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Visceral Pigmentation in Three Species of the Genus Scinax AnuraHylidaeDistinct Morphological Pattern.

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THE ANATOMICAL RECORD 295:298?306 (2012)
Visceral Pigmentation in Three Species
of the Genus Scinax (Anura: Hylidae):
Distinct Morphological Pattern
LILIAN FRANCO-BELUSSI,1* LIA RAQUEL DE SOUZA SANTOS,2
RODRIGO ZIERI,3 AND CLASSIUS DE OLIVEIRA3
1
Post-graduation Program in Animal Biology, Department of Biology, Sa?o Paulo State
University (UNESP), Sa?o Jose? do Rio Preto, Sa?o Paulo, Brazil
2
Department of Biology, Goia?s Federal Institute (IFG), Campus Rio Verde, Goia?s, Brazil
3
Department of Biology, Sa?o Paulo State University (UNESP),
Sa?o Jose? do Rio Preto, Sa?o Paulo, Brazil
ABSTRACT
Amphibians share with other ectothermic vertebrates an extracutaneous pigmentary system consisting of melanin-containing cells in various organs and tissues. We describe the interspeci?c variation in the
visceral pigmentation in three anuran species (Scinax similis, S. fuscovarius, and S. fuscomarginatus). We analyzed the visceral pigmentation
of 15 adult males from each species during the reproductive period. The
individuals were weighed and measured, and the pigmented visceral cells
were classi?ed and documented in stereomicroscope. The shape and
amount of pigment cells differed among organs and also among species.
Signi?cant differences were detected in the cardiorespiratory system,
digestory system, urogenital system, and lumbosacral peritoneum. In the
urogenital system, the main difference was observed in the testes, in
which only S. fuscomarginatus had varying degrees of pigmentation.
C 2011 Wiley Periodicals, Inc.
Anat Rec, 295:298?306, 2012. V
Key words: anurans; visceral pigmentation; melanocytes
Visceral pigmented cells occur in amphibians and
other ectothermic vertebrates in various tissues and
organs (Gallone et al., 2002). Pigmented cells found in
hematopoietic organs are denominated melanomacrophages, they are derived from hematopoietic stem cells
and have immunological functions (Agius, 1981; Sichel
et al., 1997). Melanin-containing cells are similar to
melanocytes (Agius and Agbede, 1984; Zuasti et al.,
1998) in the lungs, heart, blood vessels, thymus, gonads,
and meninges of ?sh, amphibians, and reptiles (Gallone
et al., 2002; Bagnara and Matsumoto, 2006; FrancoBelussi et al., 2009, 2011). Melanocytes are derived from
the ectodermal neural crest (Sichel et al., 1997), and are
able to produce and store melanin in the cytoplasm
(Agius and Roberts, 2003).
The visceral pigmentation in some organs varies
depending on physiological and environmental factors.
Physiological factors include age and diseases (Agius
and Agbede, 1984). In addition, low temperatures have
been shown to increase the amount of melanin and
induce metabolic and structural changes in hepatic cells
C 2011 WILEY PERIODICALS, INC.
V
of Rana esculenta (Barni et al., 1999). Although, the
functional role of these pigmented cells in most organs
is not de?ned yet, several hypotheses had been posed
(Gallone et al., 2002), including cytoprotective functions
against free radicals (McGraw, 2005) and detoxi?cation
from pollutants (Fenoglio et al., 2005).
Since the variation in the visceral pigmentation
depends on several factors and the functional role of
Grant sponsor: Fundac?a?o de Amparo a? Pesquisa do Estado de
Sa?o Paulo, FAPESP; Grant numbers: 02/08016-9, 05/02919-5,
06/57990-9, 2008/52389-0, 2011/01840-7.
*Correspondence to: Lilian Franco-Belussi, Departamento de
Biologia, Instituto de Biocie?ncias, Letras e Cie?ncias Exatas,
Universidade Estadual Paulista, Sa?o Jose? do Rio Preto, Sa?o
Paulo, 15054-000. Tel.: � 17 3221-2387. Fax: �17 32212390. E-mail: lilian.belussi@gmail.com
Received 9 April 2011; Accepted 5 September 2011
DOI 10.1002/ar.21524
Published online 20 December 2011 in Wiley Online Library
(wileyonlinelibrary.com).
VARIATION IN VISCERAL PIGMENTATION OF Scinax
visceral melanocytes is not well de?ned, our aim was to
describe the pigmentation on the organs? surface in three
species of genus Scinax in order to ?nd a pigmentation
pattern for these species.
MATERIAL AND METHODS
We analyzed 15 male specimens of each of the following species: Scinax similis, Scinax fuscovarius, and Scinax fuscomarginatus. The animals were collected in the
surroundings of Sa?o Jose? do Rio Preto (State of Sa?o
Paulo, Brazil) during their reproductive period (from October 2006 to March 2007). We also analyzed additional
specimens from the Amphibian Collection of the Department of Zoology and Botany (DZSJRP-Amphibia) housed
at the Sa?o Paulo State University (S. fuscomarginatus:
DZSJRP 7426, 7444-6, 7449, 7672, 7677, 7679-80, 7682;
S. fuscovarius: DZSJRP 6159-60, 6162-3, 6329-30, 8022,
8054, 8836, 8838; S. similis: DZSJRP 6782, 7954, 758892, 7594, 7596, 8051).
We followed the ethical guidelines of the Sa?o Paulo
State University campus Botucatu (Protocol #001/06CEEA), and the NIH Guide for Care and Use of Laboratory Animals. In the laboratory, we anesthetized and
euthanized the specimens by submersion in 20% ethanol. All specimens had the organs of the abdominal
cavity exposed by medial incision. We made the macroscopic
documentation under a stereomicroscope (Leica-MZ16),
using the software Image Manager 5.0 (Version 4.0.5, Media
Cybernetics, Bethesda, MD) to capture images.
We classi?ed the visceral pigment cells according to
the protocol proposed by Franco-Belussi et al. (2009),
based on differences in the intensity of pigmentation on
the gonads of anurans. This classi?cation is based on
the intensity of pigmentation, ranging from absence
(Category 0) to entirely pigmented, when an intense
black coloration is observed (Category 3 � maximal
intensity), with the categories 1 and 2 representing a
gradual increase in the intensity of pigmentation. We
applied this protocol of classi?cation to the following anatomical structures and regions of the specimens: (1)
pericardium and blood vessels at the basis of the heart;
(2) heart; (3) lungs; (4) stomach; (5) middle intestine; (6)
rectum; (7) intestinal mesentery; (8) kidney and renal
blood vessels; (9) testes; (10) fatty bodies; (11) urinary
bladder; (12) lumbar nerve plexus; and (13) lumbar parietal peritoneum.
To compare the differences among categories of pigmentation in each species in an organ or region, we used a G test
for goodness-of-?t, with Yates? correction (Sokal and Rohlf,
1995). This test was implemented using the code provided
by Peter Hurd available at http://www.psych.ualberta.ca/
p?hurd/cruft/g.test.r and run using the R software v. 2.11.1
(R Development Core Team, 2010). We adopted an alpha
level of 5% in all tests.
RESULTS
Visceral pigmentation occurs in organs and structures
of all organics systems (Figs. 1?4 and Table 1), and is
differentially distributed in each species analyzed. The
pigmentation on the pericardium and heart of S. fuscovarius differed from S. similis and S. fuscomarginatus
(pericardium: G � 32.57; df � 6; P < 0.0001; heart: G �
15.90; df � 6; P � 0.01; Figs. 1A, 2A, 3A, 4). All individ-
299
uals of S. fuscovarius had pigmentation on the pericardium
and cardiac blood vessels; 14 out of 15 individuals had a little pigmentation (category 1) in these regions and 1 out of
15 individuals had moderated pigmentation (category 2).
However, 12 out of 15 individuals of S. fucomarginatus had
no pigmentation in these regions, whereas 3 out of 15 individuals had a little pigmentation (category 1). In addition,
7 out of 15 individuals of S. similis showed no visceral melanocytes (category 0) on the pericardium, whereas 4 out of
15 had a little pigmentation (category 1) and 4 out of 15
individuals had moderated pigmentation (category 2). All
individuals of S. fuscomarginatus, 11 out of 15 of S. similis
and 10 out of 15 specimens of S. fucovarius had a little pigmentation (category 1) in the heart (Fig. 1A). However, 4
out of 15 individuals of S. similis and 1 out of 15 individuals of S. fucovarius had no visceral pigmentation (category
0) in these regions. Only 4 out of 15 specimens of S. fuscovarius had moderated pigmentation (category 2) on the
heart (Table 1).
We did not observe differences among species on the
lungs (G � 9.84; df � 6; P � 0.13; Fig. 4). All individuals
of S. fuscovarius had a little pigmentation (category 1)
in this region, similarly to what was found in 9 out of 15
specimens of S. similis and in 12 out of 15 individuals of
S. fuscomarginatus. However, 6 out of 15 individuals of
S. similis and 3 out of 15 of S. fuscomarginatus had no
pigmentation (category 0) on this organ (Figs. 1B, 2B,
3B; Table 1).
We observed no pigment cells on the stomach and middle intestine of all specimens of the three species analyzed (Figs. 1C, 2C?D, 3C). However, all specimens
presented pigmentation on the rectum (Fig. 1D, 3D), but
we did not observe signi?cant differences (G � 9.48; df
� 6; P � 0.15; Fig. 5). All individuals of S. fuscomarginatus and 10 out of 15 specimens of both S. similis and
S. fuscovarius had moderated pigmentation (category 2)
in these regions, while 5 out of 15 individuals of S. similis and S. fuscovarius had a few pigmented cells (category 1). On the intestinal mesentery, we also observed
differences among species (G � 37.95; df � 6; P <
0.0001) (Fig. 5). In S. fuscomarginatus, 10 out of 15 individuals had no pigmentation (category 0) in this region,
whereas 5 out of 15 had a few pigmented cells (category
1). However, all specimens of S. fuscovarius and S. similis were pigmented to some degree. On the mesentery,
13 out of 15 individuals of S. similis had a few pigmented cells (category 1) and 2 out of 15 had moderated
pigmentation (category 2), whereas 7 out of 15 individuals of S. fuscovarius had a little pigmentation (category
1) and 8 out of 15 had a moderated pigmentation (category 2; Table 1).
On the urogenital system, all species had no pigmentation (category 0) on the urinary bladder and fat bodies.
Accordingly, S. similis and S. fuscovarius had no pigmentation on the testes. However, the testes of all individuals of S. fuscomarginatus were pigmented to some
degree, and this difference was signi?cant (G � 57.29; df
� 6; P < 0.0001; Figs. 6, 7). Eight out of 15 individuals
of S. fuscomarginatus had a little pigmentation (category
1), 1 out of 15 individuals presented moderated pigmentation (category 2) and 6 out of 15 specimens had a large
amount of pigmentation (category 3). The pigmentation
was distinct among species (G � 49.90; df � 6; P <
0.0001) on the kidneys (Figs. 1E, 2E, 3E, 6). In S. similis, 1 out of 15 individuals had no pigmentation, whereas
300
FRANCO-BELUSSI ET AL.
Fig. 1. Organs and structures of the abdominal cavity of Scinax
fuscomarginatus. A and B: cardio-respiratory system. C and D:
Organs of the digestory system. E: urogenital system. F: Other regions
in which pigmentary cells were found. A � Adipose tissue; H � Heart;
I � Intestine; K � Kidney; L � Lung; Pl � Nerves of the lumbar plexus;
R � Rectum; S � Stomach; T � Testis; V � Vertebral column. Arrow:
pigmented cells and (*):drop-shaped pigmented cells.
10 out of 15 specimens had a few pigmented cells (category 1) and 4 out of 15 individuals presented moderated
pigmentation (category 2). In S. fuscomarginatus, 11 out
of 15 individuals had no pigmentation (category 0) on
the kidneys, whereas 4 out of 15 had a little pigmentation (category 1) in this organ. However, all individuals
of S. fucovarius were pigmented to some degree on the
kidneys, whereas 1 out of 15 individuals had a few
VARIATION IN VISCERAL PIGMENTATION OF Scinax
301
Fig. 2. Organs and structures of the abdominal cavity of Scinax
fuscovarius. A and B: cardio-respiratory system. C and D: Organs of
the digestory system. E: urogenital system. F: Other regions in which
pigmentary cells were found. Gb � Gall badder; H � Heart; I � Intes-
tine; K � Kidney; L � Lung; M � Mesenterium; Pl � Nerves of the
lumbar plexus; S � Stomach; V � Vertebral column. Arrow: pigmented
cells.
pigmented cells (category 1), 12 out of 15 had a moderated pigmentation (category 2) and 2 out of 15 specimens
had a high amount of pigmentation (category 3;
Table 1).
On the lumbar nerve plexus and associated parietal
peritoneum, the pattern of occurrence of pigmentation
was different among species (lumbar nerve plexus: G �
22.44; df � 6; P � 0.001; parietal peritoneum: G �
302
FRANCO-BELUSSI ET AL.
Fig. 3. Organs and structures of the abdominal cavity of Scinax similis. A and B: cardio-respiratory
system. C and D: Organs of the digestory system. E: urogenital system. F: Other regions in which pigmentary cells were found. H � Heart; I � Intestine; K � Kidney; L � Lung; Pl � Nerves of the lumbar
plexus; R � Rectum. Arrow: pigmented cells and (*): drop-shaped pigmented cells.
27.78; df � 6; P < 0.0001; Figs. 1F, 2F, 3F, 8). On the
lumbar nerve plexus, 6 out of 15 individuals of S. similis
had no pigmentation (category 0), whereas 4 out of 15
specimens had a few pigmented cells (category 1) and 5
out of 15 had moderated pigmentation (category 2). All
individuals of S. fuscovarius and S. fuscomarginatus
had pigmentation on the lumbar nerve plexus. In S. fuscovarius, 11 out of 15 individuals had a little
303
VARIATION IN VISCERAL PIGMENTATION OF Scinax
Fig. 4. Differences in categories of pigmentation in the cardio-respiratory system of Scinax similis, S. fuscovarius, and S. fuscomarginatus. Mean SE. Different letters represent statistical differences
among organs of species.
pigmentation (category 1) in this region, whereas 4 out
of 15 specimens had a moderated pigmentation (category
2). S. fuscomarginatus had a few pigmented cells in this
region, of which 14 out of 15 individuals had category 1,
whereas 1 out of 15 had a moderated pigmentation (category 2; Table 1). Pigmented cells on the lumbar nerve
plexus of S. similis and S. fuscomarginatus had a string
arrangement (Figs. 1F, 3F).
On the lumbar parietal peritoneum, 13 out of 15 individuals of S. similis had no pigmentation (category 0),
whereas 2 out of 15 specimens had a few pigmented cells
(category 1). In S. fuscomarginatus, the occurrence of
pigmented cells in the lumbar parietal peritoneum
followed a similar pattern, in which 13 out of 15 individuals had no pigmentation (category 0), whereas 3 out of
15 had a little pigmentation (category 1). However, only
1 out of 15 specimens of S. fucovarius had no pigmentation (category 0), whereas 13 out of 15 had a little
pigmentation (category 1), and 1 out of 15 had a moderated pigmentation (category 2; Table 1).
TABLE 1. Pattern of pigmentation in Scinax simils, S. fuscovarius, and S. fuscomarginatus
Categories
Organs and regions
Pericardium and blood vessels
Heart
Lung
Stomach
Intestine
Rectum
Intestinal mesenterium
Kidney and blood vessel
Testes
Fat bodies
Unirany bladder
Lumbar nerve plexus
Lumbar parietal peritonium
Species
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
S.
similis
fuscovarius
fuscomarginatus
similis
fuscovarius
fuscomarginatus
similis
fuscovarius
fuscomarginatus
similis
fuscovarius
fuscomarginatus
similis
fuscovarius
fuscomarginatus
similis
fuscovarius
fuscomarginatus
similis
fuscovarius
fuscomarginatus
similis
fuscovarius
fuscomarginatus
similis
fuscovarius
fuscomarginatus
similis
fuscovarius
fuscomarginatus
similis
fuscovarius
fuscomarginatus
similis
fuscovarius
fuscomarginatus
similis
fuscovarius
fuscomarginatus
Category 0
Category 1
Category 2
7
4
14
3
11
10
15
9
15
12
4
1
12
4
1
6
3
15
15
15
15
15
15
5
5
10
1
11
15
15
15
15
15
15
15
15
6
13
1
12
Category 3
4
10
10
15
2
8
0
4
12
2
8
1
6
4
11
14
2
13
3
5
4
1
0
1
0
13
7
5
10
1
4
304
FRANCO-BELUSSI ET AL.
Fig. 5. Differences in categories of pigmentation on the digestory
system of Scinax similis, S. fuscovarius, and S. fuscomarginatus.
Mean SE. Different letters represent statistical differences among
organs of species.
Fig. 6. Differences in categories of pigmentation on the urogenital
system of Scinax similis, S. fuscovarius, and S. fuscomarginatus.
Mean SE. Different letters represent statistical differences among
organs of species.
DISCUSSION
The three species of the genus Scinax had a different
pattern of visceral pigmentation. The main variations
were on the testes, in which S. similis and S. fuscovarius
had no pigmentation, whereas all individuals of S. fuscomarginatus presented some degree of pigmentation. An
intense black testicular pigmentation was also reported
for seven species of the family Leiuperidae (Physalaemus
cuvieri, P. olfersii, P. centralis, P. marmoratus, Eupemphix
nattereri, Pseudopaludicola cf. falcipes, and P. saltica;
Franco-Belussi et al., 2009), in which a large number of
pigmented cells occurs on the testicular interstitium associated with blood vessels (Oliveira and Zieri, 2005; Zieri
et al., 2007). The testicular pigmentation is related to the
neutralization of the effects of lipopolysaccharide, due the
bactericide role of melanin (Franco-Belussi and Oliveira,
in press). However, Moresco and Oliveira (2009) described
variation on this pigmentation during the breeding season in Rhinella schneideri, which could be related to
physiological modi?cations on this organ during an
intense testicular activity. However, some species do not
have pigmentation in this organ (e.g., Dendropsophus
nanus, D. minutus, D. sanborni, D. elianeae, Leptodactylus bokermanni, L. furnarius, L. fuscus, L. labyrinthicus,
L. mystaceus, L. mystacinus, L. latrans, L. podicipinus, L.
chaquensis, and L. notoaktites; Franco-Belussi et al.,
2009, 2011, Moresco and Oliveira, 2009). Therefore, these
?ndings demonstrated that the occurrence of visceral pigmentation varies among species and may be used as a
character in phylogenetic analysis, as conducted by Grant
et al. 2006.
The function of the visceral pigmentation is not clearly
de?ned yet (Gallone et al., 2002). However, some authors
(e.g., Zieri et al., 2007; Franco-Belussi et al., 2009) have
described visceral melanocytes closely related with blood
vessels in other organs and connective tissue membranes, such as the pericardium, intestinal mesentery,
and lumbosacral parietal peritoneum. However, FrancoBelussi and Oliveira (2011) reported an increase in the
pigmentation on the heart and kidneys in Eupemphix
nattereri following LPS administration, demonstrating
that melanocytes in these organs play a bactericidal
role.
In other regions, such as pericardium, stomach, intestine, rectum, nerves of the lumbar plexus, lumbosacral
parietal peritoneum, and mesentery, we observed a
differential occurrence of visceral pigmentation in the
species analyzed. The same pattern is reported by
Franco-Belussi et al. (2011) for the hylids D. nanus, D.
minutus, D. sanborni, and D. elianeae. However, the pigmentation in these organs does not vary in species of the
families Leiuperidae and Bufonidae during the reproductive period (Moresco and Oliveira, 2009). Therefore, the
pigmentation in these organs had apparently a phylogenetic constraint.
There was no pigmentation on the pericardium of S.
similis and S. fuscomarginatus. Similarly, to what was
reported by Franco-Belussi et al. (2011) for D. elianeae
and D. minutus. However, there was only a little pigmentation (category 1) in S. fuscovarius, similarly to the
reported by Franco-Belussi et al. (2011) for D. sanborni
and D. nanus, and Moresco and Oliveira (2009) for
Rhinella schneideri and Physalaemus cuvieri. Moresco
and Oliveira, (2009) also observed that there is no pigmentation (category 0) on the heart of R. schneideri and
P. cuvieri, similarly to the observed in D. minutus by
Franco-Belussi et al. (2011). However, on the heart of S.
similis, S. fuscovarius and S. fuscomarginatus a little
pigmentation (category 1) predominated, as in D. sanborni and D. elianeae (Franco-Belussi et al., 2011),
whereas in D. nanus a moderated pigmentation was
found (category 2; Franco-Belussi et al., 2011). There are
a few pigmented cells on the lungs of S. similis, S. fuscovarius, and S. fuscomarginatus, resembling that of D.
elianeae, D. nanus (Franco-Belussi et al., 2011) and P.
cuvieri at the beginning of the breeding season (Moresco
and Oliveira, 2009). The pigmentation in the latter species varies during the breeding season, being predominantly absent at the end of the season (Moresco and
Oliveira, 2009).
There was no pigmentation on the stomach and middle intestine of all individuals of the three species analyzed, a fact also observed by Moresco and Oliveira,
(2009) in R. schneideri and by Franco-Belussi et al.
(2011) in D. nanus, D. sanborni, and D. minutus.
VARIATION IN VISCERAL PIGMENTATION OF Scinax
305
Fig. 7. Variation in the pigmentation on testes of Scinax fuscovarius (A) and S. fucomarginatus (B, C,
and D). A: Absence of pigmentation on testes of S. fusocovarius. B: Testes of S. fuscomarginatus with a
few pigmentary cells (category 1). C: Moderated pigmentation (category 2). D: Intense pigmentation (category 3). Fb � Fat bodies; Sl � Spleen; T � Testis.
Fig. 8. Differences in categories of pigmentation on the lumbar
nerve plexus and associated parietal peritoneum of Scinax similis, S.
fuscovarius, and S. fuscomarginatus. Mean SE. Different letters represent statistical differences among the organs of species.
However, on the rectum of S. similis, S. fuscovarius, and
S. fuscomarginatus there is little (category 1) to moderate (category 2) pigmentation, whereas in D. minutus an
intense pigmentation is observed in this region (FrancoBelussi et al., 2011). In conclusion, the digestory system
for all species lacks pigmentation on the stomach and
intestine, whereas some pigmentation is observed on the
rectum.
The pigmentation varies on the kidneys, ranging from
absence (category 0) to an intense pigmentation (category 3). There is no pigmentation (category 0) in S. fuscomarginatus, as described for D. minutus (FrancoBelussi et al., 2011) and R. schneideri (Moresco and Oliveira, 2009). However, in S. similis there is a few pigmented cells (category 1), similar to the observed in D.
sanborni (Franco-Belussi et al., 2011). In S. fuscovarius,
there is moderated pigmentation (category 2), as
described for D. sanborni (Franco-Belussi et al., 2011).
This variation on renal pigmentation was also observed
in P. cuvieri during the reproductive cycle (Moresco and
Oliveira, 2009) and may be related to the breeding season of the species analyzed in this study.
306
FRANCO-BELUSSI ET AL.
We found a differential pattern of occurrence of visceral pigmentation in Scinax similis, S. fuscovarius, and
S. fuscomarginatus. The three species differed mainly in
the pigmentation on the testes. Speci?cally, only S. fuscomarginatus had varying degrees of pigmentation not
only on the testes but also on other organs. Visceral pigmentation may represent an intrinsic feature of a species, but also varies according to the age, nutritional,
and pathological status of the animal (Agius and
Agbede, 1984). In addition, low temperature increases
the amount of melanin and induces metabolic and structural changes in hepatic cells of Rana esculenta (Barni
et al., 1999). We believe that the visceral pigmentation
of some organs is phylogenetically constrained, since different families have different pigmentation patterns.
However, these cells seem to have speci?c functions,
such as protection against bacteria and damages caused
by high temperatures. Therefore, future experimental
studies testing the effects of temperature, photoperiod,
and infection should be conducted to describe the factors
that modify this pigmentation and the role of the visceral pigmentation.
ACKNOWLEDGEMENTS
The authors would like to thank Diogo Borges Provete
for critically reading the ?rst drafts of the manuscript
and helping with English and Juliana Ferreira Antoniassi for helping with the ?eldwork.
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species, genus, visceral, patterns, pigmentation, three, scinax, anurahylidaedistinct, morphological
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