A COMPARATIVE MORPHOLOGY OF ANAL TONSILSIN PLATANISTIDAEFUSAO YAMASAKI, SHUNRO KOMATSU
Department of Biology, Sapporo Medical College, Sapporo

AND
TOSHIRO KAMIYA
Department of Anatomy, Faculty of Medicine, University of Tokyo, Tokyo

ABSTRACT

Anal tonsils, complex lymphoepithelial structures in the anal canal, were
found in Platanista gangetica, and morphological observations were made macroand light microscopically. In Platanista, the anal tonsils are mainly present
and scattered on the oral half of the anal canal, however, they are relatively
poorly developed and small in number. The formation of the anal tonsils cannot be found in Inia geoffrensis, although accumulations of lymphoid tissue areobserved as far as the posterior part of the anal canal. In Pontoporia blainvillei,
even such accumulations are absent from all parts of the anal canal. Comparative considerations of the anal tonsils are mentioned in Platanistidae and insome other cetaceans.

INTRODUCTION

Ortmann (1960) reviewed the lymphatic apparata and so-called "anal tonsil" inthe anal region in many mammals, however, in his description no mention wasmade of those in Cetacea. Uys and Best (1966) made a pathological observation
on Cetacea in which they described the anal tonsil in sperm whales. This structure is present externally around the anal opening. Cowan and Brownell (1974)
reported the anal tonsil in the anal canal of gray whales and made comparativeand functional considerations on this subject. We made an anatomical observation on the digestive tract of the Ganges susu in 1972, however, we overlooked the·anal tonsils at that time. Recently, we have reexamined the previous materials
and observed other specimens of this dolphin, and similar structures to that in graywhale were found in the anal canal. No reports on this subject in Cetacea, except
for the abovementioned two reports, have been published to date and there still
remain many problems of ambiguity in the biological meanings of the anal tonsil.
Therefore, a brief morphological description of the anal tonsil in the Ganges susu
will be added to the knowledge of that of Cetacea. In addition, comparative observations were done on two other kinds of Platanistidae, Franciscana and Boutu,
and also on the striped dolphin .
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YAMASAKI, KOMATSU AND KAMIYAMATERIALS AND METHODS
Six specimens of Ganges susu, Platanista gangetica (body length; 76.0, 105.5, 106.5,
113.0, 118.0, 127.0 cm) were used in this study. For comparison four Franciscana,Pontoporia blainvillei (98.5, 113.5, 121.0, 171.0 cm) and a Boutu, lnia geoffrensis(204 cm) were examined. The Platanista and the Pontoporia were collected by the
Cetacean Research Expedition of the University of Tokyo. Specimens of 76.0,
113.0, 118.0 and 127.0 cm in the Platanista were collected in the Brahmaputra
River (Bangladesh) from 1969 to 1970 and the other in the lndus River (Pakistan)in 1974. The Pontoporia were caught off the Uruguayan coast from 1972 to 1973.
The lnia was offered to us by the Kamogawa Sea World Aquarium in Chiba,
Japan. Six striped dolphins, Stenella coeruleoalba, collected off the Pacific coast of
Izu peninsula, Japan, were also examined as one example of marine dolphins.
Materials were fixed in 10% formalin solution at the site of capture and sent
to our laboratory. After macroscopical observations from the interior of the anal
canal, the whole length of which was cut serially in about 5 mm thicknesses, detailed examinations were done. Histological pieces were embedded in paraffin andcelloidin, and then sectioned and stained with hematoxylin and eosin.
OBSERVATIONS AND COMPARATIVE CONSIDERATIONS
The anal canal, from the posterior end of the rectum to the anal orifice, varies inlength with individual body length and is about 4 to 7 cm long in the Platanista observed. The epithelium shows an abrupt change at a point between the rectum
and anal canal from intestinal glandular mucosa to stratified squamous epitheliumin all species of dolphins observed. We have labelled this point the recto-analepithelial transition (Takahashi and Yamasaki, 1972). Cowan and Brownell, in
the gray whale, labelled it as the muco-squamous junction. The oral half of theinner surface of the anal canal in Platanista is somewhat irregular and uneven inappearance and several longitudinal folds are present on the posterior half (Fig. 1).
The epithelium of the anal canal becomes pigmented towards the anal orifice andcontinues to the external skin.
Complex lympho-epithelial structures in the anal canal, anal tonsils, are foundin Platanista, with the exception of one 76 cm specimen. A well developed structure (Fig. 2) similar to that of the gray whale observed by Cowan and Brownell
was found. This structure may correspond to the ' first type ' described by them,
however, the development and the number of the tonsils in Platanista is rather poorand less, respectively, than that of the gray whale. There seems to be no sexual
difference. In Platanista the anal tonsils are present but scattered in the oral threefifths of the anal canal, except for the zone adjacent to the recto-anal transition,
approximately 2 to 3 mm in width.* The tonsils are rather well developed in the* In our previous paper on the intestinal tract of Platanista (1972) there was no mention of this structure
because we had observed only the part adjacent to the recto-anal transition where no tonsils were present.
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97

oral half of the anal canal and they decrease in size and number towards the posterior. There are a few structures which form an independent elevation and these
are usually found grouped in the irregular or longitudinal folds of the anal canal,
forming oval masses 2 to 3 mm thick, 4 to 5 mm wide and 5 to 6 mm long. In
the gray whale, distinct openings of the tonsilar crypts are abundant in Figure 1of Cowan and Brownell's article. In Platanista they are very small, usually pinhole in size, and few distinct ones are found on the inner surface of the anal canal.
Although it is fairly difficult to distinguish the existence of the tonsilar crypt with
the naked eye, especially in younger animals, when viewed through a stereomicroscope small openings can be recognized on the surface. When viewed on a crosscut surface of the anal canal masses of lymphatic nodules, being yellowish gray incolor, are rather easily distinguishable.
Anal tonsils in the gray whale, of which the anal canal is 30 to 40 cm long,
are found on the posterior part of the muco-squamous junction extending overabout 10 cm in width (Cowan and Brownell). In sperm whales, they are present
as numerous lumps and exist externally around the anal opening (Uys and Best).
The location and the distribution of the tonsils may vary considerably among different species of some cetaceans which may have anal tonsils.
The sample shown in Figure 2 is of a well developed, independent tonsil in
Platanista (113 cm) which we observed. It shows a distinct epithelial elevation,
about 5 mm across and 3 mm high. The tonsil is composed of a mass of lymphatic nodules with a few germinal centers. The mass is about 4 mm in diameter.
Its capsulation of connective tissue which is continuous with that of the submucosa
is poorly developed. The tonsilar surface is covered with stratified squamous
epithelium, invaginated into the subjacent lymphoid tissue to form a central crypt,
which ramifies into a small number of subdivisions. Invaginated epithelium fromthe free surface becomes thinner and almost disappears at the mid-portion of thecrypt. In cases of younger specimens (105.5, 106.5 cm), tonsils are small in size,
1 to 3 mm across, and they are grouped in places in the submucosa (Fig. 3). The
crypts, some of which are slightly tortuous in course, ramify near the surface tothe adjacent tonsils which are separated by connective tissue, or the crypts of twoor three tonsils open onto the surface by a common opening. Lymphatic nodules
without crypts are often present next to the tonsils. In the deeper portions of thecrypts in younger specimens secondary papillae of their epithelia are poorly developed and the limit between the epithelium and lymphoid tissue is obscured by an
infiltration of the epithelium with lymphocytes. Small numbers of mucous glands
are present at the bottom of the structure. In younger cases, glands are seen near
the masses of lymphatic nodules. In the case of the 76 cm specimen, there can beseen a very few small aggregations of lymphocytes without the formation of lymphatic nodules in the submucosa.
Thus, Platanista has anal tonsils, which are mainly present in the oral half of
the anal canal, although relatively poorly developed and small in number. Since
the anal tonsils were not formed in the 76 cm specimen and in younger stage they
are small in size, it seems that the anal tonsils develop with age in Platanista as far
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YAMASAKI, KOMATSU AND KAMIYA

as we have been able to observe.
Cowan and Brownell referred to the relation of the anal tonsils in Cetaceawith the avian bursa of Fabricius. They described the morphologic homology andsuggested the functional homology between the two structures. Assuming that theanal tonsils of Platanista develop with age, the relationship between the anal tonsils
and the bursa, which may degenerate with age, may be converse, and this problem
should be discussed based on further observations of the anal tonsils in other cetaceans.
On the other hand, in Inia, although we observed only a single case of a specimen of 204 cm in body length, diffuse accumulations of lymphoid tissue are observed in the submucosa to the posterior region of the anal canal. Crypt-likeepithelial invaginations can often be observed, but they are not always associatedwith accumulations of lymphoid tissue. Germinal centers are poorly developed.
In the Inia observed, well outlined organs of lymphoid tissue such as in Platanista
could not be observed (Fig. 4).
In contrast, in Pontoporia no accumulations of lymphoid tissue can be observedin any part of the anal canal and only a very few aggregations of lymphocytes canbe seen in all animals examined, as we briefly pointed out in a previous paper(Yamasaki et al., 1975). The submucosa is highly vasculized (Fig. 5).
In Stenella coeruleoalba, well outlined anal tonsils with distinct germinal centers
are present on the oral over about three-fourths of the anal canal. Many openingsof the tonsilar crypts are clearly visible to the naked eye at the region corresponding to the tonsils on the inner surface of the anal canal. Anal tonsils in this speciesof Stenella are far more well developed compared with those in Platanista.
There is a remarkable difference in the lymphoid tissue in the anal canal in
Platanistidae as mentioned above. It is interesting as to whether anal tonsils arepresent in other kinds of Stenella or not. Ortmann (1960) has already reviewed
the considerable variations in the presence of anal tonsils in all the species of mammals he observed, although no mention was made of those in cetaceans.
There seems to be a close relationship between the existence of the anal tonsils
and the distribution of the lymphoid tissues in the entire intestinal tract. Therefore, observation of the anal tonsils should be done along with that of the wholeintestinal tract in each species.
There are so few descriptions on this subject that further comparative observations on other cetaceans should be done and are needed to clarify biologicalmeanings from immunological, ecological and phylogenetical standpoints.
ACKNOWLEDGMENTS

We are greatly indebted to Dr. R. L. Brownell Jr., Department of Vertebrate
Zoology, National Museum of Natural History, Smithsonian Institution, Washington, D.C., who arranged for us to collect Pontoporia. Our sincere thanks are due to
Dr. K. Takahashi, Department of Anatomy, Sapporo Medical College, who gave
us valuable suggestions and advice for our study. The technical assistance of Mr.
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A. Mori, Risto-Technical Center, Sapporo Medical College, is also acknowledged.
REFERENCES
COWAN, D. F. and R. L. BROWNELL Jr., 1974. Gut-associated lymphoepithelial organ ("anal-tonsil")in the gray whale. In: Functional anatomy of marine mammals. Vol. 2., ed. by R.J. Harrison, pp. 321327., Academic Press, London, New York and San Francisco.
ORTMANN, R., 1960. Uber den lymphatischen Apparat der Analregion und die sogenannte "Analtonsille"
bei Siiugetieren. Eine vergleichend histologishe Studie. ,Z. Anal. Entwicklungs., 121: 459-477.
TAKAHASHI, K. and F. YAMASAKI, 1972. Digestive tract of Ganges dolphin, Platanistagangetica. II. Smalland large intestines. Okajimas Fol. anat.jap., 48: 427-452.
Uvs, C.J. and P. B. BEST, 1966. Pathology of lesions observed in whales ftense<l at Saldanha Bay, South
Africa. ]. Comp. Path., 76: 407-412.
YAMASAKI, F., K. TAKAHASHI and T. KAMIYA, 1975. Digestive tract of La Plata dolphin, Pontoporia blainvillei. II. Small and large intestines. Okajimas Fol anat.jap., 52: 1-26.

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EXPLANATION OF PLATE
PLATE I
Fig. I.

Inner surface of the oral three-fourths of the anal canal of a Platanista
gangetica (body length, 105.5 cm). The oral half of the surface is uneven in appearance and longitudinal folds are present on the posterior half. Anal tonsils
in Platanista are mainly present in the oral half of the anal canal. An arrowshows one of the tonsilar crypts which are usually fairly difficult to distinguishwith the naked eye. A recto-anal epithelial transition is clearly visible at the topof the photograph. Hollows seen in the longitudinal folds at the bottom of the
figure are not tonsilar crypts. X 3.3

Fig. 2. A photomicrograph of a well developed anal tonsil of a Platanista (113 cm).
Although no opening of the crypt is seen in this section, the surface epithelium
invaginates into the subjacent lymphoid tissue to form a central crypt, which ramifies into subdivisions. Germinal centers can be seen in places within the lymphoid tissue. x 15
Fig. 3. A cross section of the anal canal of the Platanista in Figure 1. In younger
specimens anal tonsils are rather small in size compared with the larger animals.
A tonsilar crypt shown by the arrow corresponds to the arrow in Figure 1. Anal
tonsils are grouped in places within the submucosa. Small glands are visible near
the anal tonsils. X 9
Fig. 4. A cross section of the oral part of the anal canal of an lnia geojfrensis (bodylength, 204 cm). Accumulations of lymphoid tissue are present but formation of
the anal tonsil cannot be seen in the lnia. Germinal centers are poorly developed.

x9
Fig. 5. A cross section of the oral part of the anal canal of a Pontoporia blainvillei(body length, 171 cm). No lymphoid tissue can be seen in any part of the anal
canal. Submucosa is highly vasculized. X 9

Sci. Rep. Whales Res. Inst.,

No. 29, 1977.

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