MUSCULAR ACTIVITY DURING PREPARATION FOR FLIGHT IN A BEETLE
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1 J. Exp. Biol. (1965), 43, 40^ With 3 text-figures Printed in Great Britain MUSCULAR ACTIVITY DURING PREPARATION FOR FLIGHT IN A BEETLE BY DENNIS LESTON, J. W. S. PRINGLE AND D. C. S. WHITE Department of Zoology, Oxford (Received 24 September 1964) In many insects flight is preceded by a period of muscular activity, during which the temperature of the thorax is raised (Dotterweich, 1928; Krogh & Zeuthen, 1941). The temperature changes accompanying this phenomenon in hawk-moths have recently been reinvestigated by Dorsett (1962) and the influence of temperature on the performance of flight muscles from various species has been considered by Neville & Weis-Fogh (1963), Machin, Pringle & Tamasige (1962) and Miller (1964), but little attention appears to have been paid to the mechanisms by which mechanical activity is generated. In the case of those insects (Orthoptera, Lepidoptera, Odonata) where the flight muscles are of the synchronous type with the rhythm of muscular activity determined by the pattern of motor nerve impulses there is little difficulty in understanding how movements of small amplitude can be produced by twitches of the flight muscles. But in insects with asynchronous, fibrillar flight muscles (Diptera, Hymenoptera, Coleoptera) it is known that rhythmic muscular activity depends on the form of the mechanical loading and it is not immediately apparent how vibration and heating can be produced when the wings are folded. No movement of the wings or elytra is visible during the pre-flight activity of beetles and bees, although there is electrical activity in the flight muscles (Krogh & Zeuthen, 1941). It was noticed by one of us (D.L.) that the pre-flight activity of a beetle, Acilius sulcatus (L.), produced a sound which rose steadily in pitch; this was therefore recorded in the hope that oscillographic analysis might provide some data on the mechanical processes involved. MATERIAL AND BEHAVIOUR Acilius sulcatus (L.) is a water beetle, family Dytiscidae, about mm. long, fairly common throughout the British Isles (Balfour-Browne, 1950). It shows marked sexual dimorphism in the structure of the elytra but, unlike many other dytiscids, is not polymorphic in wing size or in the degree of development of the flight muscles (Jackson, 1950a). The adults overwinter in ponds, both sexes dispersing when mature by flight during the spring. Flight usually occurs at night. The specimens used were captured at ponds around London during March and their behaviour in aquaria under dim light demonstrated that they were ready to migrate. Males were allowed to walk out of the water and manoeuvred onto a cork mat which was then placed 2 or 3 in. from a clamped crystal microphone. A Grundig TK 820 recorder and pre-amplifier were used for recording on standard tape at 7-5 in./ sec. tape speed; the air temperature was noted at the time of recording.
2 4io DENNIS LESTON, J. W. S. PRINGLE AND D. C. S. WHITE While producing pre-flight sound the wings are folded under the elytra and the insect remains outwardly still, save for a vibration of the thorax and elytra which can be felt rather than seen. A second or two after maximum frequency is reached the beetle commences to walk rapidly and, if able to lift its front tarsi off the substratum by climbing any available projection, opens its wings and flies. /VWWWWWWWN /vwvwwwwvw!! I I! I I I!! H^^l^^^WM^ vvvvvvvvvvvvvvvv Fig. I. OsciUograms from magnetic tape recording of the sound produced during pre-flight activity in Acilius tulcatut (L.). (a), at the start; (6), at the highest pulse frequency; (c), (d), the final decline (at higher gain). Time signal represents 2oo/sec. (see text). OSCILLOGRAPH ANALYSIS The tape recording, made at 7-5 in./sec., was played back at 3-75 in./sec. with a time signal at 100/sec.; on the oscillograms (Fig. 1) the time signal therefore represents a frequency of 200/sec. The sound track shows a train of highly damped pulses and there is usually a clear difference in amplitude and shape between alternate pulses. In a recording made at an air temperature of 19 0 C. the duration of pre-flight activity is 4 min. The frequency increases at first rapidly and then more slowly; after reaching 140/sec. it declines abruptly to 70/sec. in i-6 sec. before activity stops. Fig. 2 shows the change in frequency of the large alternate pulses during the whole period of activity and Fig. 3 shows the form of the final decline on a faster time scale.
3 Muscular activity during preparation for flight in a beetle r 120 I 80 D 1 3 I I I I t i l l Fig. a. Frequency of large (alternate) pulses during pre-flight activity at 19 C. air temperature sec. Fig. 3. Final decline in pulse frequency. DISCUSSION The mechanical properties of beetleflightmuscles. The mechanical properties of the isolated basalar muscles of the beetles Melolontha melolontha (L.), Lucanus cervus (L.) and Oryctes rhinoceros (L.) were studied by Machin & Pringle (1959). Some experiments, as yet unpublished, were also carried out on the dorsal longitudinal and dorsoventral muscles. These fibrillar muscles were incapable of single twitch contractions and developed a smooth isometric tetanus if
4 412 DENNIS LESTON, J. W. S. PRINGLE AND D. C. S. WHITE stimulated at the frequency at which motor nerve impulses are normally present in flight. Oscillatory activity occurred only if the muscle was loaded with an inertia. During flight in beetles the inertia of the wings makes the greatest contribution to the inertial loading of the flight muscles; wing inertia cannot, however, contribute to the loading of the muscles when the wings are folded. An alternative method of generating oscillatory activity from fibrillar muscles is found in the sound-production system of certain cicadas (Pringle, 1954 a, b). Here the large timbal muscles are connected to a membrane of negligible inertia in such a way that there is a pronounced click action; a rise of tension in the muscle produces little movement until a critical tension is reached, whereupon the membrane moves rapidly into a new metastable position, emitting a pulse of sound. As tension falls the membrane suddenly clicks back into its original position, emitting a second sound pulse. The sound track of cicada song shows an alternation of IN and OUT pulses, corresponding to the two movements of the timbal membrane. The mechanism of oscillation in this mode of operation of the fibrillar muscles depends on a delayed 'deactivation by release' and 'activation by stretch'. Boettiger (i960) has shown by experiments in which the isolated basalar muscle of the beetle Oryctes is subjected to quick stretches and releases that a delayed rise and fall in tension occurs also in fibrillar flight muscle under these mechanical conditions and it is now clear (Pringle, 1963, 1964) that the two modes of operation do, in fact, reveal a single property of this type of muscle. The general condition for oscillatory mechanical activity is that the characteristics of the load shall be such as to introduce a phase lag or time delay between the applied force and the resulting movement. Both an inertia and a click mechanism have this property. The significant feature of the performance of active, stimulated fibrillar muscle is that changes of length produce changes of tension after a phase lag or time delay. If the characteristics of the load are inversely matched to the characteristics of the active muscle, the whole muscle/load system generates oscillations at an appropriate frequency. Discussion of oscillograms The oscillograms of Fig. 1 show that the sound is emitted in pulses, with alternate pulses of different amplitude and shape. There is no visible wing movement and the load cannot therefore have appreciable inertia. It is difficult to avoid the conclusion that in the pre-flight activity of beetles the flight muscles are operating not in the inertial mode, but are generating an oscillation because of the presence of a click system, presumably in the movement of the axillary sclerites while the wings are held folded. If this interpretation of the records is correct, alternate pulses of sound correpond to the IN and OUT movements of some part of the thoracic structure which occur suddenly because of the setting of the axillary sclerites; the wings are, however, effectively decoupled from the muscles when in the folded position by disarticulation of certain ball-and-socket joints at the wing base (Ruschkamp, 1927). Some more precise predictions can be made about the form of the oscillograms expected from such a click system. (1) The high-frequency vibrations within each pulse should start with opposite phase in the IN and OUT clicks. In spite of noise on the record this is clearly seen in Fig. 1 c, where each pulse is a diphasic wave.
5 Muscular activity during preparation for flight in a beetle 413 (2) The IN and OUT clicks occur when the strains in the cuticular structure reach critical values. In the sound-producing system of the cicada there is no muscle antagonism, tension in the timbal muscle being balanced by cuticular elasticity. In this asymmetrical system the duration of the IN-OUT interval remains constant even when the pulse frequency varies over a wide range (Text-fig. 9 of Pringle, 19546). In the thoracic mechanism of beetles one set of flight muscles must contract while the other relaxes. Provided that the temperature and the state of excitation are the same in all the muscles, the relative intervals between the two sorts of pulse should not change much as the pulse frequency changes. This is shown by the oscillograms. (3) The changes in pulse frequency during the pre-flight period could arise from two factors. The rate of activation after a quick stretch will depend on the level of activity of the intramuscular coupling process linking membrane excitation with activation of the contractile myofibrils. This factor probably accounts for the abrupt decline in pulse frequency at the end of the period. Isometric relaxation of Oryctes basalar muscle at 25 C. takes about 1 sec. when stimulation ceases (Machin & Pringle, 1959); this is comparable to the time of the final abrupt decline in pulse frequency in Acilius. The slow rise in pulse frequency throughout the pre-flight period probably signals the rising thoracic temperature. Accurate studies have not been made of the effect of temperature on the response of a fibrillar muscle to quick stretches and releases, but Machin et al. (1962) showed that there is a considerable speeding up at higher temperatures of the characteristics of active Oryctes muscle operated in the sinusoidal (inertial) mode. From their results it can be deduced that as the temperature rises there will be a more rapid redevelopment of tension after a quick stretch. This is the probable explanation of the rise in pulse frequency during the pre-flight activity of Acilius. The warm-up time of individual insects tested at temperatures between 18 and 20 0 C. ranged between 3-5 and 4-5 min. Jackson (19566) noted a time of' quite 5 min.' for the somewhat larger Dytiscus semisulcatus Mueller, presumably at air temperature. Machin & Pringle (1959) found a rise of temperature of 6 C. in 2 min. in Oryctes muscle delivering maximum oscillatory power. Large beetles may require a thoracic temperature of above 30 C. before the flight muscles can deliver enough power to the wings to maintain the insect in flight. Pre-flight activity is one of the ways in which muscle temperature can be raised above the temperature of the environment; as Miller (1964) points out, the alternative method of perching in sunlight is important in certain Odonata. SUMMARY 1. The sound produced during the pre-flight activity of the water beetle Acilius sulcatus (L.) consists of a train of pulses, implying that there is a click mechanism present in the thorax when the wings are folded. The pulse frequency rises as the temperature rises. 2. Analysis of the sound oscillograms reveals some differences from the analogous system in cicadas which can be correlated with differences in anatomy. 3. The sinusoidal (inertial) and pulsed modes of operation of insect fibrillar muscle are alternative ways in which oscillatory activity can be generated. They
6 414 DENNIS LESTON, J. W. S. PRINGLE AND D. C. S. WHITE result from a single property of this type of muscle and occur when it is coupled, respectively, to an inertial or to a clicking load. We are grateful to Dr A. C. Neville for helpful discussions. REFERENCES BALFOUR-BROWNE, F. (1950). British Water Beetles, 2. London: Ray Society. BOETTIGER, E. G. (i960). Insect flight muscles and their basic physiology. Arm. Rev. Ent. 5, DORSETT, D. A. (1962). Preparation for flight by hawk-moths. J. Exp. Biol. 39, DOTTERWEICH, K. (1928). Beitrdge zur Nervenpkysiologie der Insekten. Zool. Jb. (Allg. Zool. Pkysiol,), JACKSON, D. J. (1956a). The capacity for flight of certain water beetles and its bearing on their origin in the Western Scottish Isles. Proc. Linn. Soc. Lond , JACKSON, D. J. (19566). Observations on flying and flightless water beetles. J. Linn. Soc. Lond. {Zool), 43, KROOH, A. & ZEUTHEN, E. (1941). The mechanism of flight preparation in some insects. J. Exp. Biol. 18, MACHTN, K. E. & PRINGLE, J. W. S. (1959). The physiology of insect fibrillar muscle. II. Mechanical properties of a beetle flight muscle. Proc. Roy. Soc. B, 151, MACHIN, K. E., PRrNGLE, J. W. S. & TAMASIGE, M. (1962). The physiology of insect fibrillar muscle. IV. The effect of temperature on a beetle flight muscle. Proc. Roy. Soc. B, 155, MILLER, P. L. (1964). Notes on Ictinogompkus farox Rambur (Odonata, Gomphidae). Entomologist, NEVILLE, A. C. & WEIS-FOCH, T. (1963). The effect of temperature on locust flight muscle. J. Exp. Biol. 40, PRINGLE, J. W. S. (1954a). The mechanism of the myogenic rhythm of certain insect striated muscles. J. Physiol. 134, PRINGLE, J. W. S. (19546). A physiological analysis of cicada song. J. Exp. Biol. 31, PRINGLE, J. W. S. (1963). Physiologie du muscle de vol chez les insectes. Actualitis neurophysiol. V* serie, PRINGLE, J. W. S. (1964). Locomotion: flight In Physiology of Insecta (ed. Rockstein, M.). Academic Press. ROSCHKAMP, P. F. (1927). Der Flugapparat der Kfifer, Vorbedingung, Ursache und Verlauf seiner Ruckbildung. Zoologica, a8, Heft 75, 1-88.
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