Prolonged Flight Research Articles

Influence of Larval Starvation and Adult Diet on Long-Duration Flight Behavior of the Migratory Moth Agrotis ipsilon (Lepidoptera: Noctuidae)

Starving fourth-instar Agrotis ipsilon (Hufnagel) for 4 d did not increase the propensity of 3-d-old moths to engage in long-duration (i.e., ≥1 h) continuous flights, or the duration of such flights, on flight mills. Adult diet (nothing, distilled water, or honey–water) did not significantly influence male flight propensity until 2 d of age or female propensity until 3 d of age. Male propensity to fly and flight profiles (flight duration, times of flight initiation and termination) seem to depend more upon the availability of liquids than carbohydrates, whereas female behavior is more dependent on a carbohydrate source. In all instances, the influence of both larval and adult diet stress on flight propensity and duration is negative. One would expect a positive effect if such stress factors act as cues that trigger a behavioral or physiological shift to a migratory phase. Instead, environmental factors that stress individuals seem only to decrease the already high propensity to make prolonged flights and decrease the duration of those flights.

The molecular and metabolic essentials for long-distance flight in insects

The mechanism of long-distance flight in insects was investigated by comparing lipid mobilization and transport in gregarious- and solitary-phase locusts and in the American cockroach. Unlike the gregarious-phase locust, both the American cockroach and the solitary locust were unable to form low-density lipophorin (loaded with increased amount of diacylglycerol) even when injected with adipokinetic hormone (AKH). The cockroach fat body responded to AKH. However, not only does the American cockroach lack apolipophorin-III (apoLp-III) in the haemolymph, but the fat body contains only an extremely small amount of diacylglycerol and a relatively large triacylglycerol pool. By contrast, the solitary-phase locust had apoLp-III in the haemolymph, but the fat body was only one-seventh or less in weight of the fat body of the gregarious locust. Furthermore, the fat body of the solitary locust contains a very small amount of triacylglycerol (1/20 or less of that of the gregarious locust) with only a trace of diacylglycerol. It was concluded that in the American cockroach and the solitary locust, the stores of fuel in the fat body are insufficient to maintain prolonged flight.

Basal and stress-induced corticosterone levels of garden warblers, Sylvia borin, during migration

Plasma levels of the metabolically and behaviorally active corticosteroid hormone, corticosterone, were studied in garden warblers in the laboratory and in the field during the autumnal migratory phase. Garden warblers showing nocturnal migratory activity in the laboratory had elevated levels of corticosterone at the end of the dark phase and low levels during daytime. When nocturnal migratory activity was experimentally disrupted by food deprivation and subsequent refeeding or after spontaneous termination of migratory activity this rhythm was absent. Garden warblers stopping over in the Sahara desert during autumnal migration had low levels of corticosterone. Levels were negatively correlated with fat stores and body mass in birds sampled throughout the day. These levels were generally lower than those associated with stress in response to repeated handling and blood sampling. The results suggest (1) the existence of diel changes in adrenocortical hormonal activity that could be involved in regulation of migration, and (2) that garden warblers carrying large fat depots are not stressed by prolonged flight or lack of appropiate feeding areas during migration over the desert.

Flight and heat dissipation in migratory birds

The effect of temperature on the functional properties of hemoglobins from two different species of birds,i.e. Gallinula chloropus and Columba livia, has been investigated. These two species are characterized by different life-behaviour, sinceGallinula chloropus is seasonally subjected to prolonged flights, whileColumba livia although flying at a quite high velocity (~50 Km/h) is not able to maintain the corresponding muscular activity for more than 10 minutes. The results reported in this paper suggest that in some migratory species, special molecular mechanisms may increase heat dissipation and stabilize the body temperature at a reasonable level. In fact birds, during normal sustained flight, must be able to dissipate more than eight times as much heat as during rest in order not to be overheated.

Changes in chromatin and nucleic acids in rat tissues after two-week spaceflight

The quantitative changes in nucleic acids and chromatin breakdown were followed in blood, thymus and spleen in rats after 14 day flights on board the biosatellites Cosmos-1887 and Cosmos-2044. Quantitative nucleic acid changes within 8–11 h after landing were only mild, most statistically non-significant. An analysis at 48 h after landing showed a marked decrease in a total content of DNA and RNA in spleen and thymus. Within 8–11 h after landing, the symptoms of chromatin breakdown were found as is seen in an increased concentration of its fragments—polydeoxyribonucleotides. The obtained results show that a partial adaptation to microgravity occurs up to flight day 14 in lymphoid organs. Adaptation is accompanied with a reappearing of the sensitive cells. Their chromatin breaks down, then, in a final phase of flight due to hypergravity stress manifesting itself by a temporary increase in poly-deoxyribonucleotide concentration several hours after landing. The results are discussed in relation to the changes in chosen parameters after shorter or more prolonged flights.

Locust flight metabolism studied in vivo by 31P NMR spectroscopy

Flight metabolism of locusts has been extensively studied, but biochemical and physiological methods have led to conflicting results. For this reason the non-invasive and non-destructive method of 31P NMR spectroscopy was used to study migratory locusts, Locusta migratoria, at rest and during flight. 1. In the flight muscle of resting locusts the ratio of phosphoarginine to ATP was the same whether determined by NMR (1.76) or biochemically, but the NMR-visible content of inorganic phosphate (Pi) was only 40% of ATP, i.e., much lower than total Pi as determined biochemically. This suggests that most of the Pi in flight muscle is not free, and hence not available as substrate or effector for cytosolic enzymes. Similarly, the free content of ADP and AMP in resting muscle was calculated to be much lower than the total content. 2. Flight brought about a marked increase in Pi and a decrease in phosphoarginine in flight muscle although there was no change in intracellular pH. 3. At the initiation of flight a new ‘steady state’ of ATP, Pi, and phosphoarginine was rapidly established and minimal changes occurred after the first 2 s of flight. 4. From the free contents of ATP and phosphoarginine in working flight muscle the flight-induced fractional increases in free ADP and free AMP were calculated to be 5.0-fold and 27.4-fold, respectively. As Pi, ADP, and AMP are substrates and potent effectors of enzymes, the flight-induced increase in their contents is likely to have marked effects on metabolic flux in working muscle. 5. After short-term flight as well as prolonged flight, phosphoarginine, ATP, and Pi returned rapidly to their preflight levels, indicating that metabolic recovery from flight is rapid. 6. The locust appears to be an appropriate model for the study of metabolic regulation in aerobic muscle during exercise.

Adipokinetic Hormones and Lipoprotein Interconversions During Locust Flight

During prolonged flight, locusts predominantly utilize lipids for energy generation. Lipid stores are mainly located in the fat body. Flight is accompanied by release of adipokinetic hormones from the corpora cardiaca. Under the influence of these hormones, fat body triacylglycerol is converted to diacylglycerol, which is released into the haemolymph. This release requires the presence of specific lipoproteins. The lipid mobilizing effect of adipokinetic hormone on the fat body is attended by the association of a high density lipophorin and a non-lipid containing protein, both already present in the haemolymph, and the increased amount of released lipid to form a new lipoprotein, low density lipophorin. Upon delivery of the lipid to the flight muscles, participating proteins dissociate again and can be reused for lipid uptake at the fat body (lipoprotein shuttle system). The flight-specific metabolic systems could be starting-points for new devices in control strategies.

Energetics and Thermoregulation of Popillia japonica Newman (Scarabaeidae, Coleoptera) during Flight and Rest

Total oxygen consumption ($V_{O_{2}}$ averaging 4.66 mL/h) of Japanese beetles (Popillia japonica Newman, Scarabaeidae, Coleoptera) during free flight was independent of body mass, while the mass-specific oxygen consumption $\dot{V}_{O_{2}}$ (averaging 52.14 mL/g · h⁻¹) was inversely related to body mass. Variations in wing beat frequency, ambient temperature ($T_{a}$), and thoracic temperature ($T_{th}$) did not alter $\dot{V}_{O_{2}}$. However, during the first few seconds following takeoff, flight metabolism was substantially increased. No change in wing beat frequency occurred during this time period; however, in separate experiments, larger wing beat amplitudes were observed during initial flight. Correspondingly, thermoregulation was more pronounced during takeoff and gradually disappeared in prolonged flight. Measured $T_{th}$ excesses were supported by data on metabolic heat gain and heat loss based on cooling curves. In resting beetles, whole-animal $\dot{V}O_{2}$ (0. 16 mL/h, averaged over a ran...

Multiple feedback loops in the flying cockroach: excitation of the dorsal and inhibition of the ventral giant interneurons.

1. In a tethered cockroach (Periplaneta americana) whose wings have been cut back to stumps, it is possible to elicit brief sequences of flight-like activity by puffing wind on the animal's body. 2. During such brief sequences, rhythmic bursts of action potentials coming from the thorax at the wingbeat frequency, descend the abdominal nerve cord to the last abdominal ganglion (A6). This descending rhythm is often accompanied by an ascending rhythm (Fig. 2). 3. Intracellular recording during flight-like activity from identified ascending giant interneurons, and from some unidentified descending axons in the abdominal nerve cord, shows that: (a) ventral giant interneurons (vGIs) remain silent (Fig. 3); (b) dorsal giant interneurons (dGIs) are activated at the onset of the flight-like activity and remain active sporadically throughout the flight sequence (Fig.4); (c) some descending axons in the abdominal nerve cord show rhythmic activity phase-locked to the flight rhythm (Fig. 5). 4. Also during such brief sequences, the cercal nerves, running from the cerci (paired, posterior, wind sensitive appendages) to the last abdominal ganglion, show rhythmic activity at the wingbeat frequency (Fig. 6). This includes activity of some motor axons controlling vibratory cercal movements and of some sensory axons. 5. More prolonged flight sequences were elicited in cockroaches whose wings were not cut and which flew in front of a wind tunnel (Fig. 1B). 6. In these more prolonged flight sequences, the number of ascending spikes per burst was greater than that seen in the wingless preparation (Fig. 8; compare to Fig. 2). Recordings from both ventral and dorsal GIs show that: in spite of the ongoing wind from both the tunnel and the beating wings, which is far above threshold for the vGIs in a resting cockroach, the vGIs are entirely silent during flight. Moreover, the vGIs response to strong wind puffs that normally evoke maximal GI responses is reduced by a mean of 86% during flight (Fig. 9). The dGIs are active in a strong rhythm (Figs. 11 and 12). 7. Three sources appear to contribute to the ascending dGI rhythm (1) the axons carrying the rhythmic descending bursts; (2) the rhythmic sensory activity resulting from the cercal vibration; and (3) the sensory activity resulting from rhythmic wind gusts produced by the wingbeat and detected by the cerci. The contribution of each source has been tested alone while removing the other two (Figs. 13 and 14). Such experiments suggest that all 3 feedback loops are involved in rhythmically exciting the dGIs (Fig. 15).

Central and regional hemodynamics in prolonged space flights

This paper presents the results of measuring central and regional (head, forearm, calf) hemodynamics at rest and during provocative tests by the method of tetrapolar rheography in the course of Salyut-6-Soyuz and Salyut-7-Soyuz missions. The measurements were carried out during short-term (19 man-flights of 7 days in duration) and long-term (21 man-flights of 65–237 days in duration) manned missions. At rest, stroke volume (SV) and cardiac output (CO) as well as heart rate (HR) decreased insignificantly (in short-term flights) or remained essentially unchanged (in long-term flights). In prolonged flights CO increased significantly in response to exercise tests due to an increase in HR and the lack of changes in SV. After exercise tests SV and CO decreased as compared to the preflight level. During lower body negative pressure (LBNP) tests HR and CO were slightly higher than preflight. Changes in regional hemodynamics included a distinct decrease of pulse blood filling (PBF) of the calf, a reduction of the tone of large vessels of the calf and small vessels of the forearm. Head examination (in the region of the internal carotid artery) showed a decrease of PBF of the left hemisphere (during flight months 2–8) and a distinct decline of the tone of small vessels, mainly, in the right hemisphere. During LBNP tests the tone of pre- and postcapillary vessels of the brain returned to normal while PBF of the right and left hemisphere vessels declined. It has been shown that regional circulation variations depend on the area examined and are induced by a rearrangement of total hemodynamics of the human body in microgravity. This paper reviews the data concerning changes in central and regional circulation of men in space flights of different duration.

The development of enzymes involved in flight muscle metabolism in Spodoptera exempta and mythimna separata

1. 1. The activities of PFK, HK, GDH, CAT, HOAD, GIDH and CS were measured in the bodywall muscles of final instar larvae and in the thoraces of female Spodoptera exempta and Mythimna separata in the pupal stage and throughout adult life. Activities were compared in moths starved or fed sucrose solution from emergence. 2. 2. The activity profiles of the enzymes are considered in relation to the moths' capacity for prolonged flight and reproductive status. 3. 3. In S. exempta there is a rapid rise in the activity of PFK, HK and GDH associated with adult eclosion, suggesting that glycolysis is important at this time. The activities of these enzyemes in starved moths and those fed sucrose suggests that glycolysis may continue to have a role in flight muscle metabolism throughout adult life. 4. 4. The results are consistent with previous reports that lipid is the major source of energy fuelling prolonged flight in both species although the increase in the activity of CAT early in the adult life of sucrose-fed S. exempta appears to reflect lipid synthesis rather than flight potential. Changes in HOAD activity appear more closely associated with flight potential. 5. 5. Only CAT and HOAD showed any indication of a fall in activity associated with the onset of reproduction and probable cessation of prolonged flight. This result further supports the evidence for the utilization by both species of carbohydrate to fuel short flights which occur throughout life and of lipid to fuel prolonged, migratory flights in the pre-reproductive period.

The effect of larval phase on flight performance of African armyworm moths, Spodoptera exempta (Walker) (Lepidoptera: Noctuidae)

AbstractThe characteristics of the high and low density forms of noctuid moths, including Spodoptera exempta (Walker), exhibiting a density-dependent phase polyphenism have frequently been discussed in relation to migration. However, the only previous (unpublished) demonstration of an effect of larval phase on adult flight performance, using a tethered-flight technique, was invalidated by the recent discovery that the principal determinant of flight potential in S. exempta is genetic. When the incidence of prolonged flight was measured in moths derived from genetically-matched (full-sib) samples, there was a clear increase in long flights by females derived from the high-density gregaria phase larvae compared with those from solitaria phase larvae. The reasons for the apparent absence of a similar effect in males is not clear, but it is possible that the tethered-flight technique provides a less reliable index of flight capacity in this sex. The characteristics and significance of phase polyphenism in migratory noctuids are discussed. It is suggested that, in S. exempta and possibly some other comparable species, the high-density phase is adapted to accelerate re-dispersal after populations become concentrated, in order to escape the detrimental consequences of high larval densities.

Simultaneous monitoring of flight and oviposition of individual velvetbean caterpillar moths (by Wales, Barfield & Leppla, 1985): a critique

ABSTRACT. Flight durations of tethered female Anticarsia gemmatalis moths recorded in the laboratory were interpreted by Wales et al. as indicating a capacity for significant inter‐reproductive displacements in the field. Indications that their data may not support this conclusion are discussed and evidence is presented that, in tethered Spodoptera exempta, prolonged flights starting early in the night represent migratory behaviour while those of similar durations starting after midnight do not.

Properties of locust muscle 6-phosphofructokinase and their importance in the regulation of glycolytic flux during prolonged flight

6-Phosphofructokinase (PFK, EC 2.7.1.11) from the flight muscle of the locust (Locusta migratoria) was purified to a specific activity of 80 μmol min−1 (mg protein)−1 (at 25°C). 1. The enzyme is made up from subunits ofMr-81600, and the smallest catalytically active form is likely to be a tetramer. 2. PFK activity is markedly affected by the pH of the assay; the optimum pH was at about 8. 3. Physiological concentrations of ATP strongly inhibit locust PFK by shifting the S0.5 for fructose 6-phosphate (concentration required for 50% of maximum activity) out of the physiological concentration range. At pH 7.4 and about physiological concentrations of ATP, the curve of PFK activity against the concentration of fructose 6-phosphate is highly sigmoidal with S0.5 several hundred-fold higher than the concentration of fructose 6-phosphate in vivo. 4. The sigmoidicity and the S0.5 values for fructose 6-phosphate are decreased by addition of activators such as NH 4 + , inorganic phosphate, AMP and fructose 2,6-bisphosphate. The sensitivity of the response to these activators is increased by synergistic effects; marked synergistic effects were observed between inorganic phosphate and NH 4 + , fructose 2,6-bisphosphate or AMP as well as between AMP and fructose 2,6-bisphosphate. 5. Fructose 1,6-bisphosphate and fructose 2,6-bisphosphate are both activators of locust muscle PFK but the latter is much more potent than the former. Either of these compounds modifies the effect of the other; when phosphofructokinase is activated by fructose 2,6-bisphosphate, addition of fructose 1,6-bisphosphate results in inhibition of the enzyme activity; and when fructose 1,6-bisphosphate is present in the assay, higher concentrations of fructose 2,6-bisphosphate are required to increase the activity of the enzyme. 6. At low AMP concentrations, fructose 2,6-bisphosphate is not very effective in activating PFK, but AMP is effective at low concentrations of fructose 2,6-bisphosphate. 7. The properties of locust PFK suggest that the marked decrease in the concentration of fructose 2,6-bisphosphate that occurs in the locust flight muscle in the early stages of flight is, in part, responsible for the decrease in PFK activity and thus conservation of carbohydrate during prolonged flight, when lipid is the major fuel. At any stage of flight, however, an increase in energy demand could bring about an increase in PFK activity via increased concentrations of AMP and phosphate.

The effect of adult feeding on lipid and protein reserves in African armyworm, Spodoptera exempta, moths before and during reproduction

ABSTRACT. Newly‐emerged Spodoptera exempta (Walker) (Lepidoptera: Noctuidae) moths contain high levels of lipid held largely in the abdominal fat body, the quantity depending on the larval feeding conditions. There is a positive relationship between weight‐related lipid content and moth weight, which is consistent for female but not for male moths, suggesting that larval feeding conditions producing large individuals allow the accumulation of quantitatively disproportionate lipid reserves. Male and female moths have comparable levels of abdominal protein.Changes in the water content in starved moths or ones provided with distilled water or sucrose solution show that while starved individuals die rapidly from desiccation, water‐fed moths regulate their water contents between narrow limits which are higher for females than for males. Sucrose‐fed moths maintain higher, more variable water contents probably due to the phagostimulatory effect of the sugar.Reproducing and unmated moths are able to supplement their lipid and, to a lesser extent, their protein reserves following carbohydrate uptake.During both larval and early adult stages, the capacity to accumulate lipid reserves in excess of those apparently required for reproduction, suggests that these reserves also provide the main fuel for the prolonged flights of which migratory individuals are known to be capable.

Comparative Thermoregulation of Four Montane Butterflies of Different Mass

In this field study, I examine whether body mass affects flight behavior and thoracic temperature ($T_{th}$) in butterflies from a relatively cool environment (3,100 m high in the Sierra Nevada of California). Comparisons are made with thermoregulatory patterns of butterflies from other habitats and are discussed in terms of male mating strategies. The smallest (.023 g) butterflies examined (males ofAgriades glandon) spent 94% of the time in the morning basking and 6% flying. Near noon, they spent only 25% of the time perched (basking). Agriades glandon did not regulate a stable $T_{th}$. Instead, these small butterflies prolonged flight duration by storing heat prior to flight; the $T_{th}$ was on the average 9.2 C higher at takeoff than at landing. Almost all A. glandon basked dorsally near midday. However, a large percentage, 30% in the morning and 60% in the evening, basked laterally. Heating rates in the field were indistinguishable between lateral and dorsal basking positions in recently killed A. g...

MIGRATION IN THE GRASSHOPPERMELANOPLUS SANGUINIPES(FAB.). II. INTERACTIONS BETWEEN FLIGHT AND REPRODUCTION

Prolonged flight behavior in females of the grasshopper, Melanoplus sanguinipes (Fab.), decreases as ovarian tract weight increases relative to body weight. However, reproductive maturation does not always permanently terminate the migratory phase of the grasshopper's life cycle; long flights are also made after ovipositions. We examine the hypothesis that migration (measured as long-duration tethered flight behavior) decreases reproductive potential, either by delaying first oviposition or by decreasing production of egg pods. No negative effects of flight on oviposition were observed. Instead, age at first oviposition tended to decrease in females flown repeatedly compared to those flown only twice. Further, oviposition was greatly enhanced in females flown for several hours relative to unflown controls. We suggest that selection pressure for rapid and successful colonization has resulted in the evolution of a suite of characters including enhanced migratory behavior and accelerated reproduction in highly migratory populations.

Fructose 2,6-bisphosphate as a signal for changing from sugar to lipid oxidation during flight in locusts

Flight in locusts is initially powered mainly by carbohydrate but if flight is to be sustained, as in migration, the animals have to utilize fat as the predominant fuel. The molecular basis of this metabolic switch has not been identified. Fructose 2,6-bisphosphate is a potent activator of 6-phosphofructokinase (EC 2.7.1.11) purified from locust flight muscle. After the first few minutes of flight in the locust the concentration of fructose 2,6-bisphosphate in the flight muscle falls dramatically, which should lead to a decrease in the activity of 6-phosphofructokinase as part of the mechanism to conserve carbohydrate during prolonged flight.

SEX-SPECIFIC EMERGENCE OF IPS TYPOGRAPHUS L. (COLEOPTERA: SCOLYTIDAE) AND FLIGHT BEHAVIOR IN RESPONSE TO PHEROMONE SOURCES FOLLOWING HIBERNATION

AbstractEmergence patterns, sex ratios, and dispersal characteristics of Ips typographus L. (Coleoptera: Scolytidae) emerging from hibernation sites were studied under field conditions. A total of 8666 emerging beetles were caught in 14 tent-traps, covering brood tree stumps at 3 different hibernation sites. Samples of these beetles were sexed at frequent intervals. The proportion of females increased as emergence progressed and the overall proportion of females was 62%. A total of 3433 beetles emerging after hibernation were marked and released on 19 separate occasions. The recapture rates were 13 and 4% in nearby and distant pheromone traps, respectively. Recaptures were recorded at distances of up to 1800 m. Beetles were able to respond and fly to pheromone sources shortly after emergence without prior feeding or prolonged flight activity. Trapping and marking techniques, temporal and spatial emergence patterns, seasonal sex ratio changes, and factors influencing pheromone trap catches are discussed.

Foraging behavior of individual workers and foraging dynamics of colonies of three Sumatran stingless bees

SummaryThe foraging behavior of three stingless bees, Trigona (Tetragonula) minangkabau, T. (Trigonella) moorei and T. (Heterotrigona) itama, was studied to describe patterns of resource harvest in disturbed forest areas in Sumatra, Indonesia. Average daily total number of foraging flights per colony was 1200 in T. minangkabau, 2400 in T. moorei and 7000 in T. itama and it was proportional to colony population size. Foragers collecting nectar, pollen or plant resin were respectively 70–80%, 10–20% and <10% in the three species. Pollen was collected most in the morning. Nectar collection peaked in midday in T. itama but continued almost evenly until dusk in T. minangkabau and T. moorei. Resin was collected evenly throughout day. In all the three species the volume of a nectar load carried by a returning forager did not decrease until 1600, followed by slight decline. In the morning the sugar concentration of nectar was almost constantly 30%, and in the afternoon its maximum value reached 60% although some remained 30%. As a result, the mean sugar weight in a nectar load gradually increased until dusk. In T. minangkabau, resin was collected by specialized foragers. Nectar foragers switched to collect pollen and vice versa. There were two types of foraging: “exploitatory” flights, the repitition of short, rather constant flights bringing back full resource loads, and “exploratory” flights, prolonged flight and/or reduction in amount of resources carried. Exploitatory flights followed the exploratory flights which led to discovery of rich sources. Mean duration of exploitatory flights was 7 min during nectar collection, 12 min for pollen and 23 min for resin. Sites of exploited flowers were estimated to be 84–434 m distant from the nest site. Mean duration of flights for nectar collection was 13 min in the morning and 6 min in the late afternoon.