DEPENDENCE OF SPERM MOTILITY AND RESPIRATION ON OXYGEN CONCENTRATION

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1 DEPENDENCE OF SPERM MOTILITY AND RESPIRATION ON OXYGEN CONCENTRATION ABRAHAM C. NEVO A.R.C. Unit of Reproductive Physiology and Biochemistry, Cambridge, England {Received 22nd June 1964) Summary. Motility and respiratory rate of bull, ram and cock spermatozoa as a function of oxygen concentration were correlated by simultaneous determinations on the same suspensions. Motility changes were found to parallel exactly those of respiratory rate. Motility and respiratory rate were both constant in the range of oxygen concentrations from that in air down to a critical oxygen concentration of 0\m=.\6\m=+-\0\m=.\06% (corresponding to an O2 partial pressure of 4 to 5 mm Hg). At this point there was a sharp reduction in respiratory rate and a rapid inactivation of the bulk of the spermatozoa. Oxygen consumption and motility ceased entirely below 1 mm Hg O2 partial pressure (0\m=.\13%O2). No appreciable differences in the critical O2 values were found between the three species. The respiratory rate and the critical O2 concentrations were not altered appreciably by the presence of glucose or fructose. INTRODUCTION As is well known, spermatozoa exhibit in the presence of oxygen a considerable respiratory activity, which is usually correlated with their motility. Sperm atozoa, of all species so far investigated, are able to support motility by endogen ous respiration and are unable to do so under anaerobic conditions, in the absence of extracellular substrates. It is also known that, in some species at any rate, the spermatozoa are capable of maintaining a high rate of oxygen uptake even when the oxygen concentration is much lower than in air (Mann, 1964, p. 293; Humphrey & Mann, 1949). There has been, however, little informa tion until now about the quantitative aspects of the mutual inter-relationship between levels of oxygen concentration on the one hand, and the rate of respiration and degree of sperm motility on the other. The present investigation aimed at providing some information with respect to that inter-relationship. Answers were sought in particular to the following questions : ( 1 ) What is the oxygen concentration above which there is no further increase in sperm motility and respiratory rate? (2) What is the concentration of oxygen below * Present address: The Weizmann Institute of Science, Rehovoth, Israel. 103

2 104 A. C. Nevo which motility and respiration cease? (3) Do changes in motility parallel in a quantitative manner those in the rate of sperm respiration? Cock, ram and bull spermatozoa were investigated. MATERIALS AND METHODS COLLECTION OF SEMEN AND PREPARATION OF SPERM SUSPENSIONS Cock semen was collected by the abdominal massage technique, and bull and ram semen with the aid of an artificial vagina. As the spermatozoa of all three species are able to maintain motility anaerobically by utilization of extra-cellular substrates (chiefly glucose or fructose) present in their seminal plasma, it is essential to remove these substrates for the correlation of motility with respiratory rate at low oxygen concentrations. Stock suspensions of washed spermatozoa were prepared by one or two dilu tions and centrifugations. Excessive dilutions and centrifugations were avoided, as they damaged the cells; they were also unnecessary in this in stance, as keeping the washed sperm suspensions for a few minutes at tem peratures above 30 C removed any slight excess of sugar left over. In order to be certain that sufficient time is allowed for the traces ofsugar to be used up, a small sample from the suspension may be incubated simultaneously in an observation chamber and the time until inactivation noted (Schindler & Nevo, 1962). The diluent was a phosphate-buffered Ringer's solution of the following composition: 0-9 % NaCl (0-153 m), 90 ml; m KC1, 5 ml; m MgS04, 1 ml; m/15 phosphate buffer, ph 7-0, 4 ml. APPARATUS FOR SIMULTANEOUS RECORDING OF AND SPERM MOTILITY OXYGEN CONCENTRATION The apparatus is shown diagrammatically in Text-fig. 1. It consists of: 'a', a thin, flat Observation chamber' of rectangular cross section, with a depth of 0-5 mm, through which the spermatozoa can be observed under a microscope; the observation chamber has two side-arms, into one of which an oxygen electrode assembly, 'b', is inserted through a ground-glass joint. The observa tion chamber is connected through one side-arm to a pear-shaped vessel, V, by way of a three-way stopcock, through which the sperm sample is introduced ; the other side-arm is connected, by way of another three-way stopcock, to pipetting a arrangement, by the aid of which the contents may be drawn into the chamber and manipulated in such a way as to remove any air bubbles. The observation chamber is immersed in the central well of a small constant tempera ture bath, 'd', which rests on the microscope stage; there is a glass window in the bottom of the central well for the light beam to pass through and a jacket through which water is circulated from a thermostatically controlled water-bath. The oxygen electrode assembly was similar to that of Silver (1963). The cathode consisted of platinum wire (10 µ in diameter) fused into a glass capil lary, and the anode of a silver-silver chloride wire: a 12 µ thick Teflon mem brane separated the electrode from the test sample ; the response time of the electrode was about 1 were calibrated in their sec. The galvanometer readings

3 Sperm motility and respiration 105 equivalents of oxygen tension by taking readings in air and in argon or nitrogen from which traces of oxygen were removed by passing the gas through an alkaline pyrogallol solution (15% pyrogallol solution in 40 % NaOH). The calibration points were checked at the beginning and end of every run. Once the observation chamber and side-arms have been filled with an from the to fall due to the aerated sperm suspension, no extra oxygen can diffuse into the sample atmosphere, consequently the 02 concentrations will begin oxygen consumption by the spermatozoa and will continue to decrease steadily until finally the spermatozoa cease to respire and become immotile due to lack of oxygen. The total time until inactivation is usually 2 to 10 min (Schindler & Nevo, 1962), depending on the specific activity of the suspension, hence the importance of using an electrode with a short response time. Apparatus for simultaneous measurement of oxygen concentration and Text-fig. 1. sperm motility. a, observation chamber; b, oxygen electrode assembly; c, pear-shaped vessel; d, constant temperature bath. The changes in 02 concentration and simultaneous motility observations were recorded as a function of time ; from the graph obtained, respiratory rate and motility as a function of oxygen concentration could be calculated. RESULTS Within a wide range of oxygen concentrations, from that in air down to about 0-6 % 02, the respiratory rate of the spermatozoa was found to be independent of oxygen concentration. The results of a typical experiment are shown in Textfig. 2. It will be seen that above a critical 02 partial pressure of 4 mm Hg (corresponding to an 02 concentration of 0-54%), the respiratory rate was constant; at this point there was a sharp decrease in respiratory rate and below

4 106 A. C. Nevo 1 mm Hg 02 partial pressure (about 0-13 % 02), oxygen consumption was zero. Motility changes paralleled those of the respiratory rate exactly no motility changes could be observed until the critical 02 concentration was reached, then there was a very rapid inactivation of the bulk of the cells; some motion, mainly weak motions of the tails without movement of the whole spermatozoa, con tinued for a short while until it also ceased completely, coincidently with cessa tion of oxygen consumption. Similar results were obtained with all three species and no appreciable differences were found in the critical 02 levels. At physiological temperatures, the critical values were between 4 and 5 mm Hg (0-54 to 0-67 % 02). Motility and respiratory rate equal zero Time (min) Text-fig. 2. Oxygen concentration and sperm motility as a function of time, in a suspen sion of washed ram spermatozoa, at 37 C. To determine the effects of glucose and of fructose on the rate of respiration, split samples of the same washed sperm suspension were used ; sugar was added to one sample while the other was used as control. It was found that during the period of the experiment the rates of oxygen consumption and the critical 02 concentrations were not appreciably altered by the presence of fructose or glucose. DISCUSSION The present investigation has shown that within a wide range of oxygen con centrations, from about 0-6 % 02 to that in air, the spermatozoa are capable of maintaining a characteristic high level of respiratory activity which is ex- 15

5 Sperm motility and respiration 107 pressed in a high level of motility. The findings obtained for bull, ram and cock spermatozoa, if applicable to other species, would suggest that under condi tions in vivo, and particularly in the female genital tract, the spermatozoa should be capable of supporting a high degree of motility by endogenous respiration alone. Campbell (1926, 1932) found in the uterus and in the peritoneal cavity of the rabbit an oxygen tension of about 40 mm Hg, Bishop (1956) found in the oviduct of the oestrous rabbit an average oxygen tension of about 45 mm Hg and Nevo & Schindler (unpublished results) found in the oviduct of the hen an oxygen tension of about 35 mm Hg. These oxygen and hence able to pressures are well above the critical values of 4 to 5 mm Hg, support maximum aerobic motility. It has to be remembered, however, that in addition to respiration, sperm atozoa, at least those of the species used in the present study, are endowed with the ability to support motility anaerobically by glycolysis of extracellular sugar. This ability has apparently developed in animals which reproduce by internal fertilization, in association with the appearance of sugar in the seminal plasma; it is absent in species with external fertilization (Mann, 1964, p. 265). This suggests that it is an evolutionary adaptation which increases the chances of successful internal fertilization, despite the apparently optimal conditions for aerobic motility encountered by the spermatozoa in the female genital tract. (For a discussion of the significance of anaerobic and aerobic metabolism for sperm survival in vivo see Mann, 1964, p. 293.) ACKNOWLEDGMENTS I am greatly indebted to Lord Rothschild, who made my visit and stay in Cambridge possible, and to Dr T. Mann, Director of the Unit of Reproductive Physiology and Biochemistry, for kindly affording laboratory facilities and for his continued interest and valuable advice. I also wish to thank Dr I. A. Silver for the loan of the oxygen measuring equipment and for his unfailing helpful ness. REFERENCES Bishop, D. W. (1956) Oxygen concentration in the rabbit genital tract. Proc. 3rd int. Congr. Anim. Reprod., Cambridge, Section 1, p. 53. Campbell, J. A. (1926) The normal CO2 and O2 tensions in the tissues of various animals. J. Physiol. 61, 248. Campbell, J. A. (1932) Normal gas tensions in the mucous membrane of the rabbit's uterus. J. Physiol. 76, 13p. Humphrey, G. F. & Mann, T. (1949) Studies on the metabolism of semen. Biochem. J. 44, 97. Mann, T. (1964) The biochemistry of semen and of the male reproductive tract. Methuen, London. Schindler, H. & Nevo, A. C. (1962) Reversible inactivation and agglutination offowl and bull sperma tozoa under anaerobic conditions. J. Reprod. Fértil. 4, 251. Silver, I. A. (1963) A simple micro-cathode for measuring 2 in gas or fluid. Med. Electron, biol. Engng. 1, 547.

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