus. But unlike of P.
pavanellii, Pavanelliella takemotoi sp. n. hasn't
loops on the distal portion of the vaginal canal. This
can be results of an inter-host speciation (Poisot &
Desdevises, 2010). However, we don't know if this
evolutive process was result of a co-speciation, or
host switch and speciation or speciation followed
by host switch. But one of these events seems have
occurred on the three Pavanelliella species found
on pimelodid fishes from Mogi Guaçu river basin.
The largest distance between centroids of P.
takemotoi sp. n. and P. laertei sp. n. (266.730),
between P. takemotoi sp. n. and P. pavanellii
(411.468) and the shorter distance between
centroids (10.418) of P. pavanellii and P. laertei sp.
n. reinforces this possibility. However, these
questions about these speciation events can't be
answered fully with morphometric analysis alone
(Poisot & Desdevises, 2010).
Two set of morphological variations were found for
P. laertei sp. n. The first set (Figs.9–11) showed by
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Two new species of Pavanelliella parasitic on pimelodid fishes Aguiar et al.
smaller specimens had a minor MCO, and lacking
hook loops while the second morphological set
(Figs. 12–15) represented by the largest specimens
had the largest MCO and hook loops present.
Although these differences have suggested us
belong to different species, we consider more
careful to keep them as intra-specific
morphological variations, especially given the
similarity of the morphology of the vagina.
Previous to present paper, Pavanelliella Kritsky
and Boeger, 1998 was represented by two species.
The type species, P. pavanellii, was described from
specimens collected from the nasal cavity of
Pseudoplatystoma corruscans (Spix & Agassiz
1829) from the Baía River, Mato Grosso (type
locality), from the Paraná River, State of Paraná
and from Callophysus macropterus (Lichtenstein
1819) collected from Solimões River in the State of
Amazonas, Brazil (Kritsky & Boege, 1998).
Subsequently, Brasil-Sato & Pavanelli (2000)
reported this species in association with Pimelodus
maculatus Lacepède, 1803 collected from the
Paraná River and São Francisco River, Brazil.
Later, another species was proposed, P.
scaphicotylus Kritsky and Mendoza-Franco, 2003,
collected from the Yucatán Peninsula in Mexico,
parasitizing nasal cavity of R h am d ia
guatemalensis Kritsky & Mendoza-Franco, 2003
(Kritsky & Mendoza-Franco, 2003).
Currently, Pavanelliella species are distributed in
fishes from 3 siluriform genera (Boeger & Vianna,
2006). As siluriforms are very speciose in the
neotropics (Lundberg & Littmann, 2003), new
records and new Pavanelliella species will
certainly be described in other species and
localities in this region.
Ringmin Ringmax Vagvest Canvagmin Canvagmax Accsing Accpart Accflam Acchook
P. pavanellii
1 2 1 1 3 1 0 0 0
P. takemotoi sp. n. 2 5 1 0 0 1 1 0 0
P. .laertei sp. n. 2 3 0 2 3 1 0 1 1
Table 1. Categorical variables of Pavanelliella spp. Minimum and Maximum number of MCO ring (Ringmin; Ringmax); Vaginal
vestibule (Vagvest; 1 = present; 0 = absent); Minimum and Maximum number of loops of the distal portion of the vaginal canal
(Canvagmin; Canvagmax); Distal end of accessory piece (Single = Accsing; Partite = Accpart; Flamed = Accflam; Hooked =
Acchook; 1 = present; 0 = absent).
Variables Factor 1 Factor 2
Pharynx diameter 0.232 0.422
Hook length -0.286 0.082
Male Copulatory Organ length -0.542 0.813
Proximal ring diameter 0.247 -0.177
Maximum number of MCO ring -1.157 -0.032
Accessory piece length 0.077 -0.499
Table 2. Canonical discriminant functions of categorical and continuous variables of Pavanelliella spp. selected by backward
stepwise LDA.
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Neotrop. Helminthol., 5(2), 2011
Figures 1–8. Pavanelliella takemotoi sp. n. 1. Whole mount, dorsal view. 2–4. Compulatory complex: ventral view. 5. Base of
MCO. 6. Hook. 7–8. Vagina, dorsal view. Scale bars: 100 µm (Fig. 2) and 20 µm (Figs. 3–9). PHARYNXD = Pharynx diameter;
ACCPIECEL = Accessory piece length; PRINGD = Proximal ring diameter; MCOL = Male copulatory organ length; HOOKL =
Hook length
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Two new species of Pavanelliella parasitic on pimelodid fishes Aguiar et al.
Figures 9–15. Sclerotized structures of Pavanelliella laertei sp. n. 9. Copulatory complex, dorsal view. 10. Hook. 11. Vagina,
dorsal view. 12–13. Copulatory complex, left side and ventral view, respectively. 14. Hook. 15. Vagina, ventral view. Scale bars:
25 µm (Fig. 12, 16), 20 µm (Figs.10, 13–14), and 15 µm (Figs. 11,15).
Figures 16–18. Pavanelliella pavanellii Kritsky & Boeger, 1998. 16. Copulatory complex, ventral view. 17. Hook. 18. Vagina and
vaginal canal, ventral view. Scale bars: 10 µm (Figs. 17, 19) and 25 µm (Fig. 18).
221
Neotrop. Helminthol., 5(2), 2011
ACKNOWLEDGMENTS
To Célio Magalhães Curador of the Invertebrate
Collection of the INPA for having kindly sent
specimens for comparison in this study. To Aida
Hiromi Kojima for their suggestions on the use of
drawing software. To Daniele Fernanda Rosim for
his assistance with the statistical analysis. J.C.
Aguiar was funded by a postgraduate scholarship
provided by CAPES. J.L. Luque was supported by
a grant and by a research fellowship from Conselho
Nacional de Desenvolvimento Científico e
Tecnológico do Brasil (CNPq).
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Correspondense to author /Autor para correspondencia:
José L. Luque
Departamento de Parasitologia Animal, Universidade
Federal Rural do Rio de Janeiro.
E-mail/ correo electrónico:
jlluque@ufrrj.br
Received July 28, 2011.
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