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Gastrointestinal Tract and Accessory Organs in the
Spotted Bent-toed Gecko, Cyrtodactylus peguensis
(Boulenger, 1893): A Histological and
Histochemical Study
Lamai Thongboon1Sinlapachai Senarat2Jes Kettratad2Wannee Jiraungkoorskul3
Sansareeya Wangkulangkul1Pisit Poolprasert4Chamnan Para5Gen Kaneko6
Theerakamol Pengsakul7
1Department of Biology, Faculty of Science, Prince of Songkla
University, Songkhla, Thailand
2Department of Marine Science, Faculty of Science, Chulalongkorn
University, Bangkok, Thailand
3Department of Pathobiology, Faculty of Science, Mahidol University,
Bangkok, Thailand
4Program of Biology, Faculty of Science and Technology,
Pibulsongkram Rajabhat University, Phitsanulok, Thailand
5Department of Western Languages and Linguistics, Faculty of
Humanities and Social Sciences, Mahasarakham Universit y, Thailand
6School of Arts and Sciences, University of Houston –Victoria,
Texas, United States
7Faculty of Medical Technology, Prince of Songkla University,
Songkhla, Thailand
JMorpholSci
Address for correspondence Sinlapachai Senarat, PhD, Department
of Marine Science, Faculty of Science, Chulalongkorn University,
Bangkok, 10330, Thailand (e-mail: Senarat.S@hotmail.com).
Keywords
►digestive region
►glycoprotein
►gecko reptile
►liver
►Thailand
Abstract The spotted bent-toed gecko Cyrtodactylus peguensis is one of the exploited reptiles in
Thailand. In order to provide basic information for the digestive system of this species,
we have examined histologically the gastrointestinal and accessory organs of
C. peguensis using routine methods. The gastrointestinal region of this reptile started
from the stomach and the intestine. The stomach was separated into fundic and pyloric
regions. In both regions, the stomach wall was formed by four distinct tissue layers,
including mucosa, submucosa, muscularis, and serosa layers. Mucous neck cells and
oxynticopeptic cells were identified as glycoprotein-producing cells in the stomach by
Periodic acid-Schiff (PAS) staining. The small and large intestines shared many
histological characteristics, but the former contained more intestinal folds, while
the latter had more PAS-positive goblet cells. Histological characteristics of accessory
organs, liver and pancreas, were also provided. Overall, the gastrointestinal and
accessory organs of C. peguensis were largely similar to those from other reptiles,
but fine structural information will open up considerable opportunities to further
studies related to the endocrinology, the physiology, and the conservation of this
species.
received
April 27, 2019
accepted
May 1, 2019
DOI https://doi.org/
10.1055/s-0039-1693021.
ISSN 2177-0298.
Copyright © by Thieme Revinter
Publicações Ltda, Rio de Janeiro, Brazil
THIEME
Original Article
Published online: 08.08.2019
Introduction
The genus Cyrtodactylus (Gray, 1,827) is the most species-rich
genus of the gekkotan lizard,1but it is distributed in geogra-
phically restricted area of Southeastern Asia. Among >200
species in this genus, 17 species are considered to have
appeared recently in areas of Myanmar,2,3 of Vietnam4,5 and
of Thailand.6The spotted bent-toed gecko Cyrtodactylus
peguensis is one of the new species that is estimated to have
diverged in the Neogene.7They usually live in dry evergreen
and peninsular monsoonal evergreen forests in western and
peninsular areas of Thailand.8Unfortunately, C. peguensis is
continuously captured for ornamental purposes due to their
scarcity value and attractive skin colors. The exploitation and
habitat lossresulted in a population decline of C. peguensis, and
this species is now listed on Appendix III of the Convention on
International Trade in Endangered Species (CITES) and as a
protected species in Thailand.9
Although evolutionary relationships have been estab-
lished for this genus taking advantage of molecular
approaches,7there is a lack of morphology-based studies,
which can provide valuable information about its biological
characteristics. In particular, the morphology and histologi-
cal features of the digestive system, such as the stomach10
and intestines,11 are of great importance to understand their
eating habits and the diet diversity, which cannot be directly
derived from molecular in form ation. In the present study, we
aim to provide a basic description of the gross morphology
and histological features of the gastrointestinal tract and of
its accessory organs to gain in-depth insight into the feeding
ecology of C. peguensis. Our contribution could be of use for
further st udies related to the pathology and the physiology of
this species, as well as reptile studies from comparative and
evolutionary perspectives.
Materials and Methods
Preserved adult specimens of C. peguensis (n¼5; PSUZC-
REP727, PSUZC-REP154, PSUZC-REP192, PSUZC-REP586, and
PSUZC-REP90) were obtained from the National Museum of
Department of Biology, Prince of Songkla University,
Thailand. All of the specimens were collected from Southern
Thailand (Surat Thani, Nakhon Si Thammarat, and Trang
provinces). Owing to the unique manner in which these
specimens were obtained, ethical approval was not required
for the present study. The snout-vent length (SVL) was first
determined for all of the specimens. The digestive tract,
along with its accessory organs, was then longitudinally
dissected out and observed for their anatomical features at
the macroscopic level. The total length of the small and large
intestines was also determined. All of the digestive tract,
except for the esophagus, was subsequently subjected to the
standard histological analyses.12,13 Briefly, using a manual
rotating microtome, paraffin blocks were cut at 4 µm thick-
ness and stained with Harris hematoxylin and eosin (H&E) to
study the basic digestive structure. Periodic acid-Schiff (PAS)
staining was also employed to detect glycoprotein produc-
tion in the mucus-secreting cells.12,13 These histological
sections were obser ved and photomic rographed using a light
microscope equipped with a TE750-Ua digital camera (Bos-
ton Industries, Inc., Walpole, MA, USA).
Results and Discussion
Gross Anatomy
The mean SVL of C. peguensis was 54.11 2.47 mm (mean
standard deviation [SD], n¼5). The length of the digestive
tract was 12.28 2.52 cm. All of the five specimens showed
similar gross anatomy, as shown in ►Fig. 1. The esophagus,
the stomach, and the small intestine were connected to
accessory organs (liver and pancreas). The stomach was a
wide J-shaped tube and was located in the left antimere.
Morphologically, the stomach was composed of t wo different
regions, including fundic and pyloric regions (►Fig. 1). This
stomach struct ure is similar to that of Hemidactylus mabouia,
which is considered to be carnivorous.10,14 In contrast, a
herbivorous animal, Iguana iguana, has a U-shaped sto-
mach.15 Although we could not find any literature on the
Fig. 1. Overall morphology of the digestive system of Cyr tod act ylu s
peguensis. The digestive system consisted of the fundic region (Fr) and
of the pyloric region (Pr) of the stomach (St), of the duodenum (Du)
and of the ileum (IL) of the small intestine (SI), and of the anterior
subregion (Asr) and posterior subregion (Psr) of the large intestine
(LI). The digestive system was connected to the liver (Li) and to the
pancreas. Scale bar ¼0.5 cm.
Journal of Morphological Sciences
Gastrointestinal Tract and Accessory Organs in Cyrtoda ct ylus peguensis Thongboon et al.
feeding habits of C. peguensis, the stomach shape might
suggest that C. peguensis is carnivorous.
The small and large intestines were separated by a narrow
tube and a wall projection (►Fig. 1), as reported in
H. mabouia.11 The small intestine was a narrow, coiled
tube, and was clearly separated into duodenum and ileum,
whereas the large intestine was composed of anterior and
posterior subregions, with a thin wall before the opening to
the cloaca (►Fig. 1).
Histology and Histochemistry of the
Gastrointestinal Tract
Stomach
The gastrointestinal tract of this species consisted of two
regions, including the stomach and the intestine. The sto-
mach was continued from the esophagus. As for most
reptiles,16–19 the stomach of C. peguensis was histologically
classified into fundic and pylorus regions.
In the fundic region, the stomach wall was thick and
formed by four distinct tissue layers (from inside to outside),
including mucosa, submucosa, muscularis layers, and serosa
(►Fig. 2A), as found in other vertebrates.19 Several long-
itudinal folds (or gastric rugae) were observed in the mucosa
and submucosa layers. The submucosa was comprised of
loose connective tissue and bloo dvessels, as found in those of
other vertebrates.19,20 Under the submucosa, there was a
thick muscularis layer consisting of two layers: an inner
circular muscle layer and an outer longitudinal muscle layer
(►Fig. 2A). The serosa was a thin layer of connective tissue
covered by the mesothelium.
The invagination of the mucosal surface formed several
furrows, the structure also called gastric pit (►Fig. 2B). The
mucosal layer was clearly composed of two sublayers,
including the epithelial layer and the lamina propria
(►Fig. 2B). The lamina propria was a part of the mucosal
layer consisted of vascularized loose connective tissues with
several simple tubular gastric glands (►Fig. 2C).
The PAS staining identified several types of glycoprotein-
producing cells in the fundic region. The epithelial layer of
the mucosa was covered by columnar epithelium cells,
which were strongly reacted with PAS (►Fig. 2D;simple
mucus-secreting cell) as previously reported in Siphonops
annulatus.21 These glycoproteins are reported to protect the
epithelial lining.22 Mucous neck cells were also reacted with
PAS (►Fig. 2D), whereas PAS-positive oxynticopeptic cells
had a polymorphic shape and concentric spherical nucleus.
The existence of glycoproteins in mucous neck cells was
consistent with previous reports on Hemidactylus
mabouia,10 Natrix natrix,23 and some other vertebrates.18
The roles of mucous neck cells and oxynticopeptic cells in
vertebrates are to secrete pepsinogen and hydrochloric acid
(HCl),24 although, in mammals, the chief cell secretes pep-
sinogen and the parietal cell secrete HCl.21
The histological structures of the pyloric region were
similar to those of the fundic region (mucosa to serosa).
Minor differences include that the fundic region constituted
more prominent longitudinal fold than the pyloric region
(►Figs. 2E–2H), and that few gastric glands were observed in
the pyloric region (►Figs. 2E–2H).
Small Intestine
The intestine was divided into two regions: duodenum
and ileum. The transitional area between the stomach
and duodenum was histologically different from the sto-
mach, with fewer mucosal folds (►Fig. 3A). The muscular
sphincter was also observed at the transitional area
(►Fig. 3A).
The duodenum region contained mucosa, submucosa, and
muscularis layers, but there were fewer mucosal folds com-
pared with the stomach (►Fig. 3B). No submucosal (Brun ner)
gland was observed. The inner circular muscle and outer
longitudinal muscle were thicker than those of the stomach
(►Fig. 3B). This duodenum structure was similar to those of
other reptiles.25,26
The duodenum region also contained goblet cells.
Remarkably, these goblet cells were stained by PAS
(►Fig. 3C), but not by H&E (►Fig. 3D), indicating that these
cells actually contain mucosa. The mucosal layer was covered
by a ciliated simple columnar epithelium (►Fig. 3D). This
characteristic has been reported in some reptiles, including
Kinosternon scopioides20 and Xerobates agassizii.27 Several
intraepithelial lymphocytes were localized in the lower
portion of the epithelium (►Fig. 3D), as also found in some
reptiles (Lacerta hispanica and Natrix maura).28 The struc-
ture of the ileum was very similar to that of the duodenum,
but with fewer goblet cells (►Figs. 3E–3H).
Large Intestine
The ileum was connected to the large intestine, which was
divided into the anterior and posterior subregions. The
histological features of the wall of the large intestine were
similar to those of the small intestine, but the number of
intestinal folds of the anterior large intestine was much
lower than that of the small intestine, and no microvilli
were observed (►Fig. 4A). The muscularis layer was classi-
fied into two layers, the outer longitudinal and the inner
circular layers (►Fig. 4A). The serosa was also observed
(►Fig. 4A).
The epithelial cells of the large intestine had a columnar,
long and narrow shape (►Fig. 4B). Cells on the apical surface
of the large intestine were strongly reacted with PAS (►Figs.
4C–4D)asandDiplometopon zarudnyi.29 Moreover, the large
intestine had more goblet cells than the small intestine, as
revealed by the PAS method (►Fig. 4D), which is consistent
with the observations in Caiman crocodilus yacare,25 and in
Xenodon merremii.30 However, the role of goblet cells in the
large intestine remains unclear, although these cells prob-
ably lubricate the food, facilitating its passage along the
alimentary tract, preventing mechanical damage to the
mucosa.31 It is also reported that these cells facilitate the
passage of feces.19
The histological characteristics of the posterior large
intestine were largely similar to those of the anterior large
intestine, except for the reduced number of intestinal folds
(►Figs. 4E–4G).
Journal of Morphological Science s
Gastrointestinal Tract and Accessory Organs in Cyrtodact ylus peguensis Thongboon et al.
Fig. 2. Fundic (A-D) and pyloric (E-H) regions of stomach. (A) Overall histology of the fundic region of the stomach. (B) The mucosal layer of the
fundic region was composed of epithelial layer (El) and lamina propria (Lp). (C) Gastric glands (Gg) and oxynticopeptic cell (Oc) were obser ved in
the lamina propria (Lp). (D) Periodicaci d-Schif f(PAS) staining of the mucosal layer of fundic region. (E) Overall histologyof the pyloric region (Pr).
(F-H) The oxynticopeptic cell (Oc) and the mucous neck cell (Mnc) in the gastric gland of the pyloric region. Cm ¼circular muscle layer,
Du ¼duodenum, Lf ¼longitudinal fold, Lm ¼longi tudinal muscle layer, M ¼mucosa, Msc ¼mucosal neck cell, S ¼serosa, Sm ¼submucosa,
Smc ¼simple mucus-secreting cells. Note: A- C, E-G ¼Harris hematoxylin and eosin (H&E) staining; D, H ¼p eriodic acid-Schiff ( PAS) staining.
Journal of Morphological Sciences
Gastrointestinal Tract and Accessory Organs in Cyrtoda ct ylus peguensis Thongboon et al.
Histology and Histochemistry of the
Accessory Organs
Liver
The liver lobes were surrounded by loose connective tissues.
The hepatic parenchyma was comprised of hepatocytes and
the hepatic sinusoid, a unique vascular structure commonly
observed in the liver (►Fig. 5A),asinthecaseofNerodia
fasciata fasciata.32 Each hepatocyte had a polygonal shape
and a spherical nucleus (►Fig. 5A). Being strongly reacted
with PAS, hepatocytes contained glycoproteins (►Fig. 5B).
This observation is similar to those from T. compressicauda,33
Fig. 3. Light photomicrograph of the small intestine. (A) The transitional area (Ta) between pyloric region (Pr) and duodenum (Du). (B) Overall
histology of the duodenum. (C-D) Duodenum with several longitudinal folds (Lf) and goblet cells (Gc). (E) Overall histology of the ilium (IL). (F-H)
The ilium (IL) contained a ciliated simple columnar epithelium (Csm) and goblet cells (Gc). CM ¼circular muscle layer, ILc ¼intraepithelial
lymphocyte, LM ¼longitudinal muscle layer,M ¼mucosa, Mv ¼microvilli, S ¼serosa, Sm ¼submucosa, Smc ¼simple mucus-secreting cells.
Note:A-C,D,E,G-H¼Harris hematoxylin and eosin (H&E); C, F ¼periodic a cid-Schiff (PAS).
Journal of Morphological Science s
Gastrointestinal Tract and Accessory Organs in Cyrtodact ylus peguensis Thongboon et al.
some anurans and urodeles.34–38 The liver of C. peguensis is
thus considered to be a carbohydrate/protein storage organ.
Expracutaneous pigment cells were also observed among
hepatic cells (►Fig. 5A). This feature was also observed in the
liver of other vertebrates, such as Sparus aurata and Dicen-
trarchus labrax,39 Prochilodus argenteus,40 and Kinosternon
flavescens.41 It is believed that the extracutaneous pigment
cells arise from Kupffer cells that belong to a mononuclear
phagocytic system of the mesodermal origin.42,43 The pig-
ment cells have protective roles against cytotoxic
agents.44–47 The hepatic sinusoid varied in size and con-
tained simple endothelial cells on the basement membrane
(►Fig. 5A). The portal area of the hepatic parenchyma
contained the hepatic vein.
Pancreas
The pancreas of C. peguensis was small colonies of two types
of pancreatic cells, exocrine and endocrine cells, distributed
along the intestine. The exocrine pancreatic cells formed
acini surrounde d by loose connective tissues (►Fig. 5C). Each
exocrine pancreatic cell had a pyramidal shape and ellipsoid
nucleus at the basal region of the cell (►Fig. 5C). Several
eosinophilic zymogen granules were also found in the cyto-
plasm (►Fig. 5C). The pancreatic duct was covered by simple
cuboidal epithelium, the apical sur face of which reacted with
PAS (►Fig. 5D). The endocrine pancreatic cells, as also called
islets of Langerhans, were a small cluster surrounding the
exocrine pancreatic cell. Several blood vessels were obser ved
near the endocrine pancreatic cells.
Conclusion
This is the first study that reports the histological and
histochemical properties of the digestive tract and accessory
organs of C. peguensis, a protected repti le species in Thailand.
Although the information from our study was largely similar
Fig. 4. Light photomicrograph of the large intestine. (A) The anterior subregion (Asr) of the large intestine with many longitudinal folds. (B)
Epithelial cells of the anterior large intestine. (C, D) PAS staining of the anterior large intestine, detecting Smc and Gc. (E) T hep osterior subregion
(Psr) of the large intestine with less longitudinal folds. (F) Epithelial cells of the posterior large intestine. (D) PAS staining of the posterior large
intestine. Ec ¼epithelium cell, CM ¼circular muscle layer, Gc ¼goblet cell, Lm ¼longitudinal muscle layer, M ¼mucosa, S ¼serosa,
Sm ¼submucosa, Smc ¼simple mucus-secreting cells. Note: A-B, E-F ¼Harris hematoxylin and eosin (H&E); C-D, G ¼periodic acid-Schiff
(PAS).
Journal of Morphological Sciences
Gastrointestinal Tract and Accessory Organs in Cyrtoda ct ylus peguensis Thongboon et al.
to that from other reptiles, it will open up future opportu-
nities to study the fine structure, the endocrinology, the
physiology, and the conservation of this species.
Conflicts of Interests
The authors have no conflicts of interests to declare.
Acknowledgements
We would like to thank the Microtechnique Laboratory,
Department of Biology, Faculty of Science, Prince of
Songkla University, Thailand, for their technical support
in the laboratory.
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