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Comparative intestinal histomorphology of five species of phyllostomid bats (phyllostomidae, microchiroptera): ecomorphological relations with alimentary habits/Histomorfometria comparativa de intestino de cinco especies de murcielagos phyllostomideos (phyllostomidae, microchiroptera): relaciones ecomorfologicas con habitos alimentarios.


The family Phyllostomidae, endemic to the Americas, constitutes the most diverse and most widely distributed family of Neotropical bats. It is represented by the New World leaf-nosed bats, and is considered the third biggest family of Chiroptera, with 50 genera and 145 species grouped in several subfamilies and tribes (Koopman, 1993; Gimenez, 1998). The evolutionary history of these bats is marked by a great adaptive radiation associated with feeding habits, including insectivorous, frugivorous, nectarivorous, carnivorous, omnivorous and sanguivorous diets (Gardner, 1977).

The first detailed study of the chiropteran gastrointestinal tract morphology dates from the end of the 19th century. Robin (1881) presented information which was new for the time, in addition to an excellent review of the literature published until then. In the 20th century, advances in histological techniques and the betterment of microscopes led to a boom in microscopic studies.

The macro- and microscopic (histological) anatomies of the gastrointestinal tract or its parts have been well reported for numerous species of Microchiroptera, e.g. Schultz (1965); Rouck & Glass (1970); Forman (1971, 1972, 1973), Kamiya & Pirlot (1975); Madkour (1977); Okon (1977); Forman et al. (1979); Ishikawa et al. (1985). However, these works represent a scarce body of information, in view of the as yet unstudied diversity of Neotropical chiropterans.

Although there is a body of literature dealing with morphological descriptions of the chiropteran gastrointestinal tracts, it is not only insufficient, but in addition almost totally lacking in a comparative analysis consistent with the existing diversity of food habits.

Comparative analysis of chiropteran gastrointestinal tract morphology can undoubtedly evidence important features to further our knowledge on the phylogenetic relations of this group, as well as to better understand the evolutionary process as a whole, by means of comparative data on the relation between adaptative radiation and availability of resources in the environment (Forman et al.). These comparative studies can additionally subsidize hypotheses for the understanding of the relations between feeding habits and the digestive physiology of Neotropical bats (Bhide, 1979).

In the present work we carried out a comparative study on the intestine histomorphology of five representatives of family Phyllostomidae, so as to acquire more knowledge on the structural components which make up these tissues. Such results will contribute to a better understanding of these bats' ecomorphology and thus provide grounds to assess evolutionary models on the adaptative radiation of phyllostomid feeding habits.


We studied 54 bats representing the 5 Phyllostomidae subfamilies: Sturnira lilium, frugivorous (Stenodermatinae); Phyllostomus hastatus, omnivorous (Phyllostominae); Carollia perspicillata, frugivorous, but also insectivorous (Carolliinae); Glossophaga soricina, nectar-polinivorous, but also consuming insects and fruits (Glossophaginae); and Desmodus rotundus, sanguivorous (Desmodontinae). These animals were captured in a joint effort with the team of researchers from the Laboratory of Mammalian Systematics and Evolution from the National Museum/UFRJ, through collections carried out in Carmo Municipality, Rio de Janeiro State (July 1999/ October and November 1999), and in Serra da Bodoquena and Bonito regions in Mato Grosso do Sul State (July 2000 / January and February 2001).

Samples of the gastrointestinal tract for microscopic study were obtained following a protocol consisting of anesthesia, sorting, weighing, measuring and dissecting. The abdominal cavity was opened through a ventromedian incision beginning roughly at 1 cm from the external genitalia and extending to the cervical region, followed by two lateral incisions towards the anterior and posterior limbs. The entire gastrointestinal tract was removed, sectioned into its anatomic portions, and washed in biological saline. Samples of the small and large intestines were cut out and fixed in buffered 10% formalin (24 to 48 hours), followed by routine histological technique down to final embedding in paraffin. The material was sectioned into 5-[micro]m slices in a microtome and stained by the routine haematoxylin and eosin staining technique and by the PAS, Alcian-blue pH 2.5 and Picrosirius red histochemical techniques.

The animals were fixed in 10% formalin, stored in 70% alcohol and placed in the scientific collection of the Mastozoology Sector at the National Museum/ UFRJ.

For morphometric analyses the Image Pro Plus software (Media Cybernetics, USA) was used.


Macroscopic study. The intestine of all species studied showed itself displaced to the right within the abdominal cavity, presenting itself extremely curved (Fig. 1A, B). In D. rotundus this curvature is less noticeable, and the largest part of the intestine is folded back upon itself in a compact series of numerous winding folds (Fig. 1C).

On analyzing the intestine macroscopically we could not distinguish the delimitation between the small and large intestines, in spite of the presence of Peyer's patches. These can be small and difficult to visualize, as in G. soricina. In S. lilium and D. rotundus we found nodular lymphoid tissue aggregates distributed along the tube. The duodenum can be identified by its diameter, which is bigger than the rest of the gastrointestinal tract.

In P. hastatus and C. perspicillata we could observe an increase in the diameter of the junction of the small and large intestines, as a result of the presence of Peyer's patches at the end of the distal portion. The large intestines of the analyzed species have neither caeca nor appendices, consisting only of a descending colon.


The intestinal length varies greatly among the species: S. lilium possessing a very long intestine, P. hastatus, D. rotundus and C. perspicillata having intestines of moderate length, and G. soricina presenting a very short intestine. All measurements were related to body length (Table I).

If the intestine is cut open longitudinally, we observe a series of definite folds in its internal surface. These are Kerckring's folds, which generally run parallel to one another and occupy from half to two-thirds of the tube's perimeter. These folds include the mucosa and part of the submucosa. In the bats studied, these folds are absent in the upper region of the duodenum and in the distal portion as it approaches the colon.

Microscopic study. Histologically, the small intestine wall of the species studied is composed of the typical layers: mucosa, submucosa, muscularis mucosae and serosa.

We observed in all species a mucosa with villi covered by a simple columnar epithelium constituted of absorptive cells, characterized for possessing microvilli (Fig. 2). Scattered among the absorptive cells, the goblet cells can be found. In the middle portion they are less numerous, but distally they increase in number. D. rotundus presented fewer numbers of goblet cells throughout the small intestine than the other species.

Shape of villi of the intestinal mucosa presented differences among the species. C. perspicillata presented fingerlike villi all over the small intestine, which were longer, arched and arranged in oblique rows in the middle portion, while distally their height decreased (Fig. 3A). In P. hastatus the villi are fingerlike, arched, oblique and long in the middle region (Fig. 3B) whereas, in the distal portion, they were short, more spaced and with not very sharp apices. S. lilium showed villi in two shapes, pyramidal in the middle-proximal portion of the duodenum (Fig. 3C), and fingerlike in the other portions (Fig. 3D). The villi are quite long in the middle portion and decrease in the distal portion. G. soricina showed a mucosa with compact, fingerlike villi (Fig. 3E), long in the middle portion and shorter in the distal portion. D. rotundus possesses pyramid-shaped villi (Fig. 3F), longer in the middle portion than in the distal portion.




In the distal portion, next to the junction with the large intestine, we found clustered lymphatic nodules, forming the lumps called Peyer's patches (Fig. 4A). In the lamina propria of the villi we could see the presence of a discontinuous lacteal vessel, a central lymphatic vessel (Fig. 4B).

Among the villi we found simple tubular glands, the crypts of Lieberkuhn (Fig. 4C). These glands are separated by the conjunctive tissue of the lamina propria and their extremities reach the muscularis mucosae. In all the studied species we found, deep in the crypts of Lieberkuhn, groups of granular cells known as Paneth cells (Fig. 4C).

Goblet cells were also found in the crypts and, as in the villi, they increase in number in the distal portion. C. perspicillata distally presented few goblet cells in its crypts, being more concentrated in the villi (Fig. 4B).

The muscularis mucosae is a very thin tissue layer, and we could not visualize it in the middle portion, but distally it was a little thicker. The submucosa proved to be formed by slack conjunctive tissue possessing blood and lymphatic vessels. In D. rotundus the submucosa was denser than in the other species (Fig. 5).


The outer muscular layer is composed of two layers, one circular and another longitudinal. Between them we could visualize the myenteric plexus. In the middle portion the circular and longitudinal layers are very thin, but distally the circular layer becomes much thicker than the longitudinal one (Fig. 6).

Finally, we found the serosa which is the thin, outermost layer, formed by slack conjunctive tissue covered by a mesothelium.

The large intestine of the bats presented uniform characteristics, being formed by only a descending colon and the rectum. All four layers were present: mucosa, submucosa, muscular and serosa.


The mucosa is smooth, without the presence of villi or folds as in the small intestine. The whole thickness of the mucosa is filled with intestinal glands (crypts of Lieberkuhn) which are long, straight and tubular.

The superficial epithelium as well as the glands epithelium is of the simple columnar type and contains absorptive cells and innumerous goblet cells. The submucosa is formed by a slack conjunctive tissue containing blood vessels. The muscularis layer is divided in two, one very thick and circular, and the other thin and longitudinal. The serosa is very thin, with abundant conjunctive tissue around the vessels.


Structures that are characteristic of the large intestines of mammals, like taeniae coli and appendices epiploicae, were not found in the species studied.

In the present work we used methods of routine staining as well as some special dyes (histochemistry). We used the Periodic Schiff Acid (PAS) to detect the presence of glycoproteins in the goblet cells of the small and large intestines. These cells tested positive for all regions of the small and large intestines of all studied species.

In all species the alcian blue pH 2.5 method tested positive for the carboxylated proteoglycans of the goblet cells all over the intestine (small and large).

The collagen distribution in the small intestine presented differences among species, being abundant in the submucosa and around the serosa vessels in P. hastatus, G. soricina and D. rotundus, but scarce in the submucosa of C. perspicillata and S. lilium. In the large intestine collagen was abundant in all species. This analysis was done using the picro-sirius method without polarization (Fig. 7A, B and C).

Under a polarized light we could notice the organization of the collagen network, which appeared to be type-I for being birefringent and displaying red-orange shades in the small and large intestine of all species studied.

The length of the crypts of Lieberkuhn and of the villi both in the middle portion of the small intestine were morphometrically analyzed (Table II and III; Fig. 8). In P. hastatus the crypts were longer than in the other species, and in D. rotundus they were shortest (Table II and Fig. 8A). The villi presented differences in length. S. lilium and C. perspicillata presented longer villi than P. hastatus, D. rotundus and G. soricina (Table III and Fig. 8B).



Intestines in the analized species are located in the same position as in the different species of Chiroptera studied by Park & Hall, (1951); Forman et al.; Tedman & Hall, (1985).

The intestine of D. rotundus is similar to that described by Forman et al., displaying very little noticeable curving, while in the other species the shape was arched, as reported by Schultz, (1965).

Special techniques like light and scanning electron microscopy have been used to distinguish the different portions of bat intestines, e.g. by Okon (1977); Ishikawa et al. (1985); Tedman & Hall (1985); Makanya & Maina (1994); Makanya (1997), Makanya et al. (2001).

External morphology does not allow a clear distinction between the small and large intestines in all bat species. Tedman & Hall (1985) stated that the intestine of Pteropus alecto and P. poliocephalus is a continuous tube without separation between the small and large intestines. Forman, (1974a, b) states that the junction of the small and large intestine is formed by a small ampulla, resulting from abundant lymphoid tissue (Peyer's patches). He revealed differences in the abundance, distribution and morphology of these tissues in phyllostomids which are possibly diet related. He also noted that frugivorous bats have more Peyer's patches than nectarivorous, carnivorous or insectivorous ones, and that they can occur anywhere along the tract. In insectivorous and carnivorous species, the patches are small, showing a low state of activity, and usually restricted to the ileum submucosa. In S. lilium and D. rotundus we noticed a greater number of aggregates of lymphoid nodular tissue, which are well distributed along the tract. In P. hastatus and C. perspicillata Peyer's patches were observed in the distal portion next to the large intestine, and the two portions of the intestine (small and large) could be distinguished. In G. soricina we could not visualize Peyer's patches externally, and so it was not possible to delimit the small/large intestine junction, as also observed by Ishikawa et al., in the insectivorous bat Myotis frater.

The absence of the caecum and of the appendix is considered characteristic of the gastrointestinal tract of chiropterans (Tedman & Hall), another feature being the absence of the ascending and transverse colons, the large intestine as a result being restricted to a descending short colon (Forman et al.). This absence is well described in the literature for several species of bats (e.g. Park & Hall, Ishikawa et al.; Tedman & Hall; Makanya & Maina; Makanya; Makanya et al., 2001), and this also applies to all species studied in the present work.

Most bats have a smaller intestine than do terrestrial mammals of comparable size (Klite, 1965). Several comparisons of bat intestinal length measurements (Robin 1881; Eisentraut 1950, Park & Hall; Forman et al.; Tedman & Hall; Makanya) reveal that frugivorous species have a longer intestine, relative to body length, than species with other feeding habits.

Eisentraut, observed a great number of bat species with a variety of feeding habits and noted that those with intestines four times longer than the body were always frugivorous species. Among the species with a longer intestine were Chiroderma villosum, Vampyrops vittatus and several species of Artibeus. Vampire bats presented intestines of moderate length and insectivorous ones a short gastrointestinal tract. Comparable measurements were taken in this work and we noted that S. lilium, frugivorous, has a long intestine relative to body length. In D. rotundus, P. hastatus and C. perspicillata intestine length is moderate, and in G. soricina it is short. The latter is similar to the insectivorous species in that it supplements its diet with insects. The short intestine observed in this species is probably an adaptation to reduce weight for improving flight. Physiological studies made by Keegan (1975, 1977) indicated that long intestines would not hamper the flight of frugivorous bats, since food transit and absorption time is quite rapid.

The disposition of Kerckring's folds, absent in the upper region of the duodenum and in the distal portion as it approaches the colon, are similar to that generally found in mammals.

The gland of Brunner is easily found in the duodenum of bats, but the taenia coli and the appendices epiploicae are absent in the large intestines of the species analized in this work, as well as in the ones studied by Tedman & Hall; Makanya & Maina; Makanya; Makanya et al. (2001).

We can distinguish the intestine segments by the increase of the goblet cells and the absence of villi, which are typical of the chiropteran large intestine. The middle and distal portions can be distinguished by decrease of the villi and increase of the goblet cells in the distal portion, also observed by Ishikawa et al.; Tedman & Hall; Makanya & Maina in other species.

The villi of the small intestine mucosa presented differences, similar to the ones described by Mathis (1928); Schultz; Forman et al. The mucosa epithelium, similar to that found in other mammals, is of the simple columnar type, which was also observed in Myotis frater by Ishikawa et al., in Pteropus alecto and P. poliocephalus by Tedman & Hall and in Epomophorus wahlbergi by Makanya et al. (2001).

The cell types found in the small intestine of the bats studied are basically the same found in mammals in general, i.e. absorptive cells which microvilli and goblet cells which become more numerous along the tube. This was observed in other species of bats by Ishikawa et al.; Tedman & Hall; Makanya & Maina; Makanya; Makanya et al. (1995, 2001). D. rotundus presented less goblet cells than the other species, a fact also observed in Pteropus alecto by Tedman & Hall. This can be associated to the type of food consumed, which is liquid and easily absorbed. D. rotundus is sanguivorous.

Paneth cells were observed by Schaaf (1970) in the insectivorous species group: Artibeus jamaicensis, Bachyphylla nana, Phyllonycteris polyi and Monophyllus redmani. These cells were also observed in all the analyzed species.

The presence of glycoproteins and carboxylated proteoglycans in goblet cells is a common characteristic in mammals, including man.

The muscularis mucosae and submucosa are not highly developed in the species here described, a fact also observed in Myotis frater by Ishikawa et al., but blood and lymphatic vessels were well observed in the submucosa. In D. rotundus this layer was thicker than the others, a characteristic previously observed by Forman et al., in vampire bats.

Many characteristics generally found in mammals were also seen in bats, such as the presence of central lacteals in the lamina propria of the villi, and an outer muscular layer composed of a circular and a longitudinal layer, the former increasing in thickness as it approaches the large intestine. A myoentheric plexus was observed between them and the outermost layer, the serosa, was formed by slack conjunctive tissue covered by a mesothelium.

The presence of colagen fibers in the intestine of mammals is common. It is believed that in the large intestine this colagen layer regulates the transport of substances which are absorbed. In the small and large intestines of all studied species a dense colagen network was found, seemingly of type I. The characteristics of the large intestine are uniform in the studied species, as well as in the ones already described in the literature.

Morphometric studies of the bat gastrointestinal tract are scarce in the literature. These studies are essential to determine important functional parameters, such as the absorption surface area available in different kinds of bats.

We may conclude that the patterns of morphological variation observed in the small intestine suggest adaptations to the different feeding habits of the bat species here studied. These results can be used as a new and promising systematic approach for formulating rules of variation concerning the histological patterns observed, to corroborate existing hypotheses or to create grounds for new studies.

List of specimens used.

* Phyllostomus hastatus (Subfamily Phyllostominae): MN 56210, MN 56233, MN 56234, MN 56235, MN 56236, MN 56238, MN 59715, MN 59835.

* Carollia perspicillata (Subfamily Carolliinae): MN 56262, MN 56289, MN 56292, MN 56293, MN 56324, MN 56352, MN 59694, MN 59696, MN 59721, MN 59732, MN 59739, MN 59803, MN 59810.

* Desmodus rotundus (Subfamily Desmodontinae): MN 56164, MN 56190, MN 59710, MN 59711; MN 59724, MN59743, MN 59766, MN 59778; MN 59823; MN 59830.

* Sturnira lilium (Subfamily Stenoderminae): MN 56186, MN 56194, MN 56342, MN 56344, MN 56345, MN 59697, MN 59716, MN 59749, MN 59750, MN 59755, MN 59761, MN 59817.

* Glossophaga soricina (Subfamily Glossophaginae): MN 56156, MN 56157, MN 56278, MN 56278, MN 56302, MN 56308, MN 56309, MN 56310, MN 56333, MN 56335, MN 59758.


We thank Dr. Leandro de Oliveira Salles from the Mastozoology Sector of the National Museum of Rio de Janeiro /UFRJ for the use of his laboratory and permission to take part in the collections performed in Serra da Bodoquena, Mato Grosso do Sul State; Dr Patricia Goncalves Guedes and Carlos Augusto Caetano for their help in some collecting trips; Prof. Hamilton G. dos Santos for his help in the field trips and in species identification; Dr. Leonardo dos Santos Avilla for the collections in Carmo--RJ State and for his help with species identification; Dr. Carlos Alberto Mandarim-de-Lacerda from the UERJ Anatomy Department for ample use of his laboratory; Dr Mara Ibis Rodrigues Apfel and Dr Jorge Jose de Carvalho from the UERJ Histology and Embriology Department for hints on histological and histochemical staining methods and the use of the laboratory; Joao Roberto de Campos Perez and Francisco Fabio da Silva Barbosa from the UERJ Histology and Embriology Department for help in preparing histological slides; Mario Pereira from the UERJ Physiology Department for his help with the morphometric analyses; Mariana Fiuza de Castro Loguercio for helping in the text revision and Humberto Moura-Neto for his help in revising the English translation.


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* Rafaela Gadelha-Alves; **,*** Andrea Melo Da Silva Rozensztranch & * Oscar Rocha-Barbosa

* Laboratorio de Zoologia de Vertebrados (Tetrapoda--LAZOVERTE)--Departamento de Zoologia, IBRAG--Universidade do Estado do Rio de Janeiro (UERJ), Brazil. Rua Sao Francisco Xavier, 524--Maracana 20550-013, Rio de Janeiro, RJ, Brazil. E-mail:

** Laboratorio de Sistematica e Evolucao de Mamiferos--Departamento de Vertebrados, Setor de Mastozoologia, Museu Nacional/Universidade Federal do Rio de Janeiro (MN/UFRJ), Brazil.

*** Laboratorio de Histoquimica, Instituto de Biologia, Universidade do Estado do Rio de Janeiro (UERJ), Brazil. Part of a M.Sc. dissertation (Rafaela Gadelha-Alves).

Correspondence to: Oscar Rocha-Barbosa

Universidade do Estado do Rio de Janeiro

Pav. Haroldo Lisboa da Cunha--sl. 522a, 5o Andar

Departamento de Zoologia

LAZOVERTE--Laboratorio de Zoologia de Vertebrados (Tetrapoda)

Rua Sao Francisco Xavier, 524--Maracana


Rio de Janeiro, RJ,



Received: 28-03-2008

Accepted: 04-08-2008
Table I. Mean [+ or -] SD intestinal length and body length
of the analyzed species.

Species       n       Intestinal          Body length       length/body

C. perspici   5   52.4 [+ or -] 12.9   142.6 [+ or -] 3.3       2.7
    D.        5   76.9 [+ or -] 13.9   208.5 [+ or -] 4.6       2.7
    G.        5   52.6 [+ or -] 6.5     99.8 [+ or -] 1.7       1.9
S. lilium     5   59.7 [+ or -] 24.5   209.6 [+ or -] 1.7       3.5
    P.        5   96.7 [+ or -] 9.9    265.6 [+ or -] 4.1       2.7

Table II. Morphometric measurements of the Lieberkuhn
crypts lengths ([micro]m).

Specimen     Carollia      Desmodus   Glossophaga
           perspicillata   rotundus    soricina

   1          172.792       79.499      155.58
   2          147.999      146.956      168.801
   3          144.177      108.335      342.97
   4            --            --          --

  Mean        154.989      111.597      222.45
   SD         15.535        33.846      104.58

Specimen   Sturnira   Phyllostomus
            lilium       hastatus

   1       119.477         424.286
   2       124.504         536.448
   3       188.853         688.676
   4          --           548.211

  Mean     144.278         549.405
   SD       38.685         108.350

Table III. Morphometric measurements of villi length ([micro]m).

Specimen     Carollia      Desmodus   Glossophaga
           perspicillata   rotundus    soricina

   1          568.800      368.520      338.230
   2          509.050      424.070      273.080
   3          444.620      396.290      415.080
   4            --            --          --

  Mean        507.490      396.293      342.130
   SD         62.105        27.775      71.080

Specimen   Sturnira   Phyllostomus
            lilium       hastatus

   1       564.860         423.360
   2       594.030         334.020
   3       564.000         445.340
   4          --           326.430

  Mean     574.296         382.287
   SD       17.095          60.862
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Author:Gadelha-Alves, Rafaela; Rozensztranch, Andrea Melo Da Silva; Rocha-Barbosa, Oscar
Publication:International Journal of Morphology
Date:Sep 1, 2008
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