Sensory Physiology of Aquatic Lower Vertebrates: Satellite Symposium of the 28th International Congress of Physiological Sciences, Keszthely, Hungary, 1980

Advances in Physiological Sciences, Volume 31: Sensory Physiology of Aquatic Lower Vertebrates covers the proceedings of the symposia of the 28th International Congress of Physiology. The book presents 17 papers that detail advance findings in the sensory physiology of aquatic lower vertebrates. The coverage of the text includes electroreceptors in Indian catfish teleosts; electroreceptive microampulla in the African mudfish Clarias lazera; and species specificity of electric organ discharges in a sympatric group of gymnotoid fish from Manaus. The book also presents comparative studies, such as the sex differences in the electric organ discharge of Eigenmannia virescens and the effect of gonadal maturation; and behavioral studies, such as social behavior in mormyrid fish. The book will be of great interest to marine biologists, ethologists, and zoologists.

• Language: English
• Publisher: Elsevier Science
• Release date: Oct 22, 2013
• ISBN: 9781483190204

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Czeh

ELECTRORECEPTORS IN INDIAN CATFISH TELEOSTS

C.B.L. Srivastava and M. Seal,     Department of Zoology, University of Allahabad, Allahabad, India

SUMMARY

Four Indian freshwater catfishes, viz. Clarias batrachus, Heteropneustes fossilis, Rita rita and Mystus vittatus, have been investigated for detailed structure of their ampullary organs. The ontogenetical development of these organs was followed in one of these catfishes, namely H. fossilis, using light microscopy. It was found that the organs of these catfishes essentially resemble those of freshwater catfishes of other tropical parts of the world and of tropical freshwater weakly electric teleosts of S. America and S. Africa. The ecological conditions of the water and nocturnal habit of the fishes in the case of the Indian species parallels those of fishes of other countries. All these facts suggest an electroreception function for the ampullary organs of Indian species as well. Developmental studies show that in H. fossilis, fully formed ampullary organs are present in the larval stage, indicating that these may be functional at this stage of life as well as assisting in the location of food and the detection of enemies.In the ontogeny of the ampullary organ, histogenesis shows a primordial stage very similar to that found in the development of ordinary lateral line organs. This feature, which we report here for the first time, is the first developmental evidence in favour of homology between these two categories of organs. It has also been brought to light that the canal of the ampullary organ has a developmental origin independent of neuromastic origin of the sensory epithelium of the ampulla. A constant accompaniment of the ampullary organs of freshwater catfishes seems to be a compact collagen layer in the dermis.

INTRODUCTION

In India a number of catfishes inhabit tropical waters (muddy bottoms of ponds and rivers, swamps and paddy fields) in which visibility is poor owing to increased turbidity. Still other catfishes live in clear water of rivers, but the nocturnal habit of these catfishes renders eyes useless. These fishes, eyes notwithstanding, may, thus, be thought to depend on a sense other than vision for normal perception of the surroundings. The electroreception mechanism, known to occur in a number of tropical freshwater teleosts including some catfishes inhabiting conditions of poor visibility (Lissmann and Machin, 1958), is also a likely candidate for Indian catfishes. Histological demonstration of ampullary organs (small pit organs) in these fishes would be the first requirement for such a suggestion. Preliminary reports have indicated the occurrence of such electroreceptor organs in Indian catfishes (Mittal, 1968; Lahiri and Kapoor, 1975; Srivastava et al., 1978; Seal and Srivastava, 1978). The present paper aims at a detailed investigation of the structure of the ampullary organs in four Indian catfishes: Clarias batrachus, Heteropneustes fossilis, Rita rita and Mystus vittatus, and of the development of the ampullary organs in one of these, namely H. fossilis. It may be pointed out that development of ampullary organs is not known, except for a brief report on Parasilurus (Sato, 1956), owing to the difficulty in procuring the developmental stages of electric and nonelectric electroreceptive teleosts.

MATERIALS AND METHODS

The catfishes were procured from local markets or collected from fishing sites on rivers. Pieces of skin from head and trunk, especially from the dorsal surface, were excised and fixed in Bouin’s fluid by immersion. Material was then processed for paraffin microtomy and 6 to 8 μm thick sections were cut. Staining was done with Haematoxylene-eosin. Developmental stages of H. fossilis consisted of spawn from induced breeding*, which was raised in the laboratory. Entire larvae were processed as above and serially sectioned. Ampullary organs were first located in an advanced stage and then these were traced back through intermediate developmental stages to their earliest recognisable stage.

OBSERVATIONS

I Structure of the ampullary organs

a) Clarias batrachus (Linn.) (Figs. 1 and 2)

Each ampullary organ has a fairly long, narrow intraepidermal canal, c. 100 um in length, leading to a single ampulla or to two or three ampullae, each of which rests on the basement membrane. The ampulla is lined with a sensory epithelium. The canal wall is composed of very compactly packed two to three layers of flat cells. These cells which line the canal lumen up to where it opens on the surface are continuous with the surface layer of the epidermis. The cells are well demarcated from ordinary cells of the middle layer and surface layer of the epidermis in size, shape and orientation. Some gland cells occur in the canal wall especially at the junction between the canal and the ampulla. The sensory epithelium shows two distinct categories of cells: the smaller but more prominent sensory cells, and the larger and more numerous supporting cells. The sensory cells are exposed to the lumen of the ampulla by an appreciable apical surface. No hair-like process is present on the apical surface. No cupula is seen in the lumen.

Fig. 1 Transverse section of skin of C. batrachus showing an ampullary organ in vertical section; inset shows a magnified view of the ampullary organ. Note the canal wall, the sensory cells and the thick collagen layer in the dermis. × 30.

Fig. 2 Tangential section of the epidermis of C. batrachus showing the canal in transverse section. Note the canal wall and the lumen. × 300.

The skin has a moderately thick epidermis, c. 150 μm in thickness. The dermis shows a thick layer of densely set collagen bundles just beneath the basement membrane.

b) Heteropneustes fossilis (Bloch) (Figs 3 – 5)

The structure of the ampullary organ is similar to that described for C. batrachus. The canal wall is very distinct and clearly distinguishable from the adjacent epidermal cells. The canal wall is continuous with the surface layer of the epidermis at the opening of the ampullary organ. The canal length measures c. 80 μm. The skin is provided with a very thick layer of compact collagen bundles, lying next to the basement membrane. The epidermis measures c. 120 μm in thickness.

Fig. 3 An ampullary organ of H. fossilis in vertical section. Note the canal wall. × 260.

Fig. 4 Tangential section of the epidermis of H. fossilis showing the canal in transverse section. Note the canal wall and the lumen. × 550.

Fig. 5 Transverse section of the skin of H. fossilis. Note the thick collagen layer in dermis. × 220.

c) Rita rita (Ham.) (Figs. 6 – 8)

The skin has a very thick epidermis measuring c. 400 μm in thickness. The canal of the ampullary organ, however, is not more than c. 40 um in length. A dermal papilla supports the ampullary organ high up in the epidermis, compensating the shortness of canal length relative to thickness of epidermis. The canal wall is very prominent. Dermis has a very conspicuous and exceptionally thick layer of compact collagen bundles just below the basement membrane.

Fig. 6 An ampullary organ of R. rita in vertical section. Note the canal wall. × 400.

Fig. 7 Tangential section of the epidermis of R. rita showing the canal in transverse section. Note the canal wall and the lumen. × 400.

Fig. 8 Transverse section of the skin of R. rita. Note the very thick collagen layer in dermis. × 70.

d) Mystus vittatus (Bloch) (Figs 9 and 10)

The ampullary organ in this case differs from that of the above three catfishes in having a very short (c. 20 μm) and broad canal which distorts the ampullary profile into a wide-mouthed pit. However, the canal wall is still very clearly distinguishable as composed of specialised flat cells. The sensory epithelium is very prominent. The epidermis appears thin, measuring c. 50 μm in thickness. But in the dermis a thick layer of densely packed collagen bundles is present below the basement membrane.

Fig. 9 An ampullary organ of M. vittatus in vertical section. Note the canal wall. × 530.

Fig. 10 Transverse section of the skin of M. vittatus. Note the collagen layer in the dermis. × 230.

II Development of the ampullary organ in H. fossilis

(i) 13 mm fry

A number of primordia of ampullary organs are located in the dorsal surface of the trunk and tail region, especially at the base of the median dorsal fin fold, on each side. Each primordium appears as a bulging structure in the otherwise thin uniform sheet of epidermis. The primordium consists of a round vesicular body in which a pronounced apical space lies at the top of a single layer of columnar cells. The surface layer of extremely flat cells of the surrounding epidermis is continuous over the primordium. The primordium rests on the basement membrane. The epidermis at this stage is very thin, about 5 μm, consisting of 2 to 3 cells in thickness.

(ii) 14 mm fry

The primordia appear as large closed ampullae. In each of these the cells which line it in a single layer show the beginnings of differentiation into two cell types: large, oval, dark staining sensory cells with a large nucleus, and slender supporting cells with a small nucleus. The apical space has now given place to a large ampullary lumen. On the outerside the ampulla is still covered with the surface layer of epidermal cells. The epidermis has increased in thickness, largely due to a great increase in the size of gland cells of its middle layer. There is a definite increase in the number of developing primordia, as compared to the previous stage.

(iii) 15 mm fry

While the primordia still remain at closed ampulla stage, a canal has appeared close to the ampulla in many cases. The canal appears as a distinct blind tubular structure, representing an invagination from the surface layer of the epidermis. The wall of this structure is composed of specialised cells that are continuous with those of the surface layer of the epidermis. The blind end of the canal rudiment lies very close to the ampulla but does not open into it. As is clearly revealed in serial sections, a gap of 24 to 32 μm remains between the two.

Fig. 11 Transverse section of skin of fry of H. fossilis at 13 mm stage showing an early primordium of ampullary organ. Note the apical space within the vasicular body. × 550.

Fig. 12 Same as above at 14 mm stage showing a closed ampulla with differentiated sensory cells. × 550.

Fig. 13 Same as above at 15 mm stage showing invaginated surface layer of epidermis into a blind tubular canal rudiment (A closed ampulla situated at 30 μm away from the blind end of the canal rudiment, without any communication with it, is present in the section series). × 550.

Fig. 14 Same as above at 16 mm stage showing an ampullary organ in which the canal rudiment has just opened into the ampulla. × 550.

Fig. 15 Same as above at 18 mm stage showing a well-formed ampullary organ. × 550.

(iv) 16 mm fry

More primordia have appeared. The more advanced among these show open communication between the lumen of the ampulla and that of the canal. The length of canal is, however, short and there is no appreciable increase in the thickness of the epidermis. Thus for the first time at this stage open, though miniature, ampullary organs are formed.

(v) 18 mm fry

Well-formed ampullary organs are developed. In each a conspicuous canal with distinct wall is discernible. The length of the canal shows an increase and a definite change in orientation with relation to the ampulla, i.e. from inclined position of the previous stage to vertical position. The epidermis also shows a clear increase in thickness.

(vi) 20–22 mm fry

Many more well-developed ampullary organs are visible.

The stages in development of H. fossilis designated above are found to be rather retarded in development as compared to the normal growth described by Thakur et al., 1974.

DISCUSSION

The ampullary organs of the four Indian catfishes resemble essentially the ampullary organs of tropical freshwater catfishes from other parts of the world, viz. N. American and European Aminurus (Mullinger, 1964), Japanese Parasilurus (Sato, 1956; 1969) and Asiatic Kryptopterus (Wachtel and Szamier, 1969) as well as those of tropical weakly electric freshwater teleosts of S. America and S. Africa (gymnotids, gymnarchids and mormyrids; Szabo, 1965; 1974). Electroreception is fairly well established for these latter fishes (Lissmann, 1958; Bennett, 1971; Szabo and Fessard, 1974), and it is believed that the ampullary organs serve as electroreceptors (Bullock, 1974). Electric sensitivity in catfishes as demonstrated for Clarias (Lissmann and Machin, 1963) is found to be no less significant than in weakly electric teleosts. Clarias, Saccobranchus (Heteropneustes), Amiurus, Silurus, etc., are known to respond to moving magnets (Lissmann and Machin, 1963). It is reasonable to presume, therefore, that electroreception operates in the four Indian catfishes also, with ampullary organs serving as electroreceptors. The habit and habitat of these fishes fully justify the adaptive advantage of electroreception. All the four catfishes are principally nocturnal and resistant to foul waters, and two of these, C. batrachus and H. fossilis, live in turbid waters and are the accessory air breathing type.

The findings on development of ampullary organs in H. fossilis suggest that at least for this species electroreception may be thought to be in operation already in the larval stages when yolk is absorbed and open ampullary organs are formed. Since the spawning occurs in muddy conditions, larval stages are passed in water of poor visibility. Electroreception at this stage of free swimming and active feeding may be looked upon as a feature of larval adaptation. The larvae might be using electroreception for location of microorganisms (ciliates, rotifers) for food and for detection of enemies, Cyclops in particular, for avoidance. The fact that the larvae mostly remain on the bottom, save for occasional vertical movements for air-breathing (Thakur et al., 1974) points to little role of vision although the eyes are well developed in the larval stages. Open and perfectly formed small pit organs have also been reported in stage 120 h after hatching for Parasilurus asotus (Sato, 1956).

The findings on the ontogenetic development of the ampullary organs in H. fossilis are very interesting. An early stage in the development of the ampullary organ shows the primordium as a round vesicular body of columnar cells in which the cells are directed towards a distinct apical cavity. This stage, it may be recalled, characterises the development of the ordinary lateral line organ in teleosts. First reported by Allis (1889), this stage was later shown to result from a process of invagination of the placode preceding it (Srivastava and Srivastava, 1967). This similarity between the development of ordinary lateral line organs and that of ampullary organs is the first evidence forthcoming from the ontogeny in favour of the proposed homology between these two functionally different catefories of sense organs (Dijkgraaf, 1963; Lissmann and Mullinger, 1968; Srivastava and Srivastava, 1968; Szabo, 1974; Srivastava, 1978). Development subsequent to this stage takes a course in case of ampullary organs different from that followed by ordinary lateral line organs. Two facts have come to light from the present findings. First, the canal tissue does not arise from cells of the neuromastic primordium. Second, the canal is formed by a definite differentiation of specialised epidermal cells organising into a tubular surface invagination. This structure extends towards the ampulla and eventually opens into it. The development of the ampullary organs (the small pit organs of Herrick, 1901) thus turns out to be very different from ordinary pit organs (the large pit organs of Herrick, 1901). The latter are known to arise from a mere increase in thickness of the epidermis outgrowing the height of the sense organ; no differentiated cells border the pit (Srivastava and Srivastava, 1968). The present finding lends full support to the proposed evolutionary derivation of the ampullary organs of non-electric catfishes from ordinary pit organs (Srivastava, 1978) by emphasizing (i) the acquisition in the former of differentiated canal replacing the simple pit of the latter, and (ii) the retention of the same neuromastic sensory homologue in both of these sense organs. In denervated ampullary organs of Clarias and Heteropneustes, following nerve transection, the sensory epithelium alone is found to degenerate and not the canal wall (Das, 1980). This is in agreement with the independence of the canal tissue from sensory epithelium in respect of ontogenetic