CHAPTER XI
THE EVIDENCE OF THE AUDITORY APPARATUS AND THE ORGANS OF THE LATERAL LINE
Lateral line organs.—Function of this group of organs.—Poriferous sense-organs on the appendages in Limulus.—Branchial sense-organs.—Prosomatic sense organs.—Flabellum.—Its structure and position.—Sense-organs of mandibles.—Auditory organs of insects and arachnids.—Poriferous chordotonal organs.—Balancers of Diptera.—Resemblance to organs of flabellum.—Racquet-organs of Galeodes.—Pectens of scorpions.—Large size of nerve to all these special sense-organs.—Origin of parachordals and auditory capsule.—Reason why VIIth nerve passes in and out of capsule.—Evidence of Ammocœtes.—Intrusion of glandular mass round brain into auditory capsule.—Intrusion of generative and hepatic mass round brain into base of flabellum.—Summary.
When speaking of the tripartite arrangement of the cranial nerves, an arrangement which gave the clue to the meaning of the cranial segments, I spoke of the trigeminal as supplying the sensory nerves to the skin in the head-region, and I compared this dorsal system of afferent nerves to the system of epimeral nerves in Limulus which supply the prosomatic and mesosomatic carapaces of Limulus with sensory fibres. I compared the ventral system of eye-muscle nerves with the system of nerves supplying the segmental dorso-ventral somatic muscles of the prosomatic region, and I compared the lateral system of mixed nerves with the nerves supplying the prosomatic and mesosomatic appendages of Limulus. I compared, also, the optic nerves and the olfactory nerves with the corresponding nerves in the same invertebrate group. My readers will see at once that one well-marked group of nerves—the auditory and lateral line system—has been entirely omitted up to the present, it has not even been mentioned in the scheme of the cranial segments; I have purposely reserved its consideration until now, because the organs these nerves supply, though situated in the skin, are of such a special character as to form a category by themselves. These nerves cannot be classed among the afferent nerves of the skin any more than the nerves of the optic and olfactory apparatus; they require separate consideration. A very extensive literature has grown up on the subject of this system of lateral line sense-organs and their innervation, the outcome of which is decisively in favour of this system being classed with the sense-organs supplied by the auditory nerve, so that in endeavouring to understand the position of the auditory nerve, we must always bear in mind that any theory as to its origin must apply to the system of lateral line nerves as well.
Now, although the auditory apparatus is common to all vertebrates, the lateral line system is not found in any land-dwelling animals; it belongs essentially to the fishes, and is, therefore, an old system so far as concerns the vertebrate group. Its sense-organs are arranged along the lateral line of the fish, and, in addition, on the head-region in three well-marked lines known as the supra-orbital, infra-orbital, and mandibular line systems. These sense-organs lie in the skin in a system of canals, and are innervated by a special nervous system different to that innervating adjacent skin-areas. The great peculiarity of their innervation consists in the fact that their nerves all belong to the branchial system of nerves; no fibres arise in connection with the trigeminal, but all of them in connection with the facial, glossopharyngeal and vagus nerves. In other words, although organs in the skin, their nerve-supply belongs to the lateral nervous system which supplies splanchnic and not somatic segments, a system which, according to the theory advanced in this book, originated in the nerves supplying appendages. The conclusion, therefore, is that in order to obtain some clue as to the origin of the sense-organs of this system in the assumed palæostracan ancestor, we must examine the mesosomatic appendages and see whether they possess any special sense-organs of similar function.
Further, considering that the auditory organ is to be regarded as a specially developed member of this system, we must especially look for an exceptionally developed organ in the region supplied by the auditory nerve.
The question of the origin of this system of lateral line sense-organs possesses a special interest for all those who attempt to obtain a solution of the origin of vertebrates, for the upholders of the view that the vertebrates have descended from annelids have always found its strongest support in the similarity of two sets of segmental organs found in annelids and vertebrates. On the one hand, great stress was laid upon the similarity of the segmental excretory organs in the two groups of animals, as will be discussed later; on the other, of the similarity of the segmentally arranged lateral sense-organs.
These lateral sense-organs of the annelids have been specially described by Eisig in the Capitellidæ, and, according to Lang, "there are many reasons for considering these lateral organs to be homologous with the dorsal cirri of the ventral parapodia of other Polychæta, and in the family of the Glyceridæ we can follow, almost step by step, the transformation of the cirri into lateral organs." Eisig describes them in the thoracic prebranchial region as slightly different from those in the abdominal branchial region; in the latter region, the ventral parapodia are gill-bearing, so that these lateral organs are in the branchial region closely connected with the branchiæ, just as is also the case in the vertebrates. It is but a small step from the gill-bearing ventral parapodia of the annelid to the gill-bearing appendages of the phyllopod-like protostracan; so that if we assume that this is the correct line along which to search for the origin of the vertebrate auditory apparatus, then, on my theory of the origin of the vertebrates from a group resembling the Protostraca, it follows that special sense-organs must have existed either on or in close connection with the branchial and prebranchial appendages of the protostracan ancestor of the vertebrates, which would form an intermediate link between the lateral organs of the annelids and the lateral and auditory organs of the vertebrates.
Further, these special sense-organs could not have been mere tactile hairs, but must have possessed some special function, and their structure must have been compatible with that function. Can we obtain any clear conception of the original function of this whole system of sense-organs?
A large amount of experimental work has been done to determine the function of the lateral line organs in fishes, and they have been thought at one time or another to be supplementary organs for equilibration, organs for estimating pressure, etc. The latest experimental work done by Parker points directly to their being organs for estimating slow vibrations in water in contradistinction to the quicker vibrations constituting sound. He concludes that surface wave-movements, whether produced by air moving on the water or solid bodies falling into the water, are accompanied by disturbances which are stimuli for the lateral line organs.
One of these segmental organs has become especially important and exists throughout the whole vertebrate group, whether the animal lives on land or in water—this is the auditory organ. Throughout, the auditory organ has a double function—the function of hearing and the function of equilibration. If, then, this is, as is generally supposed, a specialized member of the group, it follows that the less specialized members must possess the commencement of both these functions, just as the experimental evidence suggests.
In our search, then, for the origin of the auditory organ of vertebrates, we must look for special organs for the estimation of vibrations and for the maintenance of the equilibrium of the animal, situated on the appendages, especially the branchial or mesosomatic appendages; and, further, we must specially look for an exceptional development of such segmental organs at the junction of the prosomatic and mesosomatic regions.
Throughout this book the evidence which I have put forward has in all cases pointed to the same conclusion, viz. that the vertebrate arose by way of the Cephalaspidæ from some arthropod, either belonging to, or closely allied to, the group called Palæostraca, of which the only living representative is Limulus. If, then, my argument so far is sound, the appendages of Limulus, both prosomatic and mesosomatic, ought to possess special sense-organs which are concerned in equilibration or the appreciation of the depth of the water, or in some modification of such function, and among these we might expect to find that somewhere at the junction of the prosoma and mesosoma such sense-organs were specially developed to form the beginning of the auditory organ.
Now, it is a striking fact that the appendages of Limulus do possess special sense-organs of a remarkable character, which are clearly not simply tactile. Thus Gegenbaur, as already stated, has drawn attention to the remarkable branchial sense-organs of Limulus; and Patten has pointed out that special organs, which he considers to be gustatory in function, are present on the mandibles of the prosomatic appendages. I myself, as mentioned in my address to the British Association at Liverpool in 1896, searched for some special sense-organ at the junction of the prosoma and mesosoma, and was rewarded by finding that that extraordinary adjunct to the last locomotor appendage, known as the flabellum, was an elaborate sense-organ. I now propose to show that all these special sense-organs are constructed on a somewhat similar plan; that the structure of the branchial sense-organs suggests that they are organs for the estimation of water pressures; that among air-breathing arthropods sense-organs, built up on a somewhat similar plan, are universally found, and are considered to be of the nature of auditory and equilibration organs; and, what is especially of importance, in view of the fact that the most prominent members of the Palæostraca were the sea-scorpions, that the remarkable sense-organs of the scorpions known as the pectens belong apparently to the same group.
The Poriferous Sense-Organs of the Appendages in Limulus.
On all the branchial appendages in Limulus, special sense-organs are found of a most conspicuous character. They form in the living animal bluish convex circular patches, the situation of which on the appendages is shown in Fig. 58. These organs are not found on the non-branchial operculum. Gegenbaur, who was the first to describe them, has pointed out how the surface of the organ is closely set with chitinous goblets shaped as seen in Fig. 144, A, which do not necessarily project free on the surface, but are extruded on the slightest pressure. Each goblet fits into a socket in the chitinous covering, and is apparently easily protruded by variations of pressure from within. The whole surface of the organ on the appendage is slightly bulged in the living condition, and the chitin is markedly softer here than in the surrounding part of the limb. Each of these organs is surrounded by a thick protection of strongly branching spines. On the surface of the organ itself no spines are found, only these goblets, so that the surface-view presents an appearance as in Fig. 144, B. Each goblet possesses a central pore, which is the termination of a very fine, very tortuous, very brittle chitinous tubule (ch.t.), which passes from the goblet through the layers of the chitin into the subjacent tissue. The goblets vary considerably in size, a few very large ones being scattered here and there. The fine chitinous tubule is especially conspicuous in connection with these largest goblets. In the smaller ones there is the same appearance of a pore and a commencing tube, but I have not been able to trace the tube through the chitinous layers, as in the case of the larger goblets.
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Fig. 144.—A, A Goblet from one of the Branchial Sense-organs of Limulus (ch.t., chitinous tubule); B, Surface View of a Portion of a Branchial Sense-Organ.
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Fig. 145.—The Endognaths of Limulus pushed out of the way on one side in order to show the position of the Flabellum (fl.) projecting towards the crack between the Prosomatic and Mesosomatic Carapaces.
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Gegenbaur, in his picture, draws a straight tubule passing from every goblet among the fine canaliculi of the chitin. He says they are difficult to see, except in the case of the larger goblets. The tubule from the larger goblets is most conspicuous, and is in my sections always tortuous, never straight, as represented by Gegenbaur. A special branch of the appendage-nerve passes to these organs, and upon the fine branches of this nerve groups of ganglion-cells are seen, very similar in appearance to the groups described by Patten on the terminal branches of the nerves which supply the mandibular organs. At present I can see no mechanism by which the goblets are extruded or returned into place. In the case of the Capitellidæ, Eisig describes retractor muscles by means of which the lateral sense-organs are brought below the level of the surface, and he imagines that the protrusion is effected by hydraulic means, by the aid of the vascular system. In the branchial sense-organs of Limulus there are no retractor muscles, and it seems to me that both retraction and protrusion must be brought about by alterations of pressure in the vascular fluids. Certainly the cavity of the organ is very vascular. If this be so, it seems likely enough that such an organ should be a very delicate organ for estimating changes in the pressure of the external medium, for the position of the goblets would depend on the relation between the pressure of the fluid inside the organ and that on the surface of the appendage. Whether the chitinous tubule contains a nerve-terminal or not I am unable to decide from my specimens, but, judging from Patten's description of the similar chitinous tubules belonging to the mandibular organs, it is most highly probable that these tubules also contain a fine terminal nerve-fibre.
These organs, then, represent segmental branchial sense-organs, of which it can be said their structure suggests that they may be pressure-organs; but the experimental evidence is at present wanting.
Passing now from the branchial to the prosomatic region, the first thing that struck me was the presence of that most conspicuous projection at the base of the last locomotor appendage, which is usually called the flabellum, and has been described by Lankester as an exopodite of this appendage. It is jointed on to the most basal portion of the limb (cf. Fig. 155), and projects dorsally from the limb into the open slit between the prosomatic and mesosomatic carapace, as is seen in Fig. 145 (fl.). Of its two surfaces, the undermost is very convex and the uppermost nearly flat from side to side, the whole organ being bent, so that when the animal is lying half buried in sand, entirely covered over by the prosomatic and mesosomatic carapaces except along this slit between the two, the upper flat or slightly convex surface of the flabellum is exposed to any movement of water through this slit, and owing to its possessing a joint, the direction of the whole organ can be altered to a limited extent. The whole of this flat upper surface is one large sense-organ of a striking character, thus forming a great contrast to the convex under surface, which is remarkably free from tactile spines or special sense-organs.
The nerve going to the flabellum is very large, almost as large as the nerve to the rest of the appendage, and the very large majority of the nerve-fibres turn towards the flat, uppermost side, where the sense-organ is situated. Between the nerve-fibres (n.) and the chitinous surface containing the special sense-tubes masses of cells (gl.) are seen, as in Fig. 146, apparently nerve-cells, which form a broad border between the nerve-fibres and the pigmented chitinogenous layer (p.). On the opposite side, nothing of the sort intervenes between the pigmented layer and the blood-spaces and nerve-fibres which constitute the central mass of the flabellum.
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Fig. 146.—Section through Flabellum. |
Fig. 147.—Section parallel to the Surface of Flabellum, showing the Porous Terminations of the Sense-Organs and the Arrangement of the Canaliculi round them.
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At present I am inclined to look upon this mass of cells as constituting a large ganglion, which extends over the whole length and breadth of the upper surface of the flabellum. At the same time, my preparations are not sufficiently clear to enable me to trace out the connections of these cells, especially their connections with the special sense-organs.
Fig. 148.—Section through the three Sense-Organs of Flabellum.
In Fig. 148 I give a magnified representation of a section through three of these flabellar sense-organs. As is seen, the section divides itself into four zones: (1) the chitinous layer (ch.); (2) the layer of pigment (p.) and hypodermal cells; (3) the layer of ganglion-cells (gl.); and (4) the layer of nerve-fibres (n.) and blood-spaces (bl.). The chitinous layer is composed of the usual three zones of the Limulus surface—externally (Fig. 148), a thin homogeneous layer, followed by a thick layer of chitin (3), in which the fine vertical tubules or canaliculi are well marked; the external portion (2) of this layer is differentiated from the rest by the presence of well-marked horizontal layers in addition to the canaliculi.
In this chitinous layer the special sense-organs are found. They consist of a large tube which passes through all the layers of the chitin except the thin homogeneous most external layer. This tube is conical in shape, its base, which rests on the pigmented layer, being so large and the organs so crowded together that a section of the chitin across the base of the tubes gives the appearance of a honeycomb, the septa of which is all that remains of the chitin. This large tube narrows down to a thin elongated neck as it passes through the chitin, and then, at its termination, bulges out again into an oval swelling (cap.) situated always beneath the homogeneous most external layer of chitin. Within this tube a fine chitinous tubule (ch. t.) is situated similar to that seen in the branchial sense-organs; it lies apparently free in the tube, not straight, but sinuous, and it passes right through all the chitinous layers to open at the surface as a pore; in the last part of its course, where it passes through the most external layer (1) of chitin, it lies always at right angles to the surface.
If the flabellum be stained with methylene blue and acid fuchsin, then all the canaliculi in the chitin show up as fine red lines, and present the appearance given in Fig. 148, and it is seen that each of the terminations of the tubules is surrounded in the homogeneous layer of chitin by a thick-set circular patch of canaliculi which pass to the very surface of the chitin, while the canaliculi in other parts terminate at the commencement of the homogeneous layer and do not reach the surface. Further, the contents of the oval swelling, and, indeed, of the tube as a whole, are stained blue, the chitinous tubule being either unstained or slightly pink in colour. We see, then, that the chitinous tubule alone reaches the surface, while the large tube, which contains the tubule, terminates in an oval swelling, which often presents a folded or wrinkled appearance, as in Fig. 149 (see also Patten's Fig. 1, Plate I.). This terminal bulging of the tube is reminiscent of the bulging in the chitinous tubes of the lyriform organs of the Arachnida, as described by Gaubert, and of the poriferous chordotonal organs in insects, as described by Graber (see Fig. 150). This terminal swelling is filled with a homogeneous refringent mass staining blue with methylene blue, in which I have seen no trace of a nucleus; through this the chitinous tubule makes its way without any sign of bulging on its part. Patten, in his description of the sense-organs on the mandibles of Limulus, which are evidently the same in structure as those on the flabellum, refers to this homogeneous mass as a coagulum. I doubt whether this is an adequate description; it appears to me to stain rather more readily than a blood-coagulum, yet in the sense of being structureless it resembles a coagulum.
The enormous number of these organs crowded together over the whole flat surface of the flabellum produces a very striking appearance when viewed on the surface. Such a view presents an appearance resembling that of the surface-view of the branchial sense-organs; in both cases the surface is covered with a great number of closely set circular plaques, in the centre of each of which is seen a well-marked pore. The circular plaques in the case of the flabellum are much smaller than those of the branchial sense-organs, and clearly are not protrusible as in the latter organs, the appearance as of a plaque being due to the ring of thickly-set canaliculi round the central tubule, as already described. When stained with methylene blue, the surface view of the flabellum under a low power presents an appearance of innumerable circular blue masses, from each of which springs a fine bent hair, terminating in a pore at the surface. The blue masses are the homogeneous substance (cap.) of the bulgings seen through the transparent external layer of chitin, and the hairs are the terminal part of the chitinous tubules. Patten has represented their appearance in the mandibles in his Fig. 2, Plate I.
The large tubes in the chitin alter in shape according to their position. Those in the middle of the sensory surface of the flabellum, in their course through the chitinous layers, are hardly bent at all; as they approach the two lateral edges of this surface, their long thin neck becomes bent more and more, the bending always being directed towards the middle of the surface (see Fig. 146); in this way the chitinous tubules increase more or less regularly in length from the centre of the organ to the periphery. The large basal part of the conical tube contains, besides the chitinous tubule, a number of nuclei which are confined to this part of the tube; some of these nuclei look like those belonging to nerve-fibres, others are apparently the nuclei of the chitinogenous membrane lining the tube. I have never seen any sign of nerve-cells in the tube itself.
The only other kind of sense-organ I have found in connection with these sense-organs are a few spike-like projections, the appearance of which is given in Fig. 149. I have always seen these in the position given in Fig. 146 (sp.), i.e. at the junction of the surface which contains the sense-organs and the surface which is free from them. They are, so far as I have seen, not very numerous; I have not, however, attempted to examine the whole sense-organ for the purpose of estimating their number and arrangement.
As is seen in Fig. 149, they possess a fine tubule of the same character as that of the neighbouring sense-organs, which apparently terminates at the apex of the projecting spike. They appear to belong to the same group as the other poriferous sense-organs, and are of special interest, because in their appearance they form a link between the latter and the poriferous sense-organs which characterize the pecten of the scorpion (cf. Fig. 152, C).
Fig. 149.—Spike-Organ of Flabellum.
ch.t., chitinous tubule.
Such, then, is the structure of this remarkable sense-organ of the flabellum, as far as I have been able to work it out with the materials at my disposal. It is evident that the flabellar organs, apart from the spike-organs, are of the same kind as those described by Patten on the mandibles and chelæ of Limulus, and therefore it is most probable that the nerve-terminals in the chitinous tubules, and the origin of the latter, are similar in the two sets of organs.
These organs, as Patten has described them, are situated in lines on the spines of the mandibles of the prosomatic locomotor appendages, and are grouped closely together to form a compact sense-organ on the surface of the inner mandible (Lankester's epicoxite) (i.m. in Fig. 155), so that a surface-view of the organ here gives the characteristic appearance of these poriferous sense-patches. Precisely similar organs are found on the chilaria, which are, in function at all events, simply isolated mandibles, to use Patten's terminology.
On the digging appendage (ectognath), as the comparison of Fig. 155, A and C, shows, the mandibular spines are almost non-existent, and the inner mandible or epicoxite is not present, so that the special sense-organ of this appendage is represented solely by the flabellum.
This sketch of the special sense-organs of Limulus shows that all the appendages of Limulus possess special sense-organs, with the exception of the operculum. All these sense-organs are formed on the same plan, in that they possess a fine chitinous tubule passing through the layers of chitin into the underlying hypodermal and nervous tissues, which terminates on the surface in a pore. The surface of the chitin where these pores are situated is perfectly smooth, although, in the case of the branchial sense-organs, the goblet-shaped masses of chitin, each of which contains a pore, are able to be pressed out beyond the level of the surface.
As to their functions, we unfortunately do not know much that is definite. Patten considers that he has evidence of a gustatory function in the case of the mandibular organs, and suggests also a temperature-sense in the case of some of these organs. The large organ of the flabellum and the branchial organs he has not taken into consideration. The situation of these organs puts the suggestion of any gustatory function, as far as they are concerned, out of the question; and I do not think it probable that such large specialized organs would exist only for the estimation of temperature, when one sees how, in the higher animals, the temperature-nerves and the nerves of common sensation are universally distributed over the body. As already stated, the structure of the branchial organs seems to me to point to organs for estimating varying pressures more than anything else, and I am strongly inclined to look upon the whole set of organs as the derivatives of the lateral sense-organs of annelids, such as are described by Eisig in the Capitellidæ. This is Patten's opinion with respect to the mandibular organs; and from what I have shown, these organs cannot be separated in type of structure from those of the flabellum and the branchial sense-organs.
In our search, then, for the origin of the vertebrate auditory organ in Limulus and its allies, we see so far the following indications:—
1. The auditory organ of the vertebrate is regarded as a special organ belonging to a segmentally arranged set of lateral sense-organs, whose original function was co-ordination and equilibration.
2. Such a set of segmentally arranged lateral sense-organs is found in annelids in connection with the dorsal cirri of the ventral parapodia.
3. If, as has been supposed, there is a genetic connection between (1) and (2) and if, as I suppose, the vertebrates did not arise from the annelids directly, but from a protostracan group, then it follows that the lateral sense-organs, one of which gave rise to the auditory organ, must have been situated on the protostracan appendages.
4. In Limulus, which is the sole surviving representative of the palæostracan group, such special sense-organs are found on both the prosomatic and mesosomatic appendages, and therefore may be expected to give a direct clue to the origin of the vertebrate auditory organ.
5. Both from its position, its size, and its specialization, the flabellum, i.e. an organ corresponding to the flabellum, must be looked upon as more likely to give a direct clue to the origin of the auditory organ than the sense-organs of the branchial appendages, or the so-called gustatory organs of the mandibles.
The Auditory Organs of Arachnids and Insects.
The difficulty of the investigating these organs consists in the fact that so little is known about them in those Arthropoda which live in the water; the only instance of any organ apparently of the nature of an auditory organ, is the pair of so-called auditory sacs at the base of the antennæ in various decapods. We are in a slightly better position when we turn to the land-living arthropods; here the presence of stridulating organs in so many instances carries with it the necessity of an organ for appreciating sound. It has now been shown that such stridulating organs are not confined to the Insecta, but are present also in the scorpion group, and I myself have added to their number by the discovery of a distinct stridulating apparatus in various members of the Phrynidæ. We may then take it for granted that arachnids as well as insects hear. Where is the auditory organ?
Many observers believe that certain surface-organs found universally among the spiders, to which Gaubert has given the name of lyriform organs, are auditory in function. His investigations show that they are universally present on the limbs and pro-meso-sternite of all spiders; that they are present singly, not in groups, on the limbs of Thelyphonus, and that a group of them exists on the second segment of each limb in the members of the Phrynus tribe. In the latter case this organ is the most elaborate of all described by him.
It is especially noticeable that they do not exist in Galeodes or in the scorpions, but in the former special sense-organs are found in the shape of the so-called 'racquet-organs,' on the basal segments of the most posterior pair of appendages, and also, according to Gaubert, on the extremity of the palps and the first pair of feet, while in the latter they occur in the shape of the pectens.
This observation of Gaubert suggests that the place of the lyriform organs in other arachnids is taken in Galeodes by the racquet-organs, and in the scorpions by the pectens. Bertkau, Schimkéwitsch, and Wagner, as quoted by Gaubert, all suggest that the lyriform organs of the arachnids belong to the same group of sense-organs as the porous chordotonal organs of the Insecta, sense-organs which have been found in every group of Insecta, and are generally regarded as auditory organs. Gaubert does not agree with this, and considers the lyriform organs to be concerned with the temperature-sense rather than with audition.
The chordotonal organs of insects have been specially studied by Graber. He divides them into two groups, the poriferous and the non-poriferous, the former being characterized by the presence of pores on the surface arranged in groups or lines. These poriferous chordotonal organs are remarkably constant in position, being found only at the base of the wings on the subcostal ridge, in marked contrast to the other group of chordotonal organs which are found chiefly on the appendages in various regions. The striking character of this fixity of position of these organs and the universality of their presence in the whole group, led Graber to the conclusion that in these poriferous chordotonal organs we are studying a form of auditory apparatus which characterized the ancestor of the insect-group. These organs are always well developed on the hind wings, and in the large group of Diptera the auditory apparatus has usurped the whole of the function of the wing; for the balancers or 'halteres,' as they are called, are the sole representatives of the hind wings, and they are usually considered to be of the nature of auditory organs. It is instructive to find that such an auditory organ serves not only for the purpose of audition, but also as an organ of equilibration; thus Lowne gives the evidence of various observers, and confirms it himself, that removal of the balancers destroys the power of orderly flight in the animal.
A striking peculiarity of these organs in the Insecta, as described by Graber, is the bulging of the porous canal near its termination (Fig. 150, C). This bulging is filled with a homogeneous, highly refractive material, from which, according to Lowne, a chordotonal thread passes, to be connected with a ganglion-cell and nerve. This sphere of refractive material he calls the 'capitellum' of the chordotonal thread. The presence of this material produces in a surface view an appearance as of a halo around the terminal plaque with its central pore; Graber has attempted to represent this by the white area round the central area (in Fig. 150, B). A very similar appearance is presented by the surface view of the flabellum in those parts where the tube runs straight to the surface, so that the refractive material which fills the oval bulging shines through the overlying chitin and appears to surround the terminal plaque with a translucent halo.
Such a peculiarity must have a very definite meaning, and suggests that the canals in the flabellum of Limulus and in the hind wings of insects belong to the same class of organ, the chitinous tubule with its nerve-terminal in the former corresponding to the chordotonal thread in the latter. One wonders whether this sphere of refractive material or 'capitellum' (to use Lowne's phraseology) is so universally present in order to act as a damper upon the vibrations of the chordotonal thread in the one case and of the chitinous tubule in the other, just as the membrana tectoria and the otoliths act in the case of the vertebrate ear.
Patten says that the only organs which seem to him to be comparable with the gustatory porous organs of Limulus are the sense-organs in the extremities of the palps and of the first pair of legs of Galeodes, as described by Gaubert. I imagine that he was thinking only of arachnids, for the comparison of his drawings with those of Graber show what a strong family resemblance exists between the poriferous sense-organs of Limulus and those of the insects. On the course of the terminal nerve-fibres, between the nerve-cell and their entrance into the porous chitinous canal, Graber describes the existence of rods or scolophores. On the course of the terminal fibres in the Limulus organ, between the nerve-cells and their entrance into the porous chitinous canal, Patten describes a spindle-shaped swelling, containing a number of rod-like thickenings among the fibrils in the spindle, which present an appearance reminiscent of the rods described by Graber.
It appears as though a type of sense-organ, characterized by the presence of pores on the surface and a fine chitinous canal which opens at these pores, was largely distributed among the Arthropoda. According to Graber, this kind of organ represents a primitive type of sense-organ, which was probably concerned with audition and equilibration, and he expresses surprise that similar organs have not been discovered among the Crustacea. It is, therefore, a matter of great interest to find that so ancient a type of animal as Limulus, closely allied to the primitive crustacean stock, does possess poriferous sense-organs upon its appendages which are directly comparable with these poriferous chordotonal organs of the Insecta.
The Pectens of Scorpions.
Among special sense-organs such as those with which I am now dealing, the pectens of scorpions and the 'racquet-organs' of Galeodes must, in all probability, be classed. I have given my reasons for this conclusion in my former paper.[1] At present such reasons are based entirely upon the structure of the organs; experimental evidence as to their function is entirely wanting. With respect to the pectens of the scorpion (Fig. 151), it has been suggested that they are of the nature of copulatory organs, a suggestion which may be dismissed without hesitation, for they are not constructed after the fashion of claspers, but are simply elaborate sense-organs, and, as such, are found equally in male or female. The only observer who has hitherto specially studied the structure of the sense-organs in the pecten is, as far as I know, Gaubert, and he describes their structure together with that of the sense-organs of the racquets of Galeodes, in connection with the lyriform organs of arachnids, as though he recognized a family resemblance between the three sets of organs.
Fig. 151.—Under Surface of Scorpion (Androctonus).
The pecten of the scorpions is an elaborate sense-organ, or rather group of sense-organs, the special organ being developed on each tooth of the comb; its surface, which is frequently flattened, being directed backwards and inwards, when the axis of the pecten is horizontal at right angles to the length of the body. The surface view of this part of the tooth resembles that of the branchial organs or of the flabellum in Limulus, in that it is thickly covered with circular patches, in the centre of which an ill-defined appearance as of a fine pore is seen. In Fig. 152, B, I give a sketch of the surface view of a part of the organ.
Transverse sections of a tooth of the comb of Scorpio Europæus present the appearance given in Fig. 152, A, and show that each of these circular patches is the surface-view of a goblet-shaped chitinous organ, Fig. 152, C, from the centre of which a short, somewhat cylindrical chitinous spike projects. Within this spike, and running through the goblet into the subjacent tissue, is a fine tubule. The series of goblets gives rise to the appearance of the circular plaques on the surface-view, while the spike with its tubule is the cause of the ill-defined appearance of the central pore, just as the terminal pore is much less conspicuous on surface-view in the spike-organs of the flabellum than in the purely poriferous organs, no part of which projects beyond the level of the chitinous surface.
Fig. 152.—A, Section through Tooth of Pecten of Scorpion; B, Surface View of Sense-Organs; C, Goblet of Sense-Organ more highly magnified.
bl. and n., region of blood-spaces and nerves; gl., ganglion-cell layer; ch., modified chitinous layer; s.o., sense-organ.
The fine tubule is soon lost in the thickened but soft modification of the chitinous layer (ch.) which is characteristic of the sense-organ; at all events, I have not succeeded in tracing it through this layer with any more success than in the corresponding case of the tubules belonging to the smaller goblets of the branchial sense-organ of Limulus already described.
At the base of the modified chitinous layer a series of cells is seen, many, if not all, of which belong to the chitinogenous layer. Next to these is the marked layer of ganglion-cells (gl.), similar to those seen in the flabellum of Limulus. The rest of the space in the section of the tooth is filled up with nerves (n.) and blood-spaces (bl.) just as in the section, Fig. 146, of the flabellum of Limulus.
Gaubert does not appear to have seen the goblets at all clearly; he describes them simply as conical eminences, and states that they "recouvrent un pore analogue a celui des poils mais plus petit; il est rempli par le protoplasma de la couche hypodermique." From the ganglion, according to him, nervous prolongations pass, which traverse the chitinogenous layer and terminate at the base of the conical eminences. Each of these prolongations "présente sur son trajet, mais un peu plus près du ganglion que de sa terminaison périphérique, une cellule nerveuse fusiforme (g.) offrant, comme celles du ganglion, un gros noyau." He illustrates his description with the following, Fig. 153, taken from his paper.
Fig. 153 (from Gaubert).—Section of a Tooth of Pecten of Scorpion.
n., nerve; gl., ganglion.
I have not been able to obtain any evidence of a fusiform nerve-cell on the course of the terminal nerve-fibres as depicted by him; fusiform cells there are in plenty, as depicted in my drawing, but none with a large nucleus resembling those of the main ganglion. In no case, either in the flabellum or in the branchial organs of Limulus, or in the pecten-organs, have I ever seen a ganglion-cell within the chitin-layer; all the nuclei seen there resemble those of the cells of the hypodermis or else the elongated nuclei characteristic of the presence of nerve-fibres. Gaubert's drawing is a striking one, and I have looked through my specimens to see whether there was anything similar, but have hitherto failed to obtain any definite evidence of anything of the kind.
I feel, myself, that an exhaustive examination of the structure and function of the pecten of scorpions ought to be undertaken. At present I can only draw the attention of my readers to the similarity of the arrangement of parts, and of the nature of the end-organs, in the sense-organs of the flabellum of Limulus and of the pecten of the scorpion. In both cases the special nerve-fibres terminate in a massive ganglion, situated just below the chitinogenous layer. In both cases the terminal fibres from these ganglion-cells pass through the modified chitinous layer to supply end-organs of a striking character; and although the end-organ of the pecten of the scorpion does not closely resemble the majority of the end-organs of the flabellum, yet it does resemble, on the one hand, the isolated poriferous spikes found on the flabellum (Fig. 149) and, on the other, the poriferous goblets found on the sense-patches of the branchial appendages of Limulus (Fig. 144, A), so that a combination of these two end-organs would give an appearance very closely resembling that of the pecten of the scorpion.
Finally, the special so-called 'racquet-organs' of Galeodes, which are found on the most basal segments of the last pair of prosomatic appendages, ought also to be considered here. Gaubert has described their structure, and shown how the nerve-trunk in the handle of the racquet splits up into a great number of separate bundles, which spread out fan-shaped to the free edge of the racquet; each of these separate bundles supplies a special sense-organ, which terminates as a conical eminence on the floor of a deep groove, running round the whole free edge of the racquet. This groove is almost converted into a canal, owing to the projection of its two sides. Gaubert imagines that the sense-organs are pushed forward out of the groove to the exterior by the turgescence of the whole organ; each of the nerve-fibres forming a bundle is, according to Gaubert, connected with a nerve-cell before it reaches its termination.
This sketch of the special sense-organs on the appendages of Limulus, of the scorpions, of Galeodes, and other arachnids, and their comparison with the porous chordotonal organs of insects, affords reason for the belief that we are dealing here with a common group of organs, which, although their nature is not definitely known, have largely been accredited with the functions of equilibration and audition, a group of organs among which the origin of the auditory organ of vertebrates must be sought for, upon any theory of the origin of vertebrates from arthropods.
Whenever in any animal these organs are concentrated together to form a special organ, it is invariably found that the nerve going to this organ is very large, out of all proportion to the size of the organ, and also that the nerve possesses, close to its termination in the organ, large masses of nerve-cells. Thus, although the whole hind wing in the blow-fly has been reduced to the insignificant balancers or 'halteres,' yet, as Lowne states, the nerves to them are the largest in the body.
The pectinal nerve in the scorpion is remarkable for its size, and so, also, is the nerve to the flabellum in Limulus, while the large size of the auditory nerve in the vertebrate, in distinction to the size of the auditory apparatus, has always aroused the attention of anatomists.
Throughout this book my attention has been especially directed to both Limulus and the scorpion group in endeavouring to picture to myself the ancestor of the earliest vertebrates, because the Eurypteridæ possessed such marked scorpion-like characteristics; so that in considering the origin of a special sense-organ, such as the vertebrate auditory organ near the junction of the prosoma and mesosoma, it seems to me that the presence of such marked special sense-organs as the flabellum on the one hand and the pecten on the other, must both be taken into account, even although the former is an adjunct to a prosomatic appendage, while the latter represents, according to present ideas, the whole of a mesosomatic appendage.
From the point of view that the VIIIth nerve represents a segment immediately posterior to that of the VIIth, it is evident that an organ in the situation of the pecten, immediately posterior to the operculum, i.e. according to my view, posterior to the segment originally represented by the VIIth nerve, is more correctly situated than an organ like the flabellum, which belongs to a segment anterior to the operculum.
On the other hand, from the point of view of the relationship between the scorpions and the king-crabs, it is a possibly debatable question whether the pecten really belongs to a segment posterior to the operculum. The position of any nerve in a series depends upon its position of origin in the central nervous system, rather than upon the position of its peripheral organ. Now, Patten gives two figures of the brain of the scorpion built up from serial sections. In both he shows that the main portion of the pectinal nerve arises from a swelling, to which he gives the name ganglion nodosum. This swelling arises on each side in close connection with the origin of the most posterior prosomatic appendage-nerve, according to his drawings, and posteriorly to such origin he figures a small nerve which he says supplies the distal parts of the sexual organs. This nerve is the only nerve which can be called the opercular nerve, and apparently arises posteriorly to the main part of the pectinal nerve. If this is so, it would indicate that the pectens arose from sense-organs which were originally, like the flabella, pre-opercular in position, but have shifted to a post-opercular position.
The Origin of the Parachordals and Auditory Cartilaginous Capsule.
In addition to what I have already said, there is another reason why a special sense-organ such as the pecten is suggestive of the origin of the vertebrate auditory organ, in that such a suggestion gives a clue to the possible origin of the parachordals and auditory cartilaginous capsules.
In the lower vertebrates the auditory organ is characterized by being surrounded with a cartilaginous capsule which springs from a special part of the axial cartilaginous skeleton on each side, known as the pair of parachordals. The latter, in Ammocœtes, form a pair of cartilaginous bars, which unite the trabecular bars with the branchial cartilaginous basket-work. They are recognized throughout the Vertebrata as distinct from the trabecular bars, thus forming a separate paired cartilaginous element between the trabeculæ and the branchial cartilaginous system, which of itself indicates a position for the auditory capsule between the prosomatic trabeculæ and the mesosomatic branchial cartilaginous system.
The auditory capsule and parachordals when formed are made of the same kind of cartilage as the trabeculæ, i.e. of hard cartilage, and are therefore formed from a gelatin-containing tissue, and not from muco-cartilage. Judging from the origin already ascribed to the trabeculæ, viz. their formation from the great prosomatic entochondrite or plastron, this would indicate that a second entochondrite existed in the ancestor of the vertebrate in the region of the junction of the prosoma and mesosoma, which was especially connected with the sense-organ to which the auditory organ owes its origin. This pair of entochondrites becoming cartilaginous would give origin to the parachordals, and subsequently to the auditory capsules, their position being such that the nerve to the operculum would be surrounded at its origin by the growth of cartilage.
On this line of argument it is very significant to find that the scorpions do possess a second pair of entochondrites, viz. the supra-pectinal entochondrites, situated between the nerve-cord and the pectens, so that if the ancestor of the Cephalaspid was sufficiently scorpion-like to have possessed a second pair of entochondrites and at the same time a pair of special sense-organs of the nature either of the pectens or flabella, then the origin of the auditory apparatus would present no difficulty.
It is also easy to see that the formation of the parachordals from entochondrites homologous with the supra-pectinal entochondrites, would give a reason why the VIIth or opercular nerve is involved with the VIIIth in the formation of the auditory capsule, especially if the special sense-organ which gave origin to the auditory organ was originally a pre-opercular sense-organ such as the flabellum, which subsequently took up a post-opercular position like that of the pecten.
The Evidence of Ammocœtes.
As to the auditory apparatus itself, we see that the elaborate organ for hearing—the cochlea—has been evolved in the vertebrate phylum itself. In the lowest vertebrates the auditory apparatus tends more and more to resolve itself into a simple epithelial sac, the walls of which in places bear auditory hairs projecting into the sac, and in part form otoliths. Such a simple sac forms the early stage of the auditory vesicle in Ammocœtes, according to Shipley; subsequently, by a series of foldings and growings together, the chambers of the ear of the adult Petromyzon, as figured and described by Retzius, are formed. Further, we see that throughout the Vertebrata this sac was originally open to the exterior, the auditory vesicle being first an open pit, which forms a vesicle by the approximating of its sides, the last part to close being known as the recessus labyrinthicus; in many cases, as in elasmobranchs, this part remains open, or communicates with the exterior by means of the ductus endolymphaticus.
Judging, therefore, from the embryological evidence, it would appear that the auditory organ originated as a special sense-organ, formed by modified epithelial cells of the surface, which epithelial surface becoming invaginated, came to line a closed auditory vesicle under the surface. This special sense-organ was innervated from a large ganglionic mass of nerve-cells, situated close against the peripheral sense-cells, the axis-cylinder processes of which formed the sensory roots of the nerve.
Yet another peculiarity of striking significance is seen in connection with the auditory organ of Ammocœtes. The opening of the cartilaginous capsule towards the brain is a large one (Fig. 154), and admits the passage not only of the auditory and facial nerves, but also of a portion of the peculiar tissue which surrounds the brain. The large cells of this tissue, with their feebly staining nuclei and the pigment between them, make them quite unmistakable; and, as I have already stated, nowhere else in the whole of Ammocœtes is such a tissue found. When I first noticed these cells within the auditory capsule, it seemed to me almost impossible that my interpretation of them as the remnant of the generative and hepatic tissue which surrounds the brain of animals such as Limulus could be true, for it seemed too unlikely that a part of the generative system could ever have become included in the auditory capsule. Still, they are undoubtedly there; and, as already argued with respect to the substance round the brain, they must represent some pre-existing tissue which was functional in the ancestor of Ammocœtes. If my interpretation is right, this tissue must be generative and hepatic tissue, and its presence in the auditory capsule immediately becomes a most important piece of evidence, for it proves that the auditory organ must have been originally so situated that a portion of the generative and hepatic mass surrounding the cephalic region of the nervous system followed the auditory nerve to the peripheral sense-organ.
Fig. 154.—Transverse Section through Auditory Capsules and Brain of Ammocœtes.
Here there was a test of the truth of my theory ranking second only to the test of the median eyes; the strongest possible evidence of the truth of any theory is given when by its aid new and unexpected facts are brought to light. The theory said that in the group of animals from which the vertebrates arose, a special sense-organ of the nature of an auditory organ must have existed on the base of one of the appendages situated at the junction of the prosoma and mesosoma, and that into this basal part of the appendage a portion of the cephalic mass of generative and hepatic material must have made its way in close contiguity to the nerve of the special organ.
The only living example which nearly approaches the ancient extinct forms from which, according to the theory, the vertebrates arose, is Limulus, and, as has already been shown, in this animal, in the very position postulated by the theory, a large special sense-organ—the flabellum—exists, which, as already stated, may well have given rise to a sense-organ concerned with equilibration and audition. If, further, it be found that a diverticulum of the generative and hepatic material does accompany the nerve of the flabellum in the basal part of the appendage, then the evidence becomes very strong that the auditory organ of Ammocœtes, i.e. of the ancient Cephalaspids, was derived from an organ homologous with the flabellum; that, therefore, the material round the brain of Ammocœtes was originally generative and hepatic material; that, in fact, the whole theory is true, for all the parts of it hang together so closely that, if one portion is accepted, all the rest must follow. As pointed out in my address at Liverpool, and at the meeting of the Philosophical Society at Cambridge, it is a most striking fact that a mass of the generative and hepatic tissue does accompany the flabellar nerve into the basal part of this appendage. Into no other appendage of Limulus is there the slightest sign of any intrusion of the generative and hepatic masses; nowhere, except in the auditory capsule, is there any sign of the peculiar large-celled tissue which surrounds the brain and upper part of the spinal cord of Ammocœtes. The actual position of the flabellum on the basal part of the ectognath is shown in Fig. 155, A, and in Fig. 155, B, I have removed the chitin, to show the generative and hepatic tissue (gen.) lying beneath.
The reason why, to all appearance, the generative and hepatic mass penetrates into the basal part of this appendage only is apparent when we see (as Patten and Redenbaugh have pointed out) to what part of the appendage the flabellum in reality belongs.
fl., flabellum; cox., coxopodite; ent., entocoxite; m., mandible; i.m., inner mandible or epicoxite.
Patten and Redenbaugh, in their description of the prosomatic appendages of Limulus, describe the segments of the limbs as (1) the dactylopodite, (2) the propodite, (3) the mero- and carpo-podites, (4) the ischiopodite, (5) the basipodite, and (6) the coxopodite (cox. in Fig. 155). Still more basal than the coxopodite is situated the entocoxite (ent. in Fig. 155), which is composed of three sclerites or sensory knobs, to use Patten's description. The middle one of these three sclerites enlarges greatly in the digging appendage, and grows over the coxopodite to form the base from which the flabellum springs. Thus, as they have pointed out, the flabellum does not belong to the coxopodite of the appendage, but to the middle sensory knob of the entocoxite. Upon opening the prosomatic carapace, it is seen that the cephalic generative and hepatic masses press closely against the internal surface of the prosomatic carapace and also of the entocoxite, so that any enlargement of one of the sensory knobs of the entocoxite would necessarily be filled with a protrusion of the generative and hepatic masses. This is the reason why the generative and hepatic material apparently passes into the basal segment of the ectognath, and not into that of the endognaths; it does not really pass into the coxopodite of the appendage, but into an enlarged portion of the entocoxite, which can hardly be considered as truly belonging to the appendage. Kishinouye has stated that a knob arises in the embryo at the base of each of the prosomatic locomotor appendages, but that this knob develops only in the last or digging appendage (ectognath) forming the flabellum. Doubtless the median sclerites of the entocoxites of the endognaths represent Kishinouye's undeveloped knobs.
I conclude, therefore, that the flabellum, together with its basal part, is an adjunct to the appendage rather than a part of it, and might, therefore, easily remain as a separate and well-developed entity, even although the appendage itself dwindled down to a mere tentacle.
The evidence appears to me very strong that the flabellum of Limulus and the pecten of scorpions are the most likely organs to give a clue to the origin of the auditory apparatus of vertebrates. At present both the Eurypterids and Cephalaspids have left us in the lurch; in the former there is no sign of either flabellum or pecten; in the latter, no sign of any auditory capsule beyond Rohon's discovery of two small apertures situated dorsally on each side of the middle line in Tremataspis, which he considers to be the termination of the ductus endolymphaticus on each side. In both cases it is probable, one might almost say certain, that any such special sense-organ, if present, was not situated externally, but was sunk below the surface as in Ammocœtes.
The method by which such a sense-organ, situated externally on the surface of the animal, comes phylogenetically to form the lining wall of an internally situated membranous capsule is given by the ontogeny of this capsule, which shows step by step how the sense-organ sinks in and forms a capsule, and finally is entirely removed from the surface except as regards the ductus endolymphaticus.
Summary.
The special apparatus for hearing is of a very different character from that for vision or for smell, for its nerve belongs to the infra-infundibular group of nerves, and not to the supra-infundibular, as do those of the other two special senses. Of the five special senses the nerves for touch, taste, and hearing, all belong to the infra-infundibular segmental nerve-groups. The invertebrate origin, then, of the vertebrate auditory nerve must be sought for in the infra-œsophageal segmental group of nerves, and not in the supra-œsophageal.
The organs supplied by the auditory nerve are only partly for the purpose of hearing; there is always present also an apparatus—the semicircular canals—concerned with equilibration and co-ordination of movements. Such equilibration organs are not confined to the auditory nerve, but in the water-living vertebrates are arranged segmentally along the body, forming the organs of the lateral line in fishes; the auditory organ is but one of these lateral line organs, which has been specially developed.
These lateral line organs have been compared to similar segmental organs found in connection with the appendages in worms, especially the respiratory appendages. In accordance with this suggestion we see that they are all innervated from the region of the respiratory nerves—the vagus, glosso-pharyngeal, and facial—nerves which originally supplied the respiratory appendages of the palæostracan ancestor.
The logical conclusion is that the appendages of the Palæostraca possessed special sense-organs concerned with the perception of special vibrations, especially in the mesosomatic or respiratory region, and that somewhere at the junction of the prosoma and mesosoma, one of these sense-organs was specially developed to form the origin of the vertebrate auditory apparatus.
Impressed by this reasoning I made search for some specially striking sense-organ at the base of one of the appendages of Limulus, at the junction of the prosoma and mesosoma, and was immediately rewarded by the discovery of the extraordinary nature of the flabellum, which revealed itself as an elaborate sense-organ supplied with a nerve out of all proportion to its size. Up to this time no one had the slightest conception that this flabellum was a special sense-organ; the discovery of its nature was entirely due to the logical following out of the theory of the origin of vertebrates described in this book.
The structure of this large sense-organ is comparable with that of the sense-organs of the pectens of the scorpion, and of many other organs found on the appendages of various members of the scorpion group, of arachnids and other air-breathing arthropods. Many of these organs, such as the lyriform organs of arachnids, and the 'halteres' or balancers of the Diptera, are usually regarded as auditory and equilibration organs.
On all the mesosomatic appendages of Limulus very remarkable sense-organs are found, apparently for estimating pressures, which, when the appendages sank into the body to form with their basal parts the branchial diaphragms of Ammocœtes, could easily be conceived as remaining at the surface, and so giving rise to the lateral line organs.
Further confirmation of the view that an organ, such as the flabellum, must be looked upon as the originator of the vertebrate auditory organ, is afforded by the extraordinary coincidence that in Limulus a diverticulum of the generative and hepatic mass accompanies the flabellar nerve into the basal part of the digging appendage, while in Ammocœtes, accompanying the auditory nerve into the auditory capsule, there is seen a mass of cells belonging to that peculiar tissue which fills up the space between the brain and the cranial walls, and has already, on other grounds, been homologized with the generative and hepatic masses which fill up the encephalic region of Limulus.
For all these reasons special sense-organs, such as are found in the flabellum of Limulus and in the pectens of scorpions, may be looked upon as giving origin to the vertebrate auditory apparatus. In such case it is highly probable that the parachordals, with the auditory capsules attached, arose from a second entochondrite of the same nature as the plastron; a probability which is increased by the fact that the scorpion does possess a second entochondrite, which, owing to its special relations to the pecten, is known as the supra-pectinal entochondrite.
- ↑ "The Origin of Vertebrates, deduced from the Study of Ammocœtes." Part X., "The Origin of the Auditory Organ: the Meaning of the VIIIth Cranial Nerve." Journ. Anat. and Physiol., vol. 36, 1902.