Ann E. Kammer

Insect Flight Metabolism

Publisher Summary Actively flying insects achieve the highest metabolic rates known, and they do so in the fraction of a second required to shift from quiescence to flight. This chapter focuses on the various adaptations that make possible the high metabolic rates necessary for flight. Flight depends on the biochemical and mechanical work done by the flight muscles, which must be continually supplied with oxygen and fuel. The work of the muscles is under neural control and therefore the metabolic rate is also under neural control. Hormones participate as part of the biochemical mechanisms by which the neural commands are executed and also as part of the internal milieu supportive of flight. In larger insects, high metabolic rates and the associated heat production result in elevated body temperatures; temperature effects and temperature regulation are thus closely related to flight. Control of flight metabolism is accomplished by a complicated meshwork of neural, hormonal, and biochemical mechanisms. Control of the rate of metabolism is primarily neural, since the frequency of excitation of the flight muscles provides the primary control on the demand for metabolic performance. The metabolic machinery of the muscle is also influenced by these neural signals, since Ca ++ released by excitation modulates enzyme activity. Hormones that control the uptake of substrates and perhaps other biochemical reactions in the muscles also influence muscle metabolism.

The motor output during turning flight in a hawkmoth, Manduca sexta

Abstract Electrical activity was recorded extracellularly from mesothoracic flight muscles and the position of the wings was observed during attempted turning by Manduca sexta in fixed flight. The results show that changes in the phase relationships among the motor neurons to the flight muscles are an important part of the neural code by which this hawkmoth controls its flight direction. The third acillary muscle, previously presumed to function in folding the wing at the end of flight, was phasically active during flight. During turns toward the side from which the recordings were made, the wing was remoted, and the third axillary muscle was excited by one to several impulses just before the main depressor muscle (dorsal longitudinal, DLm). During a turn in the opposite direction, the third axillary muscle fired shortly before or with the elevator muscles. The subalar muscle was excited shortly before the DLm during remotion; during promotion it was excited in phase with the DLm or with both the DLm and the elevator muscles. Large changes in phase relationships also occurred in the basalar muscle. In the third axillary and basalar muscles, transition from one phase relationship to another usually involved firing at twice the wingbeat frequency. This observation suggests that the motor neurons to the direct muscles can be loosely coupled to the neurons supplying either the DLm or the elevator muscles. Phase changes during flight also occurred in decapitated animals stimulated with a touch on one side of the abdomen. Therefore alteration of phase relationships and production of motor patterns which result in a turn do not require signals from the brain.

Maturation of the flight motor pattern without movement inManduca sexta

The development of the flight motor pattern was studied by recording acutely with fine wire electrodes inserted in the thoracic muscles of pharate moths of known age and by recording chronically for up to 8 days with implanted electrodes. Externally visible morphological characteristics by which the age of a pharateManduca sexta can be established were identified (Table 1).Bouts of activity lasting approximately 30 min to 2 h and alternating with inactive periods of similar duration were recorded as early as the ninth day after pupation and on all successive days until early on the day of eclosion, typically 19 days after pupation (Figs. 1,5). During the 3 days preceding the day of eclosion a rhythmic flight motor pattern was produced (Fig. 2). The rhythmic activity ceased 51/2–101/2 h before eclosion and only an occasional, large potential change was recorded from the thoracic muscles during this time (Fig. 3).During the 3 days of rhythmic activity the percent-age of time that the animal was active did not change (Fig. 4). The flight motor pattern matured, in that the cycle-time decreased and became less variable (Fig. 6). The approximate flight phase relationship between an elevator muscle and the dorsal longitudinal depressor muscle did not become less variable as the cycle-time improved.The flight motor pattern produced by pharate moths caused neither movement of the scutum nor an increase in thoracic temperature in marked contrast to the consequences of adult motor activity (Fig. 7).Intracellular recording from the dorsal longitudinal muscle of pharate moths 20–30 h before eclosion showed that, after repeated stimulation of the motor nerve at 2/s, only small junctional potentials were elicited (Fig. 8). A burst of 6 stimuli at 50/s elicited 2–5 active membrane responses and a contraction. These observations explain the absence of thoracic movement in immature animals producing the flight motor pattern and the presence of movement in immature animals stimulated to eclose. They also show that the neuromuscular junction matures rapidly during the day before eclosion.

Thoracic temperature, shivering, and flight in the monarch butterfly, Danaus plexippus (L.)

SummaryMonarch butterflies, Danaus plexippus (L.), display a warm-up behavior characterized by wingstrokes of small amplitude. Thoracic temperature during this shivering and during fixed flight was measured by means of a smallbead thermistor inserted into the thorax. At ambient temperatures of 15–16°C, once shivering is initiated the thoracic temperature rises at a maximum rate of 1.3°C/min, and a thoracic temperature 4.0°C greater then ambient is produced (Table 1). Fixed flight at these low ambient temperatures results in a similar rate of increase in thoracic temperature, and a similar temperature excess is produced (Fig. 3). At ambient temperatures between 22 and 35°C the thoracic temperature of an animal starting to fly rises at a faster rate, 3.6°C/min, and reaches a greater excess, 7.9°C (Fig. 4). The wingbeat frequency of animals in fixed flight increases with increasing thoracic temperature (Fig. 2). In the absence of direct solar radiation, shivering typically occurs prior to flight at low ambient temperatures (13–17°C), and the resulting increase in thoracic temperature allows monarch butterflies to fly at these cool temperatures.

Patterned muscle activity during eclosion in the hawkmothManduca sexta

SummaryManduca sexta escapes from the pupal cuticle by coordinated movements of abdomen, wing-bases, and legs. We have examined the thoracic motor output during eclosion by recording extracellularly from the indirect flight muscles. The motor pattern produced during wing-shrugging movements (Fig. 2) is characterized by alternating activity in the flight muscles and increasing numbers of muscle potentials per burst in successive cycles of wing movements. The wing-shrugging motor pattern differs from that of flight and from the pattern produced by an adult moth with its wings restrained (Figs. 3, 6). Eclosion behavior, including the typical motor pattern, can be induced prematurely, 30–36 h before eclosion. Young adults that have already expanded their wings can be stimulated to repeat the eclosion and wing-expansion behavior, but after 20 h post-eclosion, both responses disappear (Fig. 5). Restraint and mechanical stimulation, particularly of the legs, are important stimuli in eliciting eclosion behavior. Since eclosion in saturniid moths is initiated by a hormone, the effectiveness of mechanical stimuli was unexpected.

Neural control of bumblebee fibrillar muscles during shivering

SummaryMuscle potentials were recorded extracellularly from the fibrillar flight muscles ofBombus sonorus andB. fervidus during shivering and during flight. During some bouts of shivering motor units of the same muscles, of synergistic muscles, and of antagonistic muscles were excited with relatively synchronous bursts of impulses. These bursts were separated from each other by varying intervals. The latency between the beginning of bursts in different units of antagonistic muscles was usually less than 12 msec. However, during other bouts of less vigorous shivering the synchrony was less precise. During any one portion of flight the interspike intervals of any one muscle unit were relatively constant, and all possible phase relationships were observed between the different muscles. The results show that control of fibrillar muscle involves 1) the average frequency of activation of individual muscles and 2) timing of the activation of muscles with respect to each other.

A comparative study of motor patterns during pre-flight warm-up in hawkmoths

SummaryTemporal patterns of activation of flight muscles were recorded by means of wires placed extracellularly in thoracic muscles. In the five species of hawkmoths studied, wingstrokes of small amplitude were produced during a preflight warm-up by synchronous contractions of certain groups of muscles which are antagonists in flight. The main depressor muscle, the dorsal longitudinal, was excited in synchrony with some or all of the indirect elevator muscles. Three direct muscles, the subalar, basalar and third axillary muscles, were usually excited out of phase with the dorsal longitudinal muscle. However, details of the motor pattern varied from species to species. During fixed flight phase changes comparable in magnitude to those which occur during the transition from warm-up to flight were observed in Manduca sexta and Smerinthus cerisyi. The results (summarized in Table 2) suggest that a variety of warm-up patterns evolved within the Sphingidae as modifications of a common mechanism generating flight motor patterns.

Role of the wings in the absorption of radiant energy by a butterfly

Abstract 1. 1. Measurements were made of the thoracic temperature of Danaus plexippus exposed to artificial radiation of an intensity comparable to sunlight. 2. 2. Butterflies with wings ablated warmed more slowly and attained a slightly lower equilibrium temperature (mean difference, 2·1°C) than did intact animals, the equilibrium temperature of which averaged 8·7°C above ambient temperature. 3. 3. The amount of water in the wings is small (mean = 17 mg), and the rate of circulation of the hemolymph, as indicated by the dispersal of vital dyes injected into the thorax, is slow. Therefore, circulation of the hemolymph does not provide a mechanism for a significant exchange of heat between the body and the wings of these butterflies. 4. 4. Dead animals with wings severed attained a temperature equilibrium 2·2°C greater than that of live butterflies with wings severed.

Control of ventilatory movements in the aquatic insect Corydalus comutus: central effect of hypoxia

ABSTRACT. The influence of hypoxia and hypercapnia on the ventilatory rhythm of the hellgrammite Corydalus cornutus L. (Megaloptera) was studied. In intact animals the frequency of rhythmic retractions and protractions of abdominal gills is increased by hypoxia (10% O2, 90% N2) but no ventilatory response is elicited by hypercapnia (1–5% CO2, 20% O2, 75–79% N2).

Membrane structures and physiology of an immature synapse

SummaryImmature synapses, developing moth neuromuscular junctions, were studied using electrophysiological and ultrastructural techniques and were compared with synapses from the flight muscles of adult moths. Neuromuscular junctions, formed by short side branches of the single fast motor axon, were assessed for functional state by stimulating the nerve and recording the endplate potential intracellularly from the muscle fibre. The muscle was then fixed and prepared for scanning, thin-section, and freeze-fracture microscopy.The immature stage differs from the adult by having very small (average 7.8 m V, compared with 20–30 mV), long duration ejps that fatigue rapidly. The immature junctions are, however, only 13% shorter than those of the adult. Within the junction, the nerve terminal comes into direct contact with the muscle membrane in a series of oval patches separated by glial processes. These regions of apposition or ‘plaques’ in the immature synapse are about half the diameter of the adult plaques. In freeze-fractured material, the nerve terminal membrane in the plaque region bears an irregular band of particles on the cytoplasmic leaflet; the length of the band is essentially the same in the immature synapse as in the adult. This band marks the location of the active zone, an electron dense bar of the same length in thin section. The apposing external leaflet of the muscle membrane bears a patch of postsynaptic particles; the patch is much smaller than in the adult plaque. These immature patches, presumably representing clusters of receptors, range in size from a dozen particles to a hundred or more. We consider it likely that a lack of postsynaptic receptors may partially explain the very small ejp in the developing synapse, but that other factors may also be limiting.Desmosome-like contacts between glial cells and the muscle fibre were observed. Small wisps of electron dense material appear to bridge the extracellular space between the nerve terminal and the muscle fibre or between the glial processes and the muscle fibre in some locations. They are found in the same regions of the neuromuscular junction as small groups of large particles, suggesting that these two features are different aspects of the same structure. From their location one could hypothesize that they have either a mechanical function of stabilizing the glial invaginations, or a role in communication between the three types of developing cell.