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Morphological characterisation of the digestive tract of the catfish

Lophiosilurus alexandri Steindachner, 1876 (Siluriformes,
Pseudopimelodidae)

Article  in  Acta Zoologica · October 2017

DOI: 10.1111/azo.12224

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DOI: 10.1111/azo.12224

ORIGINAL ARTICLE

Morphological characterisation of the digestive tract of the

catfish Lophiosilurus alexandri Steindachner, 1876 (Siluriformes,
Pseudopimelodidae)

Gabriel C. G. Mello1  |  Marcella L. Santos1  |  Fábio P. Arantes1  |  Thiago C. Pessali2  | 

Marcelo F. G. Brito3  |  José E. Santos1,4

1
Programa de Pós-Graduação em Biologia
de Vertebrados da PUC Minas, Belo
Horizonte, MG, Brazil
2
Museu de Ciências Naturais da PUC
Minas, Belo Horizonte, MG, Brazil
3
Departamento de Biologia da
UFS, Laboratório de Ictiologia, Sergipe,
Brazil
4
Tutor PET Biologia PUC Minas, Belo
Horizonte, MG, Brazil
Correspondence
José Enemir dos Santos, Graduate Program
in Vertebrate Biology, Pontifical Catholic
University of Minas Gerais, Brazil, Belo
Horizonte, MG, Brazil.
Email: enemir@pucminas.br
Funding information
Fundação de Amparo à Pesquisa do Estado
de Minas Gerais; FIP PUC Minas
Abstract
The anatomical arrangement of the digestive tract and the length (cm) of the oe-
sophagus and intestine of the catfish Lophiosilurus alexandri were described, and the
intestinal coefficient was determined. L. alexandri oesophagus is short, in median
position, and presents longitudinally folded mucosa, whilst its epithelium is stratified
and non-­keratinised, with mucous, claviform and epithelial cells. Stomach has “C”
shape, with folded mucosa along cardiac region, disordered in the fundic region, and
directed to the sphincter in the pyloric region. Its epithelium is simple prismatic, and
cardiac and fundic portions have gastric glands. Cranial intestine is formed by py-
loric flexure and descending loop attached to the right side of stomach. Middle intes-
tine is winding and positioned to the right of caudal portion of stomach. Caudal
intestine is linear and with a median position up to the anus. Intestinal coefficient was
1.39 ± 0.30 cm. Epithelium is simple prismatic with brush border and contains epi-
thelial and goblet cells. Caudal region has highest concentration of goblet cells. Were
detected neutral glycoproteins, carboxylated and sulphated acid glycoconjugates for
mucous cells and goblet cells, and neutral glycoproteins for the apical region of gas-
tric epithelial cells. Morphological features could be related to piscivorous species
feeding habit.

KEYWORDS
catfish, intestinal coefficient, mucosa morphometry, mucosubstances

1  |   IN T RO D U C T ION Godinho, 2007; Melillo Filho et al., 2016). It is a carnivorous

The pacamã Lophiosilurus alexandri Steindachner, 1876 be-
longs to the Siluriformes order and Pseudopimelodidae fam-
ily and is native to the São Francisco River Basin, south-­east
Brazil (Shibatta, 2003). According to the IUCN (2017) list,
its conservation status is vulnerable. It reproduces naturally
in captivity, does not migrate for reproduction, builds nests on
a sandy bottom, exhibits parental care and has high commer-
cial value (Assega, Birindelli, Bialetzki, & Shibatta, 2016;
Barros, Guimarães-­ Cruz, Veloso-­ Júnior, & Santos, 2007;
fish with piscivorous tendencies, lurking on the sandy sub-
strate to catch other fish. The species was introduced into the
Doce River basin, south-­east Brazil, where it is well estab-
lished, being the fourth most important species for commer-
cial fishing in the region (Alves, Vieira, Magalhães, & Brito,
2007), and studies on its biology in this basin are extremely
scarce. Lophiosilurus alexandri is interesting for aquaculture,
and studies have been carried out recently aimed at the devel-
opment of its conservation and commercial farming, such as
Barros et al. (2007); Santos and Luz (2009); Guimarães-­Cruz,

© 2017 The Royal Swedish Academy of Sciences     1

Acta Zoologica. 2017;1–10. wileyonlinelibrary.com/journal/azo |
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2       MELLO et al.
Santos, Sato, and Veloso-­ Junior (2009); Mello, Santos,
Guimarães-­Cruz, Godinho, and Godinho (2015); Cordeiro
et al. (2016). The structure of the digestive tract of teleost var-
ies with different factors, and its functions include digestion,
nutriments absorption, hormone secretion and immune pro-
tection. Its structure is also variable according to the nature
of the diet. Rather short in carnivorous species (20% of body
length), the digestive tract is long (20 times the body length)
in herbivorous fish. It comprises distinct portions: the mouth
cavity, the oesophagus, the stomach (some fishes are stom-
achless), the anterior and posterior intestine and the rectum
(Banan Khojasteh, 2012). The digestive tract of fishes shows
a remarkable diversity of morphological and functional char-
acteristics, been associated with different feeding habits and
to taxonomy, as well as to body shape and weight, size and
sex (Banan Khojasteh, Sheikhzadeh, Mohammadnejad, &
Azami, 2009; Diaz, Gracia, & Goldemberg, 2008; Kapoor,
Smith, & Verighina, 1975). The digestive tract of fish is a
widely studied topic, from the classic works of Al-­Hussaini
(1949); Angelescu and Gneri (1949) to recent works, such
as Germano et al. (2013); Santos, Arantes, Santiago, and
Santos (2015), Santos, Arantes, Pessali, and Santos (2015);
Fagundes, Rotundo, and Mari (2016); Andrade, Guimarães,
Rotundo, and Mari (2017). These studies provide crucial
information for the cultivation and conservation of species
(Santos, Arantes, Santiago et al., 2015; Wilson & Castro,
2011). Therefore, the aim of our work was to describe the
anatomical and histological characteristics of the oesopha-
gus, stomach, and intestine of the L. alexandri, relating these
characteristics to its eating habits and expand their biological
knowledge to improve conservation programmes.
2  |  M AT E R IA L A N D ME T H O DS
Thirty specimens of L. alexandri were collected from the
Doce River (19°02′15″S and 42°08′11″W), south-­eastern
Brazil, between November 2013 and August 2014. Sampling
was conducted using gillnets with mesh sizes of 8–20 cm
between opposite knots. Thirty specimens, 17 females and
13 males (standard length 44.6 ± 10.4 cm; standart weight
2,058 ± 1,267 g) in good condition of health were fixed in
10% formalin for 12 hours and transferred to 70% ethanol,
which were then used for morphometric and anatomical
study. Fragments from different regions of the digestive
tract of ten other specimens were taken for histological
study and statistical analysis. The handling of the speci-
mens followed the guidelines of the National Council for
the Control of Animal Experimentation (CONCEA) for eu-
thanising animals (Brazil, 2013) and CEUA PUC Minas
(003/2016), and the fish collection was authorised by the
State Forest Institute of Minas Gerais (IEF – licenses 086-­
08). Voucher specimens are deposited in the fish collection
housed in the Museu de Ciências Naturais, Pontifícia
Universidade Católica de Minas Gerais, Belo Horizonte
(MCNIP-­0116).
Morphometry: For each specimen, the standard length
(SL; cm), body weight (g) and intestine length (CI, mm)
were recorded. The digestive tract was dissected for anal-
ysis of the mucosa and the anatomical relationship of the
oesophagus, stomach, intestines. Subsequently, the intes-
tinal coefficient (CO) was calculated using the equation:
CO = CI/SL, according to Angelescu and Gneri (1949). To
measure the intestines, a tape measure (MACROLIFE) was
used to measure length and flexure. The results are given
as mean and standard deviation (M ± SD). All structures
were analysed using an Olympus SZ-­11 stereomicroscope.
To the intestinal mucosa, the height and width (μm) of mu-
cous folds and the thickness (μm) of the muscle layer of
the cranial, middle and caudal regions of the intestine were
determined by analysis of histological slides prepared from
ten individuals. The number of goblet cells in a 250 μm
length from the mucosa folds of the cranial, middle and
caudal intestines, extending up to the villi, was determined.
Ten slides from each region were made, and twenty random
measurement replicates from each slide were taken. The
results referring to the number of goblet cells are given as
mean and standard deviation (M ± SD). From scanned im-
ages, measurements were performed using the free ImageJ
software. To determine whether there were differences in
the number of goblet cells between the three intestinal re-
gions, we used the arithmetic mean of the measurement rep-
licates, according to Jaroszewska, Dabrowski, Wilczynska,
and Kakareko (2008).
Light microscopy: Fragments of the oesophagus, stom-
ach (cardiac, fundic and pyloric regions), intestine (cranial,
middle and caudal sections) were fixed in Bouin’s fluid for
six hours and submitted to routine histological technique, and
sections were stained with haematoxylin–eosin (HE) or sub-
mitted to histochemical assays. Some sections were used for
carbohydrate and protein analysis, following Pearse (1985):
periodic acid-­Schiff (PAS) for carbohydrates with 1:2 glycol
groups; glycogen, neutral glycoproteins and sialomucin; al-
cian blue pH 2.5 (Ab pH 2.5) for carboxylated and sulphated
glycoconjugate acids including sialomucines, alcian blue pH
0.5 (Ab pH 0.5) for sulphated glycoconjugates.
Statistical analysis: Appropriate statistical analysis was
conducted using the Lilliefors test of normality and we used
M ± SD. Data with normal distribution were compared using
analysis of variance for a randomised block design (RBD
ANOVA), where the blocks were the individuals and the
treatment was the intestinal regions. Post hoc (Tukey) tests
were performed when the ANOVA indicated a significant
difference between treatments or between blocks to detect the
difference between the means. All analyses were performed
using the BioStat 5.0 package (p < .05).
MELLO et al.   
|
   3

3  |   R E S U LTS
3.1  |  Oesophagus: anatomy and histology
The average length of the oesophagus was 3.1 ± 0.8 cm,
being considered short. It had a median position and the
mucosa layer contained longitudinal folds throughout its
length (Figure 1). The oesophagus was organised in the fol-
lowing layers: mucosa with epithelium plus lamina propria,
submucosa with stratum compactum and stratum laxum, in-
ternal and external muscular layer, and serosa (Figure 2a).
The mucosa layer consisted of stratified non-­ keratinised
squamous epithelium which presented three types of cells:
claviform, epithelial and mucous (Figure 2b). The claviform
cells were the largest ones, with a dense and central nucleus,
and their cytoplasm was acidophilus. They were supported
in the stratum compactum of the lamina propria and formed
disorganised strata. Epithelial cells were present in different
layers in the epithelium tissue and were cubical at the base
and squamous at the apex. They had a central, dense nucleus
and scant cytoplasm. The mucous cells were arranged at the
apex of the epithelium and presented a basal nucleus and
cytoplasm with neutral glycoproteins, glycoconjugates car-
boxylated and glycoconjugates sulphated acids. Taste buds
were not observed in the cranial region of the mucosa. The
lamina propria-­submucosa consisted of two strata: stratum
compactum and stratum laxum. The stratum compactum con-
sisted of dense connective tissue formed by densely packed
layers of collagen fibres, blood vessels and dispersed strata
of smooth muscle. The stratum laxum was thicker, located
below the stratum compactum and consisted of loose connec- F I G U R E   1   Anatomical view of the digestive tract in the
tive tissue, collagen fibres and blood vessels. The muscular coelomic cavity with mesoscopic details of the mucosa indicated in
layer consisted of two striated muscle sublayers. The inner longitudinal sections: Segments of the digestive tract: oesophagus (O),
layer was longitudinally orientated, and muscle packages de- cardiac stomach (CS), fundic stomach (FS), pyloric stomach (PS),
cranial intestine (CRI), middle intestine (MI) and caudal intestine
limited by connective tissue were observed, whilst the outer
(CDI). Bar = 1 cm. Side inserts: (O) mucosa of the oesophagus
layer is circularly orientated circular and has continuous bun-
longitudinally folded. Bar = 2 mm. (CS) mucosa of the cardiac stomach
dles of fibres. The serosa was the outermost layer, consisting
with longitudinal and transverse folds. Bar = 2 mm. (FS) mucosa of the
of dense connective tissue and involved by the mesothelium. fundic stomach with disorganised folds. Bar = 2 mm. (PS) Mucosa of
The transition between oesophageal and stomach mucosa the pyloric stomach with folds oriented towards the pyloric sphincter.
was characterised by the change from non-­keratinized squa- (CRI) mucosa of the cranial intestine with longitudinal primary folds
mous epithelium to simple cubic epithelium and the presence and oblique secondary folds, in a network arrangement. Bar = 1 mm.
of gastric glands in the lamina propria (Figure 2c). (MI) mucosa of the middle intestine with longitudinal primary folds
and oblique secondary folds, in a network arrangement. Bar = 1 mm.
(CDI) mucosa of the caudal intestine with large and spaced longitudinal
3.2  |  Stomach: anatomy and histology primary folds and scarce secondary folds. Bar = 1 mm [Colour figure
The stomach, when empty, had a “C” shape, with cardiac, can be viewed at wileyonlinelibrary.com]
fundic and pyloric regions (Fig. 1). It communicated with the
oesophagus through the cardiac region and with the intestine cardiac, fundic and pyloric regions differ from each other
through the pyloric region. The cardiac region was tubular, in the organisation of the mucosa and the absence of gastric
cranial and median and had transverse folds separated by glands in the pyloric region (Figure 2e). The stomach was
larger longitudinal folds. The fundic region was saculiform, organised into mucosa, submucosa, internal and external
caudal, median and with disordered folds. The pyloric region muscular, and serosa layers (Figure 2d). The gastric mucosa
was tapered and located on the left side of the coelomic cav- layer presented simple prismatic epithelium with epithelial
ity, with folds oriented towards the pyloric sphincter. The cells showing an oval and basal nucleus with accumulation of
 |
4       MELLO et al.
neutral glycoproteins in the apex of the cell. The lamina pro-
pria consisted of connective tissue and gastric glands only in
the cardiac and fundic regions. The gastric crypts communi-
cated with the gastric glands in the lamina propria. Thin and
discontinuous bundles of smooth muscle were observed in
the lamina propria below the gastric glands, but they did not
form a defined muscular layer of the mucosa. The submucosa
layer presented a layer of loose connective tissue with col-
lagen fibres, thicker than the lamina propria, and blood ves-
sels. The muscular layer contained two sublayers of smooth
muscle. The orientation of the inner layer was circular, and
the outer layer was longitudinal. The serosa layer consisted
of dense connective tissue and blood vessels and externally
presented a layer of mesothelium squamous cells. The py-
loric region had a thin lamina propria with dense connective
F I G U R E   2   Histological cross
sections of the oesophagus and stomach of
pacamã. (a) Layers of the oesophagus wall
showing mucosa (m), stratum compactum
(sc), stratum laxum (sl), internal muscular
layer (ime), external muscle layer (eme),
serosa (s). HE. (b) Epithelium consisting
of mucosal cells (arrow head), claviform
cells (arrow) and stratum compactum (sc).
HE. (c) Transition from the oesophageal
epithelium (O) to the stomach epithelium
(S), gastric glands of the stomach (gg).
PAS. (d) Layers of the cardiac stomach
walls showing mucosa (m), gastric glands
(gg), submucosa (sm), internal muscular
layer (imc), external muscle layer (emc)
and serosa (s). HE. (e) Layers of the
pyloric stomach wall showing mucosa
(m), submucosa (sm), internal muscular
layer (imc), external muscle layer (emc)
and serosa(s). HE. (a, d-­e) bars = 400 μm;
B bar = 50 μm; C bar = 100 μm [Colour
figure can be viewed at wileyonlinelibrary.
com]
tissue. The submucosa was thick and consisted of loose con-
nective tissue. The pyloric sphincter consisted of the thicken-
ing of the inner muscle layer.
3.3  |  Intestine: anatomy and histology
The intestine of pacamã had 62.3 ± 19.5 cm in length and
showed an intestinal coefficient of 1.39 ± 0.30. The intestine
was divided into cranial (23,9%), middle (70,7%) and caudal
(5,4%) parts, according to the anatomical and morphologi-
cal organisation (Figure 1), histologically showed four folds:
mucosa, submucosa, muscular and serosa layers. The cranial
intestine was formed by pyloric flexure, which was ventral to
the oesophagus and by the descending loop that runs attached
to the right side of the stomach. The middle intestine was
MELLO et al.   
|
   5

convoluted, with many folds and it remained to the right of
the caudal portion of the stomach. The caudal intestine was
linear and positioned medially in the coelomic cavity until
the anal opening. The mucosa of the cranial and middle in-
testine showed primary and secondary folds longitudinally
oriented and secondary folds obliquely oriented, forming a
network. The mucosa of the caudal intestine had a less devel-
oped network and exhibited pleated primary folds longitudi-
nally oriented. In the specimens, examined pyloric caeca are
not observed. The intestine segments showed lamina propria-­
submucosa consisting of a dense connective tissue layer and
blood vessels, accompanying the folds of the mucosa. The
muscular layer consisted of two smooth muscle sublayers,
the internal one with circular orientation and the external one
with longitudinal orientation. The serosa layer consisted of
dense connective tissue surrounded by a layer of mesothelial
squamous cells and blood vessels (Figure 3a). The mucosa
layer of the epithelium of the three segments of the intestine
was simple, prismatic with brush border with epithelial gob-
let cells supported by the lamina propria. The goblet cells had
cytoplasm filled with mucosubstances and were interspersed
between the epithelial cells. Intra-­ epithelial lymphocytes
were observed between the epithelial cells (Figure 3b). The
epithelial cells had a basal, spherical and vesicular nucleus
and abundant cytoplasm. The intestinal folds of the cranial
and middle regions were significantly taller and thinner than
those of the caudal region (p < .05). The muscular layer of
the caudal region was thicker than that of the cranial and
middle regions, and the cranial was higher than the average.
Statistically, they were different from each other (p < .05).
The caudal region of the intestine had a significantly higher
concentrations of goblet cells compared to the cranial and
middle regions (p < .05) (Figure 3c-­e). The mean number of
goblet cells was calculated by each 250 μm of tissue to each
intestinal region, being 14.0 ± 2.5 to cranial, 10.5 ± 1.9 to
middle and 20.6 ± 4.0 to caudal region (Figure 4).
3.4  |  Histochemical analysis
By histochemical analysis, we detected neutral glycoproteins
and carboxylated and sulphated acid glycoconjugates for the
mucous and goblet cells and neutral glycoproteins for the api-
cal region of gastric epithelial cells (Table 1).
4  |  DISCUSSION
Most teleosts have a short oesophagus, including Leporinus
macrocephalus (Rodrigues, Navarro, & Menin, 2008),
Salminus brasiliensis (Rodrigues & Menin, 2008) and L. al-
exandri. However, the oesophagus can also be long, as ob-
served in Gymnotus carapo (Menin, 1989). In pacamã, the
longitudinal folds of the oesophageal mucosa were like
those of other Siluriformes (Jaroszewska et al., 2008; Raji
& Norouzi, 2010) and this adaptation can be related to the
stretching capacity of its wall, which is a feature of piscivo-
rous species. The oesophagus of fish can present two types
of epithelium: stratified, as in Glyptosternum maculatum

F I G U R E   3   Cross sections of the

cranial, middle and caudal intestine: (a)
Layers of the cranial intestine wall showing
mucosa (m), lamina propria-­submucosa
(lp), internal muscular layer (imc), external
muscle layer (emc) and serosa (s). HE.
(b) Epithelium of the caudal intestine with
epithelial cells (arrow head) and intra-­
epithelial lymphocytes (red arrow), lamina
propria-­submucosa (lp) and the brush
border (br). HE. Bar = (c) Epithelium of
the cranial intestine showing goblet cells
(black arrow). PAS. (d Epithelium of the
middle intestine showing goblet cells (black
arrow). PAS. Bar = 20 μm. (e) Epithelium
of the caudal intestine showing goblet cells
(black arrow). PAS. A Bar = 400 μm; B-­E
bars = 20 μm [Colour figure can be viewed
at wileyonlinelibrary.com]
 |
6       MELLO et al.
(a) (b) (c)
(d)
F I G U R E   4   Histochemistry cross sections of the oesophagus
and stomach of pacamã. (a) Epithelium with mucosal cells reactive
to histochemistry with Ab pH 2.5 (arrowhead). (b) Epithelium with
mucous cells reactive to histochemistry Ab pH 0.5 (arrowhead). (c)
Epithelium with mucosal cells reactive to histochemistry with Ab
pH 2.5 +  PAS. (arrowhead). (d) Transition from the oesophagus
epithelium (esf) to the epithelium of the stomach (est). Arrowhead =
mucous cells of the oesophagus; gg = gastric glands of the stomach,
with PAS + H. Ab = alcian blue; PAS = periodic acid-­schiff. A-­C
bars = 50 μm; D bar = 100 μm [Colour figure can be viewed at
wileyonlinelibrary.com]
(Xiong et al., 2011), and pseudostratified in L. alexan-
dri, as in Leporinus taeniofasciatus (Albrecht, Ferreira, &
Caramaschi, 2001). These epithelial variations may be re-
lated to the feeding habits of the species and provide protec-
tion from food abrasion.
Several authors have reported the presence of taste buds
in the cranial portion of fish oesophagus (Jaroszewska
et al., 2008; Santos, Arantes, Pessali et al., 2015; Xiong
et al., 2011). The absence of taste buds in the oesophagus
of the pacamã, as well as in Odontesthes bonariensis, (Diaz,
Escalantes, Garcia, & Goldemberg, 2006), Clarias batrachus
and Serrasalmus nattereri (Raji & Norouzi, 2010), suggests
T A B L E   1   Histochemistry characteristics of secretion present in
digestive tract
Prismatic
Histochemistry Mucous cells cells Goblet cells
Periodic acid-­ + + +
schiff (PAS)
Alcian blue pH 2.5 + − +
Alcian blue pH 0.5 ± − ±
(+) positive reaction; (±) weak positive reaction; (−) negative reaction.
that food selection is performed in the oral cavity after prey
capture (Albrecht et al., 2001).
The presence of claviform cells in the epithelium of
the pacamã oesophagus has also been described for other
Siluriformes, such as Trichomycterus brasiliensis (Ribeiro &
Fanta, 2000). The function of the claviform cells still not well
understood. Some authors suggest that these cells are related
to the globular epidermal cells that are responsible for the
alarm chemistry, and take part in digestion, as well as hav-
ing immunological, cellular regeneration and healing func-
tions (Alexander & Ingram, 1992; Al-­Hassan, Thomson, &
Oriddle, 1983; Nakamura, Watanabe, Kamiya, & Muramoto,
2001; Perillo, Pace, Seilhamer, & Baum, 1995). The oesoph-
ageal epithelium in teleosts presents mucous cells throughout
its length (Al-­Abdulhadi, 2005; Marchetti et al., 2006; Park
& Kim, 2001; Raji & Norouzi, 2010; Xiong et al., 2011). In
our study, L. alexandri presented mucous cells with acidic
and neutral glycoconjugate synthesis. This can provide pro-
tection against injuries caused by mechanical damage, as well
as facilitating the swallowing of food and aiding in digestion.
The stomach of fishes is divided into many categories
depending on their shape: (i) no stomach as in Cryprinids
and Labrids; (ii) J-­shape in African and American catfish;
(iii) straight with enlarged lumen in pike; (iv) channel catfish
and halibut; (v) U-­shaped in salmonide; and (vi) Y-­shaped in
tilapia (Moawada, Awaadb, & Tawfiekb, 2017). The anatom-
ical shape of the pacamã stomach differs from that of most
teleosts due to its “C” shape, whilst most studies report a
“U” shape (Andrade et al., 2017; Cao & Wang, 2009; Xiong
et al., 2011), “J” shape (Sis, Ives, Jones, Lewis, & Haensly,
1979) and “Y” shape (Rodrigues & Menin, 2008). The latter
two authors suggest that the different anatomical shapes of
fish stomachs may be related to different eating habits, but
the anatomical shape may well be related to phylogeny, as
there are no conclusive studies. The stomachs of other fish
have been divided into cardiac, fundic and pyloric regions,
like that of pacamã (Cao & Wang, 2009; Raji & Norouzi,
2010; Santos, Arantes, Santiago et al., 2015). This anatom-
ical division may be a characteristic of teleosts that have a
true stomach and indicates the specialisation of regions of the
stomach for gastric secretion, maceration, homogenisation
MELLO et al.
and guidance of food. The pattern of the folds of the stomach
mucosa of the pacamã is defined by the shape and function
of the region and differs from other fish which have longitu-
dinal folds in the three regions of the stomach, such as in the
species studied by Scocco, Ceccarelli, and Menghi (1996). In
the pacamã, the folds of the cardiac region were related to the
movement of food from the oesophagus to the fundic portion
of the stomach and the stretching capacity of the region. The
disorganised folds of the fundic region were related to the
saculiform shape and the stretching capacity of the stomach
for food storage. The fundic portion presented folds directed
to the sphincter, which facilitates the passage of food from
the stomach to the intestine. The simple columnar epithelium
of the stomach is a common characteristic of teleosts (Al-­
Abdulhadi, 2005; Raji & Norouzi, 2010; Xiong et al., 2011).
The synthesis of neutral glycoproteins in the apical por-
tion of the stomach cells has been reported by several authors
(Al-­Abdulhadi, 2005; Albrecht et al., 2001; Raji & Norouzi,
2010; Ribeiro & Fanta, 2000) and can be related to the pro-
tection of the gastric epithelium against the action of secreted
acids and enzymes, as well as increasing mucous viscosity.
The presence of crypts associated with tubular gastric glands
in the cardiac and fundic regions and the absence in the py-
loric region are a feature of fish stomachs (Al-­Abdulhadi,
2005; Albrecht et al., 2001; Marchetti et al., 2006; Xiong
et al., 2011). In contrast, Raji and Norouzi (2010) only re-
ported a reduced concentration of gastric glands in the py-
loric region, suggesting that the pyloric region acts mainly
to direct food towards the intestine. The layers of connective
tissue of the lamina propria and submucosa are developed
and thick in the stomach of carnivorous Siluriformes (Cao
& Wang, 2009; Ribeiro & Fanta, 2000; Xiong et al., 2011).
The thick layer of connective tissue observed in L. alexandri
allows the organ to expand, which permits the intake of a
large amount of food.
In teleost fishes, the length of the intestine provides a
good gauge on their feeding. Behaviour being longer in ilio-
phagous, omnivorous and herbivorous species, and shorter in
insectivorous and carnivorous species (Canan, Nascimento,
Silva, & Chellappa, 2012; Machado et al., 2013). The in-
testinal coefficient of L. alexandri is relatively low (1.3)
and falls within the range expected for carnivorous fishes
(0.2–2.5). On the other hand, the intestinal coefficient of pa-
camã was higher than that of other carnivorous Siluriformes.
In Pseudoplatystoma fasciatum, the coefficient ranges from
0.68 to 0.84 (Rodrigues et al., 2009) and in G. maculatum,
the coefficient is 0.89 (Xiong et al., 2011). Another thirteen
carnivorous teleosts studied by Carrassón and Matallanas
(1994) showed an intestinal coefficient lower than that of
pacamã, ranging from 0.27 to 0.90. Furthermore, the intes-
tinal coefficient of the pacamã was close to that of the om-
nivorous Characiforms L. friderici and L. taeniofasciatus
(Albrecht et al., 2001) and higher than that of the omnivorous
  
   7
|
P. maculatus, whose coefficient ranged from 0.4 to 1.1
(Godinho, 1967). The length of the intestine is used as a
trophic-­level morphological indicator in nutritional ecology
(Horn, 1997). However, intestinal length is influenced by sev-
eral factors other than the diet, including fish size, body shape,
recent feeding history, ontogeny and phylogeny (Clements &
Raubenheimer, 2005; Horn, 1997). Although Seixas-­Filho
et al. (2001) have described four regions in the intestine of
the Siluriformes Ictalurus punctatus and Pseudoplatystoma
corruscans, other authors mentioned only three regions for
Siluriformes (Cao & Wang, 2009; Raji & Norouzi, 2010;
Rodrigues et al., 2009; Xiong et al., 2011). The convolution
of middle intestine of pacamã has also been observed in other
Siluriformes, such as P. fasciatum (Rodrigues et al., 2009),
and less convolution in and G. maculatum (Xiong et al.,
2011). These anatomical variations may occur among species
to allow for greater food plasticity. Pyloric caeca have been
reported in several species of teleosts (Albrecht et al., 2001;
Nachi et al., 1998; Seixas-­Filho et al., 2001). However, this
structure was not identified in the pacamã intestine, which
is like that of 65 other Siluriformes species (Cao & Wang,
2009; Raji & Norouzi, 2010; Rodrigues et al., 2009; Xiong
et al., 2011), possibly indicating the absence of such structure
for fish of the Siluriformes order.
The intestinal folds of pacamã were similar to those of the
Siluriformes P. maculatus (Godinho, 1967), differing only by
a “zig-­zag” arrangement in the cranial region of the P. mac-
ulatus intestine. They are different than the complex mor-
phology of L. macrocephalus (Rodrigues et al., 2008), which
exhibits longitudinal folds in the first loop, transverse in the
second and an oblique “V” in the third loop of the posterior
intestine. The morphology of the intestinal mucosa folds has
been associated with feeding habits (Rodrigues et al., 2008),
as they can increase the absorption area, as well as influence
the velocity of bolus transport. The results of our study were
similar to those of Cao and Wang (2009) who, through mor-
phometry of the intestinal folds, observed a decrease in height
of the folds in the caudal region. The intestine epithelium in
teleosts is the simple, columnar type. It presents epithelial
cells with a brush border interspersed by goblet cells (Banan
Khojasteh et al., 2009; Morrison & Wright, 1999; Ribeiro &
Fanta, 2000). In L. alexandri, it is suggested that mucosub-
stances in the goblet cells can be associated with the lubri-
cation of the intestinal mucosa which facilitates transport of
food macromolecules. The concentration of goblet cells in
the caudal region is associated with the need of greater pro-
tection of the mucosa and to increase its viscosity for faecal
expulsion.
Due to the absence of the muscularis mucosa in the intes-
tine of pacamã, it was impossible to differentiate the lamina
propria and submucosa, like other teleosts studied by Albrecht
et al. (2001) and Xiong et al. (2011). The orientation of the
smooth muscle layers of the pacamã intestine was similar
 |
8       MELLO et al.
to the teleosts studied by Ribeiro and Fanta (2000) and Cao
and Wang (2009). Besides pacamã, other Silurifomes exhib-
ited thickening of the muscular layer in the caudal intestine,
such as T. brasiliensis (Ribeiro & Fanta, 2000), P. fasciatum
(Rodrigues et al., 2009) and G. maculatum (Xiong et al.,
2011). The increase in thickness of the muscular layer in the
caudal intestine may also be related to the expulsion of the
faecal matter.
In summary, the oesophagus is similar to the descriptions
for other species of Siluriformes, the stomach differs from
most teleosts by having a “C” anatomical shape and histo-
logically similar to most Siluriformes. The intestine had a
greater intestinal coefficient than that proposed for fish with
similar piscivorous eating habits, but its morphology was like
other Siluriformes. The mucosubstances synthesised by the
mucosa, gastric epithelial, and goblet cells have the same
chemical nature of other teleosts. This study provides import-
ant information for breeding and conservation of L. alexan-
dri, as this species is considered vulnerable and is important
for commercial fishing.
ACKNOWLEDGEMENTS
The authors wish to thank FAPEMIG and FIP PUC Minas for
their financial support, Rubens Miranda and Rogério Matos
for preparing the histological slides.
ORCID
José E. Santos  http://orcid.org/0000-0002-5238-2173
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How to cite this article: Mello GCG, Santos ML,
Arantes FP, Pessali TC, Brito MFG, Santos JE.
Morphological characterisation of the digestive
tract of the catfish Lophiosilurus alexandri
Steindachner, 1876 (Siluriformes,
Pseudopimelodidae). Acta Zool. 2017;00:1–10.
https://doi.org/10.1111/azo.12224

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