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In the Dogfish (Scyliorhinus Canicula)

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In the Dogfish (Scyliorhinus Canicula) J. Exp. Biol. (1965), 43, 363-383 363 With 12 text-figures Printed in Great Britain THE MUSCULAR BASIS OF THE RESPIRATORY PUMPS IN THE DOGFISH (SCYLIORHINUS CANICULA) BY G. M. HUGHES* AND C. M. BALLINTIJNf Marine Biological Laboratory, Plymouth, and Department of Zoology, Cambridge {Received 17 March 1965) The mechanism of gill ventilation in the dogfish has been shown to be fundamentally the same as that found in teleost fishes (Hughes, 19606; Hughes & Shelton, 1962). Water enters the respiratory system through both the mouth and the spiracle during expansion of the oro-branchial cavity (Woskoboinikoff, 1932) and after passing across the gills it enters the parabranchial cavities before being ejected to the outside through the five pairs of gill slits. The flow across the gills is maintained partly as a result of the increased pressure in front of the gill resistances but also because of the suction pump action of the parabranchial cavities. The muscular activities producing the changes in volume of these two cavities and hence the required pressure gradient across the gills have not been established and descriptions of the relationships of muscles and skeleton are not always clear in detail. Woskoboinikoff (1932) and others were of the opinion that the coraco-mandibularis muscle was of importance during the phase of the cycle when the mouth opens and the oro-branchial cavity expands, but this was categorically denied by Balabai (1938) in a footnote to his paper. From observations on dogfish, anaesthetized so that they no longer pumped water across their gills, it was suggested (Hughes, 1960 a) that the main muscular action during the cycle was due to the constrictor muscles. These compress the branchial region and on their relaxation the elastic properties of the skeleton and ligaments are sufficient to account for expansion of the parabranchial cavities. A dogfish in this condition can be made to pump water through its respiratory system by compressing the branchial region by hand. It was also clear in Scyliorhinus that, as had also been observed by Satchell (1959) in Squalus, the respiratory cycle begins with a compression and is followed by relaxation and a relatively long respiratory pause. As with the study of all muscular activities it is extremely difficult to describe the function of a given system from the morphology alone and for respiration it has been shown both in mammals (Campbell, 1958) and fishes (Hughes, 1961; Hughes & Shelton, 1962) that electromyography is an ideal technique. This technique has recently been applied to teleost fishes in greater detail (Ballintijn & Hughes, 1965). The purpose of the present work therefore was to study the action of the main muscles of the head and branchial region of the dogfish, Scyliorhinus canicula, in order to establish the phase of the respiratory cycle at which they are active and to ascertain their role in the action of the oro-branchial pressure pump and parabranchial • Present address: Department of Zoology, University of Bristol. f On leave from the Zoological Laboratory of the University, Groningen, The N< therlands. Sup- ported by a grant of the Netherlands Organization for the Advancement of Pure Research (Z.W.O.)- 364 G. M. HUGHES AND C. M. BALLINTIJN suction pumps. The results have shown that most muscles are active during the com- pression phase of the respiratory cycle and that relatively few are active during the phase of expansion of either the oro-branchial or parabranchial cavities. It appears, therefore, that the hypobranchial musculature plays a relatively minor role in normal respiration although it is important during hyperventilation and at other times when the volume of the pharynx is increased as, for example, during feeding. MATERIAL AND METHODS The methods used in the present study were fundamentally the same as those described in Hughes (i960) and Ballintijn & Hughes (1965). The dogfish was anaesthe- tized in MS222 (Sandoz), initially at a concentration of 1 g. in 10,000 c.c, and after being fixed in the holder it was placed in a tank containing 25 1. of sea water and about 1 g. MS 222. Individual variations in susceptibility to the anaesthetic were often found. For this reason the exact concentration was varied either by diluting the bath containing the preparation or by pipetting small volumes of concentrated anaesthetic (1 g. in 250 c.c.) into the mouth. For the placement of the paired stainless steel elec- trodes it was necessary to make a small cut in the thick skin above the muscle to be investigated. Larger pins were used than in studies of the trout and it was also necessary to use thicker wire in the input leads to the amplifier. The animal was maintained in this condition with four pairs of electrodes in different muscles. In some cases the output of the preamplifiers was passed through an integrator circuit and gave a convenient record of the discharge pattern in a given muscle. Pressures in the oro-branchial and one of the parabranchial cavities were recorded using Hansen manometers (Hughes & Shelton, 1958). Movements of the lower jaw and branchial region just dorsal to a given slit were recorded using RCA 5734 mechano-transducer valves. All recordings were made while the fish breathed continuously and was under light anaesthesia. Each animal was used in two experiments, involving the study of muscles first on one side and later on the other side. For the latter it was found advantageous to keep the animal lighdy anaesthetized between experiments. Following the recording of electromyograms, pressures and movements, the positions of the electrode tips were determined by passing a small current through them and so depositing ferric ions. The fish was then killed and the electrode position visualized by immersing the head in a solution containing 4 % potassium ferrocyanide. Dissection revealed a spot of Prussian blue at the point from which the recordings had been made. RESULTS A. The skeletal and muscular systems (Fig. 1) The skeleton of the head and branchial region of the dogfish are so well known (see Daniel, 1934; Marinelli & Strenger, 1959) that a complete description here is not necessary; but certain important aspects of the morphology will be mentioned. The branchial arch skeleton is made up of a series of cartilages which are inclined forwards from the dorsal to the ventral elements. In transverse section the main curvature lies between the epi- and cerato-branchial cartilages and it is across this joint that the adductor branchialis muscle operates. From the lateral surfaces of the Respiratory muscles of the dogfish 365 hyoid and branchial arches there spread out a series of gill rays which support the septa separating the gill pouches from one another (Fig. 2). The gill rays attached to the hyoid arch are particularly long and bridge the wide space between the spiracle and the first gill slit. In addition to the gill rays each of the inter-branchial septa is supported by a large extra-branchial cartilage lying external to the gill rays. This cartilage is important in maintaining the shape of the parabranchial cavities. The pharyngo-branchials lie just beneath the vertebral column and are functionally anchored to it by means of a series of muscles (Fig. 1). The anterior muscle, the subspinalis, has its origin between the ventral part of the skull and the vertebral column and is inserted on the first pharyngo-branchial cartilage. The latter is con- nected by an interarcual muscle to the second pharyngo-branchial, which is similarly Interarcualis dors alls Lev. palatoquadrati Lev- hyomandibulae Subspinalis Arcuills Coraco-mandlbularls Coraco- Coraco-branchlales communls hyoldeus Fig. 1. Diagram of the skeleton and main muscles of the dogfish head seen from the left aide. The superficial constrictor sheets are not shown. The direction in which movement occurs when a given muscle contracts is shown by the arrow. Add. br., adductor branchialis; Add. md., adductor mandibulae; Pal.-pt. Qu., palato-pterygoid. connected to the third and so on. This system of dorsal interarcualis muscles appears to function by pulling forwards the whole of the dorsal part of the branchial arch skeletons. At the ventral ends of the branchial cartilages are inserted the coraco-branchial muscles. Contraction of these muscles would pull the ventral part of the skeleton downwards and backwards and so expand the oro-branchial and parabranchial cavities. These hypo-branchial muscles are some of the few clearly denned muscles of the head region, which is covered by a whole sheet of superficial constrictor muscles. Parts of the latter become concentrated to form more specific muscles as, for example, the levator hyomandibulae. The constrictor sheet is formed of several overlapping sheets, each associated with a given arch. Posteriorly the superficial constrictor of the hyoid segment extends to form the valve of the first slit. The superficial constrictor of the first branchial segment is overlain slightly by this and in its turn covers the second branchial constrictor and so on (Lighttoller, 1939). Most of the fibres in these sheets run in a dorso-ventral direction around the branchial region. In this work we have made an artificial distinction between dorsal, lateral and ventral regions. The former 366 G. M. HUGHES AND C. M. BALLINTIJN lies above the upper end of the gill slit and the ventral constrictors begin at the ventral end of the gill slits, while the lateral portions are in the region over which the slit extends on the side of the body. Another and most important part of each con- strictor sheet, however, is not external but lies within the gill septum. In these septal constrictors the fibres run dorso-ventrally (Fig. 2) and in the same plane as the gill rays across which the fibres can be seen to pass, although in other elasmobranchs it is reported that they insert on individual rays.
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