Keio J. Med. 20: 5-14, 1971

THE STRUCTURE OF THE BURSA OF

FABRICIUS IN WILD BIRDS

TADAYOSHI KOBAYASHI

Department of Pathology, School of Medicine,

Keio University, Tokyo

(Received for publication May 8, 1971)

B. Glick et all,2 found that the antibody-producing ability is markedly re

duced when the bursa of Fabricius (abbreviated as BF) of the newly-hatched

chick is removed. Thus the function of this organ which is specific for birds

received a great deal of attention. With the comparative study of bursectomy and

thymectomy, it has been ascertained that the BF and the thymus play distinctive

roles in establishing acquired immunity, i.e., the BF is implicated in the produc

tion of serum antibody and the thymus in the production of cellular immunity.

Moreover, Cooper et a13" investigated the relationship between the central lym

phoid tissue and the peripheral lymphoid tissue, and suggested the separation of

the immunological system of an animal into two systems, i.e., the thymus-de

pendent and the bursa-dependent.

Study of the BF has also expanded into the medical field, however, most of

the studies were done on chickens, while only a few studies concerned the domes

tic fowls such as the Japanese quail5,6 and the duck.

The structure and function of the BF of the Japanese quail had been studied in this laboratory, and research was extended to wild birds since the necessity

arose several years ago. The Passerine species of wild birds were especially subjected to a structural examination of the BF. The newly-hatched chick of

Passer montanus was subjected to bursectomy and then utilized in an immu

nological experiment. The results of this immunological experiment with Passer montanus were different from that for the domestic fowl which had previously been obtained. The details will not be mentioned here, however, because of in

sufficient data due to technical difficulties.

The structure of the BF of wild birds will be explained in this paper to pro

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6 TADAYOSHI KOBAYASHI

vide the basis for elucidating the immunological mechanism in higher mammals

from a phylogenic viewpoint.

MATERIAL AND RESULTS

The author investigated 16 species of Passeres (Passer montanus, Lanius

bucephalus, Sturnus sturnia, Sturnia cineraceus, Motacilla cinerea, Turdus

carides, Emberiza cioides, Hirundo rustica, Erithacus cyanurus, Cettia diphone,

Emberiza yessbensis, Phoenicurus auroreus, Emberiza f ucata, Emberiza rustica,

Padda oryzivora, Parus atricapillus), 4 species of Phasianidae (Phasianus

colchicus, Gennaeus nycthemelus, chicken and Japanese quail), and 1 species each

of Anatidae (duck) and Rallidae (Gallinula chloropus). The BF was observed

macroscopically and microscopically at every stage of growth from the embryo

to maturity in Passer montanus, Lanius bucephalus and Emberiza cioides, while

in other species only one or two young or adult birds were utilized.

a) Although there was a difference in the size of the BF when observed

macroscopically, the location and the shape were almost identical. The BF is an

egg-shaped organ projecting from the back of the cloaca. The connection between

the BF and the cloaca is generally closed after the BF has been formed. How

ever, the open connection of these cavities is quite evident in Sturnur sturnia . The cavity of the BF of Phasianidae was clearly observed, and this fact closely

Fig. 1. Diagrams showing the early developmental stages of the bursa of Fabricius of tubulus-type (A) and plica-type (B) . Left half in each figure shows

epithelial bud formation and right half shows follicle formation .

BURSA OF FABRICIUS IN WILD BIRDS 7

relates to the histological structure which will be mentioned below.

b) As far as the author's observations of birds are concerned, the structure

of the mucosa of the BF can be classified into two types. The first type is already

well known in chickens. A longitudinal plica is formed in the cavity of the BF,

and mucosal epithelium of the plica forms the epithelial bud, centered about which

the lymph follicles grow. The BF of the birds belonging to Phasianidae falls

into this category. This, being named the "plica type," is distinguished from the

second, "tubulus type." The tubular structure in the second type extends in

arborescence from the main duct on the inside of the BF. The epithelial bud

forms at one, side of the tubulus and grows to form the lymph follicles. The

lymph follicles are rarely formed on the wall of the main duct. The "tubulus

type" is common to 16 species of Passeres, and 2 species of water birds.

Fig. 2. Semi-diagramatic representation of "tubulus type" of the bursa of

Fabricius of passerine birds. BF: bursa of Fabricius, R: rectum,

C: cloaca, A: anus.

c) The structure of the lymph follicle of the BF was generally of the in

vaginated type, and the protruded type (ausgestulte Follikel) which had been

8 TADAYOSHI KOBAYASHI

described in Raptores and in Ratinae by Wenckebach7 and Mathis" was never

found. The follicle itself consists of the lymphoepithelial and the lymphoreticular

parts in both the plica and tubulus type, and so the structure of the follicle will

not be discussed.

d) The cecum was observed in relation to the BF. The cecum of birds is

attached to the intestinal tube located on both sides above the anus. It consists

of miliary configuration or of an oat-like granule in the passerine birds, but it is

in the form of a cord in Phasianidae, and in the duck and gallinule belonging to

water birds. The lymphoid tissue in the former had developed remarkably, and

some of them revealed the germinal centers, while few lymphocytes were observed

in the latter.

e) The thymus in wild birds is usually irregular in shape and number and

is in direct contrast with that observed in domestic fowls. The main thymic

gland in passerine birds is large and triangular, located in the submental region whereas the other accessory glands are variable in number and are observed to

be scattered along the bilateral jugular veins. Although accessory glands were

distributed in a relatively regular manner during the embryonic period, none or

a few submiliary thymic glands were grossly found in newly-hatched passerine

weighing 3 to 5 g and in some adult birds. Histologically the cortical area is

scanty or absent in some cases. Therefore the passerine birds are considered to

be easily infected in their natural environment after hatching. The histological

structure of the thymus in wild birds is very similar to that in mammals, but a

considerable number of myoid cells are frequently involved in the tissue.

COMMENT

It has thus been established that there are at least two types, i.e., the plica

type and the tubulus type in the structure of the mucous membrane of the BF.

No such structural differentiation has hitherto been reported. The distinction

between the two types is clear in the early stages of BF formation and involu

tion, but this becomes difficult in a matured stage because of the distorted con

struction of the mucous membrane formed as a result of a marked growth of the

lymph follicles. This is why the difference between the two types has not re

ceived any attention.

A great deal of work has been done over the years, on the other hand, con

cerning the relationship between the lymph follicle and the epithelium . Mathis8 classified them into 3 types; a) a follicle which develops from the invaginated

epithelial bud, b) a disk-like follicle which protrudes on the surface of the mucous

BURSA OF FABRICIUS IN WILD BIRDS 9

membrane, c) a follicle which protrudes in a polyp-like manner on the surface

of 'the mucous membrane. He also noted that type b was observed in Raptores

and type c in Ratinae such as the ostrich and the rhea.

Table 1

* Quoted from a Text-book of Zoology** Mathis8

*** Ackerman & Knouff12

Birds were classified in Table 1 according to the type of the BF structure,

the type of the follicle, the shape of the cecum and its lymphoid tissue (some

of them were quoted from references). It is apparent from the table that there

is some structural correlation between the BF and the cecum, the functional

interaction between them is also speculated.

Only the birds belonging to Phasianidae such as the chicken and the Japa

nese quail in recent years were subjected to bursectomy experiments, and those

belonging to Passeres, which have structural differences in the BF and the cecum

have scaresely been subjected to immunological experimentation. Therefore, one

should be cautious in speculating the function of Aves in general only on the

basis of the results obtained from experiments with chickens. This is the reason

the author is reporting these fundamental data at this time. Furthermore the

BF is known as the cloacal thymus and has been compared with the thymus . This point will also be clarified here. The location and the shape of the BF are

constant (macroscopical immutability) in spite of a difference in their size. How

ever, the histological elements, i.e., the structures of the mucous membrane and

the follicle vary remarkably (histological multiplicity). This is in striking con

trast to thymuses of birds and mammals which vary macroscopically but are con

10 TADAYOSHI KOBAYASHI

stant histologically.

These facts, mentioned above, may give some suggestion to the following

problems which still remain obscure. The problems are 1) it seems that there are some interactions between the thymus and the BF although their functions

appear to be independent with each other; 2) the problem of gut epithelium in

general as the lymphoid organ of the first level as proposed by, Fichtelius9,10; 3) the significance of the absence of lymph nodes generally in birds. The origin

of lymphoid cells in the follicle, on the other hand, has not been definitely estab

lished, while Moore and Owen"l postulated bone marrow cell origin. Relative to

this problem, the author was interested in the development of lymphoid cells in the

follicle of the BF of the tubulus type and observed them electron-microscopically;

however, none of the findings which could be positively discussed were observed.

SUMMARY

The bursa of Fabricius of wild birds, especially that of Passerine birds was

investigated, and it was established that there are two types of structures in the

mucous membrane, i.e., the plica type and the tubulus type. The development and

structure of the lymph follicle in each type were discussed. Morphological cor

relation between the bursa and the cecum was observed, and these results were

collectively arranged in a table. It was also mentioned that the variations of the

structure of the BF should be taken into consideration in future when the func

tion of the BF of birds are discussed.

The author wishes to express his gratitude to Mr. Eiichi Sato, Akita

Prefecture, for the sincere help in collecting the materials.

REFERENCES

1. Glick, B. et at (1956) The bursa of Fabricius and antibody production. Poultry Science 35: 224-225.

2. Glick, B. (1964) The bursa of Fabricius and the development of immunologic competence. The Thymus in Immunobiology, pp. 343-358. Hoeber, New York.

3. Cooper, M. D. et at (1960) The function of the thymus system and bursa system in the chicken. J. Exp. Med. 123: 75-102.

4. Cooper, M. D. et at (1965) Delineation of the thymic and bursal lymphoid systems in the chicken. Nature 205: 143-146.

5. Sato, K. and Sato, K. (1968) The significance of the bursa of Fabricius in Japanese quail. (in Japanese) Igaku-no-Ayugi 64: 523-524.

6. Habu, S. (1970) Antibody production and morphologic studies of lymphoid tissues in Japanese quail. (in Japanese) Proc. Jap. Soc. Reticuloendothelial System 9: 261-267.

BURSA OF FABRICIUS IN WILD BIRDS 11

7. Wenckebach, K. F. (1896) Die Follikel der Bursa Fabricii. Anat. Anz. 11: 159- 160.

8. Mathis, J. (1938) Zum Feinbau der Bursa Fabricii. Z. mikrosk-anat. Forsch. 43: 179-190.

9. Fichtelius, K. E. (1968) The gut epithelium-A first level lymphoid organ? Exp. Cell Res. 49: 89-104.

10. Fichtelius, K.E. et al (1968) Bursa equivalents of bursaless vertebrates. Labor. Tnvastig. 19: 224-R.51

11. Moore, M. A. S. and Owen, J. T. T. (1966) Experimental studies on the development of the bursa of Fabricius. Devel. Biol. 14: 40-51.

12. Ackerman, G. A. and Knouff, R. A. (1964) Lymphocytopoietic activity in the bursa of Fabricius. The Thymus in Immunobiology, pp. 123-146. Hoeber, New York.

EXPLANATION OF PLATES

Photo 1. Transverse and longitudinal section of the bursa of Fabricius of sparrow

embryo (800 mg).

Photo 2. Early developmental stage of lymph follicle, attached to one side of the tubulus (swallow).

Photo 3. BF of a young sparrow. Silver impregnation. T: Tubulus, A: Medulla of

the follicle, which directly connected with the epithelium, B: Cortex of the

follicle, which is separated by argirophil fibers from medulla.

Photo 4. BF of a young swallow.

Photo 5. BF of a young Sturnus sturnia.

Photo 6. BF of a young Gallinula chloropus.

Photo 7. Longitudinal section of BF of a young ringnecked peasant (plica type).Photo 8. The cecum of granular form, which contains distinct lymph follicles (spar

row).

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