Morphology of Lymphoid Organs in a Cichlid Teleost, Tilapia mossambica (Peters) K . SAILENDRI 2 AND VR. MUTHUKKARUPPAN 3 Department of Biological Sciences, Madurai University, Madurai-625021, India

ABSTRACT In Tilapia mossambica organized lymphoid tissues are present in the thymus, head-kidney and spleen, whereas they are lacking in pericardial tissue, liver, mesonephros, intestine and rectum. No lymphoid tissue was observed in the chondrocranium and cartilaginous viscerocranium of young adults. The thymus in Tilapia is encapsulated by thin strands of collagen fibers and consists of outer, middle and inner zones. While middle and inner zones are comparable to the thymic cortex and medulla of higher vertebrates, the homology of the outer zone is not clear. A t the anterior end of the thymus, a loose aggregation of lymphocytes without a definite boundary has been observed. The head-kidney is characterized by the presence of lymphoid follicles, a subcapsular sinus, a hilus-like area and lymphatic vessels. The spleen is grossly divisible into white pulp and red pulp; the white pulp contains only a reticular area without definite lymphoid centers and the latter contains predominantly erythrocytes. Morphological changes in the lymphoid organs associated with immune response have been discussed.

The morphology of various lymphoid organs has been studied in fishes, including cyclostomes (Finstad et al., '64; Good et al., '66). These studies revealed that the development of immunologic capacity is associated with the development of well organized lymphoid centers such as the spleen or thymus, and also of a well developed plasma cell system in chondrostean, holostean and teleostean fishes. In contrast to cyclostomes, teleost, show a definite order of lymphoid tissue development and organization. There is evidence that the thymus plays a key role in the ontogeny of immunologic competence (Miller, '61; Good et al., '62; Cooper and Hildemann, '65; Cooper, '73). Studies by Beard (1894) on elasmobranchs suggested that the thymus is the source of lymphoid cells, ultimately distributed to other peripheral lymphoid organs. In teleosts the head-kidney is also a definite lymphoid organ (Rasquin, '51 ; Smith et al., '67; Chiller et al., '69; Pontius and Ambrosius, '72). However, there is a need for better understanding of the organization of lymphoid tissues and their cellular elements in teleosts. With such information, it would be possible to elucidate the role of lymphoid tissues in the development of immune funcJ. MoK~H.,147: 10S122.

tions as well as structural changes resulting from immunization and immunosuppression. This report is a part of our comprehensive study on the origin, development and functional morphology of the lymphoid system in a species of higher teleost, Tilapia mossambica (Sailendri, '73). It describes the morphology and lymphoid elements of the thymus, head-kidney and spleen. MATERIALS AND METHODS

Adult specimens of Tilapia mossambica (African mouth breeder) were collected from local ponds and a stock was maintained in a large cement tank of about 2 m depth. In the laboratory six to eight fish were maintained in each aquarium with continuous aeration and fed with boiled eggs, bits of earthworm, cooked rice and aquatic plants. A total of 40 adult fish of both sexes, weighing 45-50 gm (standard length, 11.5-12 cm), were used in the present study. The thymus along with its sumunding tissues, head-kidney and spleen were 1 Supported in part by a grant (01-077) from the U. S. National Institutes of Health, under special foreign currency research program (PL-480). 2 With award of Junior Fellowship from University Grants Commission, India. 3 Please send reprint request to VR. Muthukkaruppan.

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dissected out and immediately fixed in Bouin’s fluid, embedded in paraffin and sectioned serially at 6 p. Sections were stained with Harris’ haematoxylin and counterstained with eosin. Some of the sections were stained with orcein-aniline blueorange G to study the distribution of collagen fibers (Margolena and Dolnick, ’51). Cell suspensions from the thymus, spleen and head-kidney were individually prepared by gently rubbing the tissues on stainless steel wiremesh in 1 ml of phosphate-buffered saline (pH 7.2) and cell counts were made in a hemocytometer. For cytological study, blood smears and imprints from spleen, head-kidney and thymus were made, fixed in methanol, rapidly dried in air and stained with May-Grunwald-Giemsa. In addition, other tissues such as liver, mesonephros, heart, intestine, rectum from adult specimens and chondrocranium and cartilaginous viscerocranium of young adults were also processed for histological examinations. RESULTS

Peripheral blood cells of Tilapia In addition to nucleated erythrocytes, the blood contains several types of white cells, namely, neutrophils ( 5 % ) , basophils (3%), small, medium and large lymphocytes (66%). monocytes (23%), thrombocytes (2 % ) and plasma cells (1 % ). The staining properties of these cells are similar to those of mammals. However, there is a difference in nuclear morphology. Nuclei of fish granulocytes are oval as compared to the lobed, granulocytic nuclei of mammals. Thymus The thymus is an opaque whitish organ, situated on either side at the superior corner of the opercular cavity. It lies superficially in close association with the epithelial lining of the opercular cavity; its pointed end faces anteriorly and the broad end posteriorly. It measures about 6 mm X 3 mm X 1 mm (in fish weighing 45-50 gm) and contains 11-1 3 million lymphocytes. Histologically, the thymus is partially separated into lobes by muscle fibers at its posterior end (figs. 1-5). It is fully encapsulated by strands of collagen fibers. Even though the thymus is closely associated with muscle fibers, collagen fibers of the capsule completely encircle it, thereby ex-

cluding the muscle fibers as well as extrathymic lymphoid accumulation (fig. 5). The thymus consists of three zones: the outer, middle and inner. The outer zone is a relatively narrow band which partially encircles the other zones. The middle zone is more deeply stained and is similar to the thymic cortex of higher vertebrates, while the inner zone resembles the thymic medulla (figs. 1-5). The boundaries between these three zones are not sharply delimited. Furthermore, the inner zone is not fully surrounded by the middle zone, as in higher vertebrates; it is exposed at its posterior end as shown in figure 1. Apart from these three zones, there is a loose aggregation of lymphocytes at the anterior side of the thymus, and this is designated as “extra-thymic lymphoid accumulation” (figs. 3, 4). The outer zone consists mostly of thymoblasts which are larger and less chromophilic (fig. 6) than lymphocytes. The middle zone is characterized by dense, tightly packed small lymphocytes (figs. 6, 7). The inner zone (figs. 7, 8) consists of various epithelial cell types and lymphocytes distributed sparingly. Various epithelial cell types such as reticular cells, endothelial cells and Hassall’s corpuscles (fig. 8a) are distributed within the inner zone. Large cystic epithelial cells are also found in this region and they are characterized by the presence of a number of vacuoles occupying the greater part of the cytoplasm, pushing the nucleus to one side (fig. 8b). The thymus is well vascularized by an extensive capillary network associated with the branchial vascular system. These vessels along with the connective tissue enter the gland at the inner zone (figs. 2, 7). Neither a lymph sinus nor lymphatic vessels were observed in the thymus. The extra-thymic lymphoid accumulation does not have thymic organization. It is made up of loose aggregations of lymphocytes with two distinguishable regions (fig. 9). One consists of mainly small lymphocytes with an island of erythrocytes in the center and the other is fdled with large lymphoid cells arranged homogenously (fig. 10). With increasing age, the thymus becomes flattened against the epithelial lining of the opercular cavity, but it remains still visible to the naked eye. An increase in the connective tissue elements in both the capsule

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and subcapsular portions of the parenchyma is also evident. Adipose tissue infiltration, the presence of large cysts, and epithelial islands characterize the process of age involution (Sailendri, '73). Head-kidney The head-kidney refers to the modified pronephros which lies dorsal to the body cavity, just outside the pleuroperitoneum. It extends from the level of thymus in the branchial region to the anterior end of the mesonephros. In adults (weighing 45-50 gm), it measures about 8 to 15 mm in length. It is dark brown and consists of approximately 9-16 million white cells. The head-kidney is encapsulated by thin strands of collagen fibers and includes lymphatic and blood vessels and sinuses (fig. 11). A broad subcapsular or marginal sinus lies directly beneath the capsule which enters at different points into the kidney pulp as trabeculae carrying blood vessels. Toward the posterior end of the head-kidney, a dimpled portion comparable to the hilus of a mammalian lymph node is found. Through this region arteries and veins enter or leave the head-kidney. The head-kidney is mainly a lymphoreticular organ and consists of two different zones, a deeply stained lymphoid zone and a non-lymphoid zone (fig. 12). The former is represented by a number of lymphoid islands or follicles. Each lymphoid follicle consists of tightly packed small lymphocytes at the periphery (fig. 13), and in the center of the follicle large vacuolated cells with dark pigments and a few large lymphocytes are found. The follicle also encloses numerous blood vessels and blood sinuses. The non-lymphoid zone consists of reticular cells, granulocytes and islands of erythrocytes. Lymphatic and blood vessels, and lymph and blood sinuses are also present in this zone (fig. 12). Lymphocytes of all sizes, monocytes, plasma cells, granulocytes (especially basophils and neutrophils) and erythrocytes were identified in the head-kidney (fig. 14). Spleen The spleen is an elongated, flattened structure, measuring about 12 mm in length and 4 mm in thickness (in fish weighing 45-50 gm). It lies along the left side of the stomach, in close association

with the pancreas. It is reddish brown and contains 5 to 9 million white cells. The splenic capsule is not well defined, is rather thin and made up of collagen fibers. Through the anterior end of the capsule, strands of collagen fibers representing the trabeculae traverse the splenic pulp, carrying blood vessels. This splenic blood vessel is trunk-like and gives off many branches toward the periphery of the organ. In addition there is a subcapsular sinus. The interior of the organ contains red and white pulp (fig. 15). The red pulp is fully erythroid with very few lymphocytes. The white pulp comprises reticular centers around the blood vessel. It is small and rather poorly developed, since no identifiable accumulation of lymphocytes is found within the stroma (fig. 15). Imprints of spleen consist of various cell types, namely, lymphocytes, plasma cells, granulocytes, monocytes and erythrocytes (fig. 16). In addition, serial sections of other tissues such as the liver, mesonephros, heart, intestine and rectum from the adult specimens were examined for the presence of lymphoid tissues or aggregations of lymphocytes. However, none was observed. Chondrocranium and cartilaginous viscerocranium from young adults were examined for the presence of bone-marmw-like tissue. Neither the cavity nor the lymphoid accumulation was found in skull and visceral skeleton. DISCUSSION

In Tilapia mossambic, a higher teleost, well defined lymphoid tissues are present in the thymus, spleen and head-kidney. The thymus is a well organized lymphoepithelial organ which resembles the thymus of higher vertebrates in general. It is organized into three identifiable regions, i.e., outer, middle and inner zones. This type of organization has also been reported in another teleost fish, Astyanax (Hafter, '52). Although Hafter ('52) has suggested that the thymoblasts in the outer zone give rise to small thymocytes, the function of the outer zone is still not known. Hassall's corpuscles are well represented in the thymus of Tilapia, whereas they were reported to be absent in the eel, Anguilla uulgaris (Von Hagen, '36), in Astyanax (Hafter, '52) and in Lepomis (Smith et al., '67). Only a primitive type of corpus-

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cle was observed in the primitive bony fish Polyodon spathula (Good et al., ’66). The function of Hassall’s corpuscles is still unknown in fishes and in mammals (Blau and Veall, ’67). Cystic epithelial cells are characteristic cell types found in the thymic medulla or inner zone of Tilapia and in a variety of other species including mice (Mandel, ’70), guinea pigs (Mandel, ’68), snakes (Raviola and Raviola, ’67) and the amphibian A m b y stoma m e x i c a n u m (Klug, ’67). It has also been reported in the teleost Astyanax (Hafter, ’52). The presence of such unique cells in a wide range of animals suggests that they may indeed subserve some highly specialized functions. For instance, they have been shown to incorporate labeled glucosamine (Clark, ’68) and to synthesize PASpositive material (Mandel, ’68). On the basis of these findings it has been proposed that they produce a sulphated lymphopoietic hormone or the thymic factor. This view is further supported by the recent observation that this type of epithelial cell is absent in the thymus of “Nude” mice. In fact, the immunological deficiency in the “Nude” mouse might be due to the absence of such cystic epithelial cells (Cordier, ’74). Clearly much remains to be learned about the role of thymic epithelial cells in normal thymic functions. As in Tilapia, a double band of endothelial cells extends through the thymus in Amia (Hill, ’35), again with unknown function. The phenomenon of age involution in the thymus of teleosts has been described. Most investigators, however, agree that the process is characterized by an overall reduction in the size of the gland, proliferation of connective tissue and decrease in thymocyte number (cf. Hafter, ’52). Lele (‘33) described in the plaice, structures called “Coagulum Balls” which were small spherical masses, containing nuclei of thymus, reticular cells and dark granules. The number and size of these “Coagulum Balls” increased with age. Adipose tissue idiltration into the thymus was reported in the eel (Von Hagen, ’36). In Tilapia, the presence of cysts and epithelial islands and progressive infiltration of connective tissue and adipose tissue characterize the process of age involution (Sailendri, ’73). It is apparent that considerable variation exists among different species in the time

the thymus begins to undergo age involution. Complete disappearance of the thymus was reported in female trout, the time of its disappearance varying with the individual (Deanesly, ’27). It was too small to be seen with the naked eye in Astyanax at about 34 weeks of age (Hafter, ’52); but in Tilapia it is present in all the age groups, from the hatchling to three years old (Sailendri, ’73). In Tilapia an accumulation of lymphocytes just outside the thymus was observed. Such structures have not been described in other fishes (Hafter, ’52). Since this structure appears to be similar in its cellular contents to that of a n extra-thymic accumulation of lymphocytes in the frog (Cooper, ’67; Manning and Horton, ’69), i t is named accordingly. Further it was observed even in the young adult stage (2.5 months) of Tilapia (Sailendri, ’73). The splenic white pulp of Tilapia is a rather poorly developed reticular tissue without well defined lymphoid centers. But after antigenic stimulation, increase in lymphoid population and also lymphoid aggregation around the reticular area is observed (Sailendri, ’73; Sailendri and Muthukkaruppan, ’75). Among primitive bony fishes (gar and paddlefish) however, the white pulp of normal fish is well defined, with lymphoid centers around the reticular area (Finstad et al., ’64). Further study is needed in other species of higher teleosts in order to characterize the phylogeny of splenic structure. The head-kidney in Titapia is characterized by the presence of lymphoid follicles, a subcapsular sinus, hilus-like area and lymphatic vessels. In the embryonic condition, head-kidney is involved in excretory function (pronephros), but in adults it is modified into a bulk of lymphoid tissue (Sailendri, ’73). In addition to its lymphoid organization, cellular changes associated with antigenic stimulation and the presence of antibody-producing cells (Sailendri and Muthukkaruppan, ’75) suggest that the head-kidney bears functional and possibly structural similarity to the mammalian lymph node. The lymphoid nature of the head-kidney was also reported in other species of teleosts (Rasquin, ’51; Smith et al., ’67; Chiller et al., ’69). The teleostean thymus is found to be similar to that of higher vertebrates both struc-

LYMPHOID ORGANS IN TILAPIA

turally and developmentally (Sailendri, ’73). Further, it subserves a central lymphoid function. Thymectomy during a young adult stage of Tilapia has been shown to suppress antibody response to sheep red blood cells and delay allograft reaction (Sailendri, ’73). On the other hand, antibody-secreting cells were detected in the thymus of Tilapia after antigenic stimulation. Therefore, the basic problem is to delineate the origin of such antibody-producing cells in the thymus of Tilapia, as discussed elsewhere (Sailendri and Muthukkaruppan, ’75). In Tilapia the thymus, head-kidney and spleen are the major lymphoid centers. Histological survey of other organs revealed the absence of lymphoid tissue in heart, liver, mesonephros, chondrocranium, cartilaginous viscerocranium and pericardial tissues. However, in lampreys and paddle fish, protovertebral arch and pericardial hematopoietic tissues have been considered to be the equivalent of mammalian bone marrow (Good et al., ’66; Finstad and Fichtelius, ’65). Therefore, it seems incisive to focus on the morphologic development of the lymphoid system from the phylogenetic perspective, especially with reference to the differentiation of B lymphocytes (equivalent of mammalian bone-marrow cells). Further study on the morphological, developmental and functional aspects of immunity in Tilapia might yield information concerning the dichotomy of immune responses. ACKNOWLEDGMENTS

The authors wish to thank Dr. E. L. Cooper, University of California, for reading the manuscript and Mr. RM. Pitchappan for the technical help in preparation of the illustrations. LITERATURE CITED Beard, J. 1894 The development and probable function of the thymus. Anat. Anz., 9: 476486. Blau, J. N.,and N. Veal1 1967 The uptake and localization of proteins. Evans blue and carbon black in the normal and pathological thymus of the guinea-pig. Immunol., 12: 363-372. Chiller, J. M., H. D. Hodgins, V. C. Chambers and R. S. Weiser 1969 Antibody response in rainbow trout (Salrno guairdneri) I. Immuno-competent cells in the spleen and anterior kidney. J. Immunol., 102: 1193-1201. Clark, S. L., Jr. 1968 Incorporation of sulphate by the mouse thymus; its relation to secretion by medullary epithelial cells and to thymic lymphopoiesis. J. Exp. Med., 128: 927-957.

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Cooper, E. L. 1967 Some aspects of the histogenesis of the amphibian lymphomyeloid system and its role in immunity. In: Ontogeny of Immunity. R. T. Smith, P. A. Miescher and R. A. Good, eds. University of Florida Press, Gainesville, pp. 87101. 1973 The thymus and lymphomyeloid system in poikilothermic vertebrates. In: Contemporary Topics in Immunobiology, Vol. 2. A. J. S. Davies and R. L. Carter, eds. Plenum Publishing Co., New York, pp. 13-38. Cooper, E. L., and W . H. Hildemann 1965 Allograft reactions in bullfrog larvae in relation to thymectomy. Transplantation, 3: 446448. Cordier, A. C. 1974 Ultrastructure of the thymus in “Nude” mice. J. Ultrastruct. Res., 47:2640. Deanesly, R. 1927 The structure and development of the thymus in fish with special reference to SaZmofario. Quart. J. Micr. Sci., 71 ; 113-145. Finstad, J., and K. E. Fichtelius 1965 Studies on phylogeny of immunity: immunologic memory and responsive cellular proliferation in lamprey. Fed. Proc., 24: 491. Finstad, J., B. W. Papermaster and R. A . Good 1964 Evolution of the immune response. 11. Morphologic studies on the origin of the thymus and organized lymphoid tissue. Lab. Invest., 13: 490-512. Good, R. A,, A. P. Dalmasso, C. Martinez, 0. K . Archer, J. C. Pierce and B. W. Papermaster 1962 The role of thymus i n development of immunologic capacity in rabbits and mice. J. Exp. Med., 1 1 6 : 773-796. Good, R. A., J. Finstad, B. Pollara and A. E. Gabrielson 1966 Morphologic studies on the evolution of the lymphoid tissues among the lower vertebrates. In: Phylogeny of Immunity. R. T. Smith, P. A . Miescher and R. A. Good, eds. University of Florida Press, Gainesville, pp. 149-168. Hafter, E. 1952 Histological age changes in the thymus of the teleost, Astyanax. J. Morph., 90: 555579. Hill, B. H. 1935 The early development of the thymus in Amia c a l m . J. Morph., 57:61-89. Klug, H. 1967 Submikroskopische Zytologie des Thymus von Ambystoma mexicanurn. Z. Zellforsch., 78: 388401. Lele, S. H. 1933 On the phasical history of the thymus in plaice of various ages with note on the involution of the organ including also notes on the ductless glands in this species. J. Univ. Bombay, 1: 37-53. Manning, M. J., and J. D. Horton 1969 Histogenesis of lymphoid organs in larvae of the South African clawed toad Xenopus Zaeuis. J. Embryol. Exp. Morph., 22: 265277. Mandel, T. 1968 Ultrastructure of epithelial cells in the medulla of the guinea-pig thymus. Aust. J. Exp. Biol. Med. Sci., 46: 755-767. 1970 Differentiation of epithelial cells in mouse thymus. 2.Zellforsch., 106: 49-15. Margolena, L. A , , and E. H. Dolnick 1951 Orceinaniline blue orange G. A differential stain for elastic fibres, collagen, keratin etc.. Stain Tech., 26: 119-121. Miller, J. F. A. P. 1 9 6 1 Immunological function of the thymus. Lancet, 2 : 748-749. Pontius, H., and H. Ambrosius 1972 Contribution to the immune biology of poikilothermic vertebrates. IX. Studies on the cellular mechanism of

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humoral immune reactions in perch Percafluviatilis L. Acta biol. med. germ., 2 9 : 3 1 S 3 3 9 . Rasquin, P. 1951 Effects of carp pituitary and mammalian ACTH on the endocrine and lymphoid system of the teleost, Astyanax mexicanas. J. Exp. Zool., 117: 317-358. Raviola, E., and G. Raviola 1967 Striated muscle cells in the thymus of reptiles and birds: an elmtron microscopic study. Amer. J . Anat., 121 : 623646. Sailendri, K. 1973 Studies on the development of lymphoid organs and immune responses in

the teleost, Tilapia mossambica (Peters). Ph.D. Thesis, Madurai University, Madurai. Sailendri, K., and VR. Muthukkaruppan 1975 Immune responses to soluble and cellular antigens in teleost, Tilapia mossambica. J. Exp. Zool., 191: 371-383. Smith, A. M., M. Potter and E. B. Merchant 1967 Antibody-forming cells in the pronephros of the teleost, Lepomis macrochirus. J. Immunol., 9 9 : 876-882. Von Hagen, F. 1936 Die wichtigsten Endokrinen des Flussaals. Zool. Jahrb., 61 : 467-538.

PLATE 1 EXPLANATION O F FIGURES

1 5

Serial sagittal sections of adult thymus of Tilapia mossambica passing through different regions.

1

Showing outer zone (Oz), middle zone (Mz) and inner zone (Iz) of thymus. Muscle fibers (Mf) are at the posterior end. X 10.

2

Showing outer (Oz), middle (Mz) and inner zone (12). Within thelatter are large blood vessels (Bv). Muscle fibers (Mf) are seen between middle and inner zones. X 10.

3

Showing middle (Mz) and inner zones (Iz)of thymus, and extra-thymic lymphoid accumulation (Et) at the anterior end. Muscle fibers (Mf) and adipose tissue (At) are adjacent to lymphoid tissue. x 10.

4

Showing a portion of middle (Mz) and inner zones (Iz)of thymus along with a section of the complete extra-thymic lymphoid accumulation (Et). Muscle and adipose tissue (At) separate the m a s s e s of lymphoid tissues. X 13.

LYMPHOID ORGANS IN TILAPIA K. Sailendri and VR. Muthukkaruppan

PLATE I

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PLATE 2 E X P L A N A T I O N OF FIGURES

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5

Cross section of thymus showing outer ( 0 2 ) and middle (Mz) zones. Outer zone contains collagen fibers. x 10.

6

Sagittal section of thymus showing outer ( O z ) , middle (Mz) and inner zones (12). x 200.

7

Sagittal section of thymus showing deeply stained middle zone (Mz) with tightly packed lymphocytes and the inner zone (Iz) with prominent blood vessel (Bv). X 200.

8

Enlarged view of thymic inner zone showing loosely distributed lymphocytes (Ly), reticular cells (Rc), Hassall's corpuscles (Hc) and cystic epithelial cell (C). X 1500.

LYMPHOID ORGANS IN T I L A P I A K. Sailendri and VR. Muthukkaruppan

PLATE 2

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PLATE 3 E X P L A N A T I O N O F FIGURES

118

9

Extra-thymic lymphoid accumulation, consisting of loosely aggregated lymphoid cells. Two distinguishable regions ( R , , R2) a r e illustrated further in figure 10. X 60.

10

Enlarged view of a portion of figure 9 showing the region (RI) with tightly packed small lymphocytes (S1) surrounding a central accumulation of erythrocytes (Er), a n d the other region (R2) containing large lymphoid cells (Ll). X 650.

11

Sagittal section of head-kidney showing blood vessels (Bv), lymphatic vessels (Lv) a n d subcapsular sinus (Sc). X 10.

12

Section of head-kidney showing lymphoid zone with lymphoid follicles (L) and nonlymphoid zone ( N ) containing blood sinus (Bs) and blood vessel (Bv). X 250.

LYMPHOID ORGANS I N T I L A P I A K . Sailendri and VR. M u t h u k k a r u p p a n

PLATE 3

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PLATE 4 EXPLANATION OF F I G U R E S

120

13

Enlarged view of the peripheral region of a lymphoid follicle in headkidne; showing blood-sinGs (Bs) and highly concentrated lymphocytes (Ly). X 850.

14

Imprint of head-kidney showing the large lymphocytes (Ll), medium lymphocytes (Ml), small lymphocytes (Sl), granulocytes (Gr), erythrocytes (Er) and monocytes (Mo). X 800.

15

Section of spleen showing white pulp (Wp) containing reticular cells, and red pulp (Rp) containing predominantly erythrocytes (Er). X 1000.

16

Imprint of spleen showing the large lymphocytes (Ll), medium lymphocytes (Ml), small lymphocytes (Sl) and erythrocytes (Er). x 1500.

LYMPHOID ORGANS I N T I L A P I A K. Sailendri a n d VR. Muthukkaruppan

PLATE 4

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Morphology of lymphoid organs in a cichlid teleost, Tilapia mossambica (Peters).

In Tilapia mossambica organized lymphoid tissues are present in the thymus, head-kidney and spleen, whereas they are lacking in pericardial tissue, li...
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