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International Journal of Morphology

versión On-line ISSN 0717-9502

Int. J. Morphol. v.26 n.3 Temuco sep. 2008 


Int. J. Morphol., 26(3):701-705, 2008.


Microarchitectural Adaptations in the Stomach of African Tree Pangolin (Manis tricuspis)

Adaptaciones Microarquitecturales en el Estómago del Pangolin Africano (Manis tricuspis)


Ofusori, D. A.; Caxton-Martins, E. A.; Keji, S. T.; Oluwayinka, P. O.; Abayomi, T. A. & Ajayi, S. A.

Department of Anatomy, and Cell Biology, Faculty of Basic Medical Sciences, Obafemi Awolowo University, Ile-Ife, Nigeria

Direccion para correspondencia

SUMMARY: The microarchitecture of the pangolin's stomach favouring the high chitinous diet has been less waived into, despite extensive morphological investigations. Histological analysis of the microanatomy will provide powerful tools for interpretation to yield reliable insights. We investigated this by fixing the tissues in 10% formol saline for histological analysis. Serial sections at 5 µm thickness were subjected to general staining methods for lightmicroscopic study (Haematoxylin and eosin, Van Gieson's and Verhoeff's). The results revealed basic structural arrangements in their coats, with a modification of the epithelial lining of cardia and fundus into stratified squamous keratinized epithelium. These modifications were also reflected in the distribution of collagen and elastic fibers in the various layers (coats) of the stomach. The present study has shown that there was an adaptation of the stomach of African tree pangolin to its diet as reflected in the microarchitectural configuration.

KEY WORDS: Stomach; Microarchitecture; Histological analysis; Diet; Coats.

RESUMEN: La micro arquitectura del estómago de los pangolines que favorece la alta dieta de chitinous sido poco tomada en cuenta, a pesar de las amplias investigaciones morfológicas. El análisis histológico de la microanatomía proporcionará herramientas de granimportancia para la interpretación, junto con dar una información confiable. Se investigó mediante la fijación de los tejidos en solución salina de formol al 10% para análisis histológico. Las serie de secciones fueron sometidos a métodos de tinción estándar para el estudio con microscopía de luz (hematoxilina y eosina, Van Gieson y Verhoeff s). Los resultados revelaron adaptaciones estructurales básicas en sus capas, con una modificación del revestimiento epitelial del cardias y fundus en epitelio escamoso estratificado (queratinizado). Estas modificaciones también se reflejan en la distribución de colágeno y fibras elásticas en las diversas capas del estómago. El presente estudio ha demostrado que es una adaptación del estómago a la dieta como se refleja en la configuración de la microarquitectura.

PALABRAS CLAVE: Estómago; Microarquitectura; Análisis histológico; Dieta; Capas.


The African tree pangolin (M. trisuspis), a mammal, is commonly found in the western part of Nigeria and consumes a very specific insectivorous diet (Griffiths, 1990; Ofusori et al, 2007). Fossil pangolins are first found in the Eocene in Europe. In the Messel shales of Germany they are particularly well preserved, showing that their characteristic scales were already developed. Recent DNA analysis has shown them to be bizarre offshoots of the Carnívora - the carnivores such as cats, dogs, bears, hyenas, civets and mongooses (Schlitter, 2005). Pangolin is an animal with short legs covered in brownish red overlapping scales making it look like a pinecone (Fig. 1.). It has a long, slightly-flattened prehensile tail (equally scaled), and 5 long curved claws on each foot. Its head is small and pointed with very small eyes protected by thickened eyelids, and it has a long sticky tongue for catching ants and termites. This rod-shaped tongue is covered with sticky saliva which is used as a tool to collect prey by inserting it into the termite tunnels (Pangolin Specialist Group, 1996). They have no teeth and their gizzard-like stomach may be specially adapted for grinding food. Ofusori et al. revealed from their work on the morphometric study of the stomach of M. tricuspis that the corpus is more metabolically active than the other parts of the stomach. It is therefore expedient to study the microarchitectural adaptations adopted by pangolin's stomach to cope with their diets.

The general sections of the mammalian gut (including the stomach under investigation) are usually specialized to suit the dietary requirement of particular species (Hildebrand & Goslow, 2001; Schlitter). Pangolin will often choose the larger member of the ant and termite population (for example they will choose against the smaller workers); this decreased the percentages of chitin. Calculating the nutritional value of arthropods is difficult, due to the presence of their hard exoskeleton that serves to protect their bodies. The exoskeleton and the chitin components provide a relatively indigestible substance (Griffiths et al.). In addition to the difficulties of digesting the chitin, the latter surrounds and protects the softer nutrients which are rich in fat and protein (Redford, 1983). The sand and ditrus is known to add bulk to the digestive load of insectivores and reduce the caloric proportions of their digestive content (Cohan, 1984). This finding is consistent with other ant and termite eaters (Redford, 1983).

The mucosa and muscular wall of the stomach are therefore expected to be modified in such a way as to protect it from probable ulceration by the chitin and also provide an effective churning process that will expose the soft internal part which contains the needed nutrients.

Beneath the mucosa which lines the stomach are the laminar propria, muscularis mucosa, sub mucosa, circular and outer longitudinal muscle layers and serosa layer, all of which are arranged in different patterns depending on the part of the gut under consideration (Hildebrand & Goslow) and the gut of the animal in view (Sherwood, 2004).

This study looks at the microarchitectural adaptations adopted by Pangolin's stomach to cope with its high chitinous diet.


Care of the animals. Eight presumably healthy African pangolins were procured 2 hours before sacrifice at Asejire, a local village in Osun state, south-west zone of Nigeria. They were kept and monitored in the Animal Holdings section of the Department of Anatomy and Cell Biology, Obafemi Awolowo University, Nigeria. They were fed with termites and water liberally. All animals were treated in accordance with the "Guide for the Care and Use of Laboratory Animals" prepared by the National Academy of Sciences and published by the National Institutes of Health (1985).

Excisión of the stomach. Midline laparatomy were performed under slight anesthesia using pentobarbital (6.4mg/100g body weight i.m.). The stomachs were dissected out as shown in Fig. 2 and the stomach excised and cut on a regional basis (i.e. Cardia, Fundus, Corpus, and Pylorus).

Histological procedures. The excised stomach were cleared of adhered mesentry, washed in physiological saline andµmmediately fixed in 10% formol saline for 48 hours. After fixation, the tissues were dehydrated through graded alcohol. The tissues were then cleared in three changes of xylene for 1.5 hours duration each. After clearing, the tissues were infiltrated with molten paraffin wax at 56°C. The tissues were embedded in paraffin wax for a period of 24-48 hours. Sectioning of the tissues was carried out on a rotary microtome (Bright automatic rotary microtome) at 5µm. The sections were stained with (a) Verhoeff's Haematoxylin elastic tissue stain for the demonstration of elastic fibers, (b) Van Gieson's staining method for the demonstration of collagen fibers and (c) Haematoxylin and eosin for histo-architecture.


It was noted from our present study that the epithelial lining of the stomach are mainly simple columnar with the exception of the cardia and fundus which had stratified squamous keratinized epithelium (Table I. and Fig. 3). The mucosa and muscular coats were also observed to be well organized with a well formidable muscularis externa (Fig. 3) believed to be adopted for the churning of the high chitinous diet. Also, collagen fibers were observed to stain more intensely in the submucosa compared to the mucosa and muscularis externa. The staining intensity was observed to be more in the cardia and fundic regions of the stomach as shown in Fig. 4. Smooth muscle fibers were also observed to stain intensely. Elastic fibers were stained so well in the muscularis externa of all the regions of the stomach. Traces of these fibers were also noticed along the length of the gastric glands in the corpus and pyloric regions Fig. 5.


The structural arrangement of the layers of the stomach of pangolin conforms to the basic organization. This was characterized by four concentríc layers which included: mucosa, sub mucosa, muscularis externa and serosa; all arranged in different patterns depending on the región of the stomach investigated.

The mucosa of pangolin's stomach has both nonglandular (cardia and fundus) and glandular (corpus and pylorus) regions (Fig. 3). This non-glandular región, which was observed to be lined mainly by stratified squamous keratinized epithelium, in contrast to the simple columnar epithelium of the glandular part (Fig. 3), probably offers a protection against the probable ulceration by the hard chitinous ingesta (ants and termites); and may also be the active sites for the mechanical activities of the stomach which exposes the soft internal part of the ingesta which is rich in fat and protein as reported by Redford & Dorea (1984) and Redford (1985). This is in agreement with the morphometric study of the stomach of M. tricuspis by this same author (Ofusori et al.). Ants and termites are the main diet of pangolin. They use their claws to break open ant or termite nests and capture the occupants with their long sticky tongue. They can take up to 200,000 ants each night. The parietal cells (acid secreting cells) which stain eosinophilic with centrally located nucleus were distributed along the length of the gastric gland in the corpus. Although it is still unclear if the acid secreting parietal cells have some other function in M. tricuspis but it is known that like other mammals, acid secreting cells works by the production of carbonic acid by the enzyme carbonic anhydrase from hydrochloric acid which then dissociate into hydrogen and bicarbonate ions. The corpus in pangolin is characterized with secretory features and so secretes acid-peptic gastric juices as well as some protective mucus. Zymogenic cells secrete pepsin which is anµmportant digestive enzyme for protein. Henee, its presence is indicative of protein digestión thus buttressing the reports of Redford and Dorea (1984) and Redford (1985) that the internal part of pangolins diet (ants and termites) is highly rich in protein. The presence of lymphocytes in the stomach placed them as some of the mammals so endowed and may be responsible for protection against microorganisms and for destroying virus-infected enterocytes. This is in agreement with the findings of Heath et al. (1999) who investigated the function of lymphocytes in human gastrointestinal tract. Other structural components probably provide some balance for, the longitudinal and circumferential stress generated by the elastic recoil, mechanical activity (Churning process) of the stomach which progressively modifies the pulsadle flow of the chyme out of stomach into the intestine. Our findings and their probableimplications are in conformity with the work of Glenn & Robert (1997). The results of the Van Gieson staining confirmed the presence of collagen fibres, which were more in the sub mucosa than the mucosa and muscularis externa of the stomach (Fig. 4). The intense staining of collagen fibers observed in the sub mucosa may be an indication of the high tensile strength required to withstand the mechanical activity of the stomach against the hard ingesta and to accommodate the pressure generated by the air-filled stomach which ensures buoyaney. The elastic tissue staining intensity in the muscularis externa was stronger than what was observed in the mucosa and sub mucosa (Fig. 5). The high concentration of elastic fibers observed in the muscularis externa of the stomach underlines their functionalµmplication. This suggests the stretching and recoiling property needed for the proper churning of the hard ingesta to expose the soft internal part which is rich in fat and protein (Redford & Dorea), and for the distention of the stomach to accommodate air for buoyaney during swimming (Pangolin specialist group, 1996). It can therefore be reported that there was a micro anatomical adaptation in the stomach of M. tricuspis to suit its high chitinous diet. These adaptations are efficient for successfully coping with its high chitinous food and to compénsate for the lack of teeth in African tree pangolin (M. tricuspis).


The author is very grateful to Prof. C.O Adewunmi of the Faculty of Pharmacy, Obafemi Awolowo University, Nigeria, for his contribution when taking the photomicrographs of this research work.



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Correspondence to:

Dr.. David A. Ofusori


Received: 07-06-2007 Accepted: 17-08-2007


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