Fat combustion and metabolic rate of flying locusts ( Schistocerca gregaria Forskål)

Abstract

The nature and the amount of fuel used by flying Schistocerca gregaria Forskål have been estimated from direct analyses of the total content of fat and glycogen in control groups and in the corresponding flying groups, i.e. groups which had flown continuously for several hours. The locusts were cage-bred and resembled phase gregaria or phase transiens. Each batch was so homogeneous that it was possible to select two groups, consisting of six to fifteen individuals, which did not differ by more than 2 % from one another. Because of this uniformity and because of the high rate of metabolism during flight, this rate could be estimated within about ± 15 % (in one case ± 30 % ). For flight, the locusts were suspended at the periphery of a special roundabout (Krogh & Weis-Fogh 1952). The groups could choose the flying speed that they would naturally adopt. The speeds and durations of flight were of the same order of magnitude as observed in swarms in nature, so that some of the results could be applied to natural swarms. Analyses of the geometric similarity and of the distribution and nature of dry matter made possible an estimation of average size and gross composition of fully developed but sexually immature S. gregaria. Such standard individuals were found to contain large amounts of lipids (an average of 10 % of the fresh weight), and about 85 % of the stored energy was in the depot fat. The cuticle and the wing muscles of newly emerged adults (fledglings) contained only one-third of the dry matter that was found in fully developed individuals, and the accumulation of dry matter lasted 2 or 3 weeks. Fledglings were unable to fly or disinclined to fly for long. In spite of differences in age, sex, training and food, in all flight experiments fat constituted the principal source of energy, the remainder being glycogen. An average of 80 to 85 % of the total energy expenditure was derived from fats or fatty acids during the first 5 h of flight. All the available glycogen was utilized during the first few hours, most of it probably within the first hour. Flight was nevertheless maintained for several hours without reduction of speed. The metabolic rate on the roundabout increased approximately with the second power of the flying speed. The speed was almost independent of temperature and varied between 2.3 and 3.7 m/s, but the speeds recorded from a large number of experiments were equally distributed around 3 m/s; the average metabolic rate of flying Schistocerca was about 75 kcal/kg/h. This corresponded to an oxygen uptake of 16l. O2/kg/h. The values deduced for the first few minutes after the start were three times higher, and cruising rates twice as high were sometimes maintained for several hours. An average flight performance of 5 h at 3 m/s required twice as much energy as was contained in the constituent proteins of the wing muscles. Sustained flight therefore depends on large-scale transport of fuel from the stores to the muscles. The fat body delivered 85 to 90 % of the energy, and the remainder was mobilized from wing muscles, legs and wings. Since even the remote cells of the wings provided stores of fuel, the mobilization was of a general nature and the transport of fuel took place via the blood. Concerning migrating swarms the following was suggested: in the morning, milling and surging of groups of locusts before mass departure tends to empty the stores of glycogen; the proper migratory flight therefore takes place at the expense of fat and, under suitable climatic conditions, the endurance of flight is proportional to the amount of fat in storage before the start. Standard individuals with 10 % of fat (by fresh weight) should be able to fly continuously for about 12 h, 20 h being the upper limit (15 to 16 % of fat). The amount of vegetation daily consumed by a migrating swarm probably weighs as much, and possibly three times as much, as the weight of the swarm. Sufficient time and opportunity for feeding will therefore be essential for migrations. A large migrating swarm (say 15000 tons) was estimated to require as many calories per day as do 1.5 million men. The rate at which the wing muscles of locusts converted energy was between 400 and 800kcal/kg muscle/h; i.e. the same rates as found in hovering humming birds and flying Drosophila. Even for very intense muscular work, fat cannot therefore be regarded as inferior fuel in well-oxygenated muscles. An increasing amount of evidence from the literature favours the view that fat can be utilized directly. A possible cause for the lowered mechanical efficiency of man when fat is oxidized is the formation of ketone bodies parallel to the direct combustion of fat. On the other hand, initial mobilization seems to be slower for fat than for glycogen. When flight starts, this gives glycogen an advantage over fat, whereas the weight economy, and thus the endurance, is decisively improved by the ability to utilize stored fat; this will be further discussed elsewhere.