Studies in the Localisation of Respiratory Exchange in Invertebrates

The physiological function of the book lungs of Arachnids has not received a great deal of attention. No attempt has been made to investigate their respiratory function, and what references exist deal with the question of respiratory movements. Treviranus (1814) stated that there are no respiratory movements in scorpions. Muller (1828) described an extension of the lung membrane over the stigma, forming a valve-like structure, but he recorded no respiratory movements. Blanchard (1851) observed rhythmical movements of the dorsal wall of the lung sacs, causing the opening and shutting of the stigmata. Plateau (1887), on the other hand, using methods of graphical recording, failed to discover any movement of the respiratory apparatus. The respiratory movement of the abdominal plates bearing the book gills in Limulus polyphemus are unquestionable, and was shown by Hyde (1894) to be under nervous control.The structures described in text-books as the respiratory organs of scorpions appear externally as paired slit-like openings situated on the ventral surface of the ninth, tenth, eleventh and twelfth segments. Each of the eight stigmata communicates with a chamber, the pulmonary sac, containing 130 to 150 lamellae. The whole organ is called a book lung. The lamellae are attached at their base and along part of their edge to the walls of the chamber. Each lamella is a compressed sac with thin membranous walls, and is filled with blood which is supplied from the ventral venous sinus. From the gills the blood is returned through paired veins to the dorsal venous sinus, which is the space of the pericardium, and from which the heart fills itself. Paired veno-pericardiac muscles connect the roof of the ventral sinus with the ventral wall of the pericardium, and their rhythmic contraction is said to enlarge the cavities of the sinuses, and facilitate the circulation of blood through the gill lamellae. The whole structure is obviously one which would predispose one to the view that it is an organ of respiratory exchange. This view is confirmed by the following experiments. The animals employed belonged to the species Opisthophthalmus capensis, commonly found on the slopes of Table Mountain and Signal Hill.The scorpions were kept in the laboratory in large petri. dishes containing sand about an inch in depth. They were fed once a week with small scraps of raw meat. In this manner they survive satisfactorily for 2 months and longer. Oxygen consumption was measured by means of the Barcroft micro-respiration apparatus.In order to determine the functional rôle of the book lungs it was desired to occlude the stigmata. For this purpose vaseline was at first employed, but the results obtained were inconsistent, and the use of vaseline was finally abandoned in favour of Dunlop’s rubber solution, which proved highly satisfactory. The solution was applied to the stigmata in a thin layer, which rapidly dried and left a film of rubber firmly adhering to the stigmata. Animals with all the lungs occluded in this way became sluggish and comatose in 15 to 30 minutes and died after about 2 hours. If, however, the rubber films were peeled off while the animal still showed signs of life, complete recovery followed.Determinations of oxygen consumption were carried out with twenty untreated animals, twenty animals with all the book lungs occluded, and thirteen with four occluded and four left open in different combinations. The summarised results are given in Table I.In every case the animals with all the book lungs occluded showed no consumption of oxygen whatever. The half occluded animals all consumed oxygen, but the average value for this group is significantly lower than that for the untreated group, being approximately 70 per cent, of the normal respiration. Since this group comprises animals in which the two posterior pairs, the two anterior pairs, four on one side, and two anterior on the right with two posterior on the left, stigmata were occluded, it would seem that all the book lungs are in a general way functionally equivalent, and that normal respiration cannot be maintained by only four of the eight organs.A small number of determinations of carbon dioxide output by the Pettenkofer method were in complete agreement with the oxygen determinations. Blank determinations with no animal in the apparatus showed that a small quantity of carbon dioxide, varying between one- and two-tenths of a cubic centimetre per hour, was taken up by the baryta solution. This was due either to incomplete absorption in the caustic potash solution, or to a very slight leak in the chain. It was not found possible to eliminate this error, which in any case was hardly significant, and the summarised results given in Table II are corrected for this quantity. It is seen that when the book lungs were occluded with rubber solution the output of carbon dioxide was in each case reduced to zero.Additional confirmation of the view that the book lungs in the scorpion are the only region of gaseous exchange in that animal is furnished by the data presented in Table III. In this experiment the narcotising effect of an atmosphere of pure carbon dioxide on untreated animals and on animals with occluded book lungs was determined. A normal scorpion, when picked up with forceps and placed upon the bench, will immediately proceed to run for shelter at a rapid rate, travelling more or less in a straight line. The same response is exhibited by animals with occluded book lungs, though more sluggishly, for the first half hour or so after the application of the rubber solution. After that they become too comatose to move to any extent. This “escape response” was employed as an index of the degree of narcotisation after immersion in carbon dioxide. The animals were placed in a bottle through which carbon dioxide was blown from a cylinder of compressed gas for the specified period of time. They were then taken out and placed in the centre of a sheet of paper on which concentric circles of radius 3, 6, 9, and 12 inches were drawn. The distance travelled by the animal in 30, 60, 90, and 120 seconds after removal from the CO2 bottle was recorded. Untreated animals when removed from the carbon dioxide were all quite paralysed. After several minutes, violent and characteristic twitching of the legs and pedipalps occurred, followed a minute or two later by the recovery of the power of locomotion.Table III shows that five scorpions with all book lungs occluded were not in any way affected by the carbon dioxide treatment, four of them walked rapidly to the circumference of the outer circle, that is to say in considerably less than 30 seconds, and one reached the circumference in 90 seconds. Their behaviour was not distinguishable from that of animals that had not been subjected to the carbon dioxide treatment. The figures for the untreated animals all show that they remained paralysed for from 4 to 8 minutes. Those animals in which the two posterior pairs of book lungs were occluded showed only a slight narcosis after immersion for 5 or 6 minutes. They began to move usually during the first minute and then crawled slowly to the outer circumference. The experiment affords very definite confirmation of the complete localisation of gaseous exchange in the book lungs of the scorpion.In the scorpion the respiratory exchange is found to be entirely localised in the book lungs. This result was unexpected in view of the claim of Buddenbrock and Rohr (1922) that in Dixipus 25 percent, of the respiration is cutaneous. One is inclined to question this conclusion. Certainly in an animal with so thick an integument as the scorpion a very insignificant cutaneous respiration is to be expected. The scorpion, moreover, inhabits arid and semi-arid regions, so that evaporation must be effectively prevented in this animal. It does not seem probable that an integument which does not permit of the diffusion of moisture should be permeable to oxygen. It was shown in the introductory section that the majority of authors who have considered the question are agreed that respiratory movements are absent in the scorpion. My own observations confirm this conclusion as regards any externally perceptible movement. But the possibility still remains that there may be some slight but nevertheless significant ventilating movement within the lung chambers. The circulation of the blood in the respiratory lamellae may serve in some measure to stir the air in the chamber. But theoretical considerations do not demand the existence of a ventilating mechanism. As in the scaphognathectomised crab, simple diffusion should suffice to renew the oxygen at the respiratory surface. How the exsiccation of the book lungs is avoided is a problem that demands investigation. In the scorpion the habit of living in dry situations is correlated with an integument impervious alike to moisture and to the respiratory gases, and with enclosed organs of strictly localised respiratory exchange, which, apparently, can function successfully without the aid of any ventilating movements. In the aquatic Arachnid Limulus the function of the very similar structures, the book gills, depends upon a highly developed mechanism of ventilation.