Phase Gregaria Research Articles

The determination of larval phase coloration in the African armyworm, Spodoptera exempta and its consequences for thermoregulation and protection from UV light

Abstract Spodoptera exempta exhibits a density‐dependent phase polyphenism in which caterpillars reared in isolation (phase solitaria) tend to be green/brown and cryptic while those reared in groups (phase gregaria) are black and highly visible. Differences in coloration between solitaria and gregaria phase larvae become apparent in the third instar and are pronounced by the final instar. Larval rearing densities as low as two larvae per 250 ml container are sufficient to induce gregaria coloration in 61% of the insects and at higher densities this is the only coloration expressed. Larvae transferred from isolated to crowded conditions or vice versa tend to retain or adopt gregaria phase coloration which suggests that this is highly advantageous. Black coloration is also induced in single larvae reared with other species of caterpillar (S. littoralis). Isolated larvae reared at low temperature tend to become melanic while crowded larvae reared at high temperature tend to be less melanised although they do not adopt the solitaria phase coloration. These results suggest that phase coloration is determined by non species‐specific inter‐larval contact, although it can be modulated by temperature. Under laboratory conditions, gregaria phase larvae heat up faster than solitaria; this is partially a consequence of their black coloration but their smaller size is a more important factor. The cuticles of the gregaria larvae absorb significantly more ultraviolet radiation than those of solitaria but this does not confer any protection when larvae are irradiated at 254 nm.

The response of predators to varying densities of Gregaria locust nymphs

The response to varying densities of prey was investigated by presenting predators (four human volunteers and a lizard, Lacerta lepida Daudin), in an arena, with from 5 to 120 fifth instar phase gregaria nymphs of the desert locust ( Schistocerca gregaria Forskål). The activity of the nymphs was also varied by varying the feeding and temperature conditions. Above a certain prey density (which differed between predators) human catching efficiency declined, while the lizard became totally incapable of catching any locusts. Efficiency of all predators was reduced by increasing activity of the prey.

Phase transformation and chiasma frequency variation in locusts. I. Schistocerca gregaria.

Locusts exhibit two basic forms or phases, one characteristic of swarming populations, termed phase gregaria, and the other characteristic of low density populations, termed phase solitaria. It has been claimed by Nolte that locusts living at low density, both in the field and in the laboratory, have a reduced chiasma frequency compared with animals living at high density. A postulated gregarisation pheromone is held to be responsible for the stimulation of melanin biosynthesis in the swarming animals and an unknown metabolite in this pathway causes the increase in chiasma frequency, as well as other phenotypic changes associated with phase transformation. According to Nolte this represents a means of releasing stored genetic variation necessary for adaptation in the areas invaded by swarms. — This claim has been re-examined in laboratory stocks of Schistocerca gregaria using a methodology comparable to that of Nolte. No reduction in the chiasma frequency of isolated animals was observed in any of the experiments. The isolated animals did, however, develop a phenotype characteristic of phase solitaria in terms of their pigmentation and morphometrics.

Learning and social aggregation in locust hoppers

1. 1. When locusts swarm, the hoppers (nymphs) live together in bands that depend on the individuals being attracted towards one another (phase gregaria, obtained in the laboratory by rearing hoppers together in crowds). They are then said to aggregate socially. This behaviour pattern can be measured in the laboratory in a cage that provides a physically uniform environment. In non-swarming periods, the scattered hoppers (phase solitaria, obtained in the laboratory by rearing hoppers in isolation) are not attracted towards one another when first confined together, If hoppers that have been reared in isolation are forcibly crowded together they learn to aggregate socially within a few hours. The types of stimuli between hoppers that are of importance during the process of learning to aggregate socially were studied in the two locust species Locust migratoria migratorioides (R. & F.) and Schistocerca gregaria (Forsk.). 2. 2. Single hoppers reared with a crowd of non-gregarious grasshoppers or woodlice (Isopods) aggregated socially when first placed together. 3. 3. By rearing single hoppers in transparent boxes placed in a cage full of other hoppers, direct tactile contact with other hoppers was eliminated, but visual, auditory and olfactory stimuli were received from the others. In such box-reared hoppers, social aggregation was increased a little in Locusta, but not at all in Schistocerca. 4. 4. Previously isolated hoppers showed increased grouping after being crowded with other hoppers for only seven hours. Crowding in the dark produced similar results to crowding in the light. Social aggregation was also increased in hoppers that were reared isolated but touched with fine wires for a seven-hour training period before being tested; they grouped almost as well as hoppers that had been crowded with other locusts. 5. 5. The behaviour patterns shown by crowded and by previously isolated hoppers when they first meet others are described. Both types of hopper examined objects, including other locusts, with the antennae and palps, but they differed in behaviour when they were themselves touched. Previously isolated hoppers moved away; crowded hoppers remained where they were and kicked with the hind legs or twirled the antennae. During the process of learning to aggregate socially, previously isolated hoppers appear first to become habituated to being touched. This is followed, after further contacts, by hind-leg kicking and antenna twirling, and these probably play a positive role in keeping the hoppers together in groups. The complete learning process can be brought about by touching isolated hoppers repeatedly with fine wires before they are put with other locusts. 6. 6. In contrast to locusts, grasshoppers do not aggregate socially even when reared in crowds. 7. 7. Records of colour changes were kept during the experiments. Phase gregaria hoppers are typically black and orange or yellow, whilst phase solitaria hoppers are mainly green or fawn. The various treatments suggested that phase gregaria colouring depended on a complex of stimuli between hoppers, through the auditory, visual, olfactory and tactile sense organs. 8. 8. On the whole, the two species of locust gave similar results. The process of learning to aggregate socially was a little more rapid in Schistocerca than in Locusta.

PHASE AND MOULTING POLYMORPHISM IN LOCUSTS

According to the Phase Theory formulated by Uvarov (1921, 1928), locusts exhibit a graduated type of densitydependent dimorphism. So marked is this dimorphism that the phases of most common locusts were once accorded specific rank. Phase polymorphism is characterized by two limiting forms linked by a whole range of intermediates; the form found in bands or swarms is known as phase gregaria, and the sedentary isolated form as phase solitaria: intermediate or transiens forms are designated by the terms congregans and dissocians, according to the direction of the phase-change. The ideas presented in this essay stem from different kinds of morphometric analysis of the locusts. First, the occurrence of an extra moult in some individuals is found to be part of a twin homeostatic growth-regulating process during ontogeny. The polymorphism that ensues is stochastically related to the density of the parental population. This density-dependent quality, though inherited, is not genically determined. Careful study of the wing-pads of the developing nymphs distinguishes insects whose innately determined phase status is not in equilibrium with the density of the larval population of which they are part. Congregans and dissocians nymphs form two separate categories of this transiens phase, illustrating at once the dynamic conception of phase polymorphism and the existence of hysteresis in cycles of densitydependent changes of shape in locusts. New methods for the quantitative study of form in locusts show that the generic differences between Red and Desert Locusts are independent of their phase polymorphism and of their normal growth. Finally, a necessarily speculative discussion of the role of polymorphism in the life-cycle of locusts is attempted.

PHASE TRANSFORMATION IN LOCUST BIOLOGY

SUMMARYUvarov's phase theory of locust plagues stated, first, that these insects were continuously variant physiologically and morphologically, in both sexes and at all stages, between two extreme types orphases: solitariawhich led a solitary sedentary life and was produced when the individuals were dispersed, andgregariawhich was highly gregarious and active and was produced when the population was dense; and, secondly, that this reversible process of phase transformation provided a sufficient explanation of the intermittency of plagues.The first point is generally accepted with some qualification. The second point has been the object of mounting criticism and is now generally rejected; this appears to be justified in so far as the previous emphasis on phase change meant neglect of the more fundamental question of changes in numbers. The connected claims that phase change is but a secondary concomitant of locust outbreaks, that the only relevant aspect of it is the behavioural change, and that even that change is merely quantitative, do not appear to be justified.The phase differences in post‐embryonic development, and in adult morphology and metabolism, suggest a greater influence of the corpus allatum (juvenile) hormone insolitariathan ingregariathroughout life, for which there is some direct evidence from implantation experiments. This provides the starting point for an hypothesis of the nature of phase variation: that phasesolitariais a more juvenile andgregariaa more adult type, in terms of morphology, physiology (including behaviour) and ecology.It is further suggested that the main difference between adults and juveniles, among terrestrial animals in general, is that adults find growth resources, while juveniles exploit them. The adult has more elaborate sensor i‐motor equipment and spends accumulated resources in more activity, while the juvenile is more vegetative. On this view, finding the appropriate mate and oviposition site are strictly adult functions, but the development of the sexual products is a functional reversion toward juvenility. Thus there is evidence that phasegregarialocusts are more adult and less vegetative thansolitaria, not only behaviourally and morphologically but also in their lesser fecundity and longevity.Change of phase towardgregariais brought about by mutual nervous stimulation. Visual, mechanical and chemical stimuli all contribute among fully gregarized individuals, but their relative importance during the process of gre‐garization is in doubt. The nature of the central nervous process in gregarization is also in doubt; conditioned reflex formation has been suggested. The result of it is to accentuate adult characters as defined, including locomotor activity, and strikingly to concert not only locomotor responses but also other processes such as pigmentation, sexual maturation, mating and oviposition, among the individual insects.Inheritance of the effects of mutual stimulation has been demonstrated in both physiological and morphological characters; the egg stage being no barrier but rather a key point of divergence. Within one generation the effects are considerable but limited, and more than one generation is needed to complete gregarization.The two phase extremes differ only quantitatively in respect of the isolated components of their behaviour such as the tendency of hoppers to march or of adults to embark on long migratory flights. But these responses are weak insolitariaand usually overridden by opposing ones to extraneous stimuli, while they dominate the behaviour ofgregaria.Thus the resultant behaviour patterns of the two differ qualitatively.Water is a limiting and variable factor in the ecology of locusts, and their habitats are patchy and ephemeral. The two phases of one species may exhibit similar seasonal cycles of geographical redistribution, travelling on the wind between adjacent regions offering complementary wet and dry seasons. Within one such region thesolitariahabitat offers the most favourable conditions for multiplication within a small compass. Thesolitariamode of life is well adapted to exploit this, as thegregariais not.Given sufficient multiplication within thesolitariahabitat, the return of unfavourable conditions can entrain mutual stimulation and gregarization to the point of swarming out into the largergregariahabitat. There multiplication cannot proceed at the high rates possible inside thesolitariahabitat, but the active, opportunistic mode of life of thegregarialocusts in swarms appears to be well adapted to their habitat, since they can maintain themselves even in regions where thesolitariahabitat does not occur at all. Eventually the swarms dwindle and disperse, but individuals from them revert to phasesolitariaand re‐colonize its habitat.The outstanding peculiarity of locusts, it is concluded, is that they veer between two forms, two modes of life and two habitats, in response to the vagaries of their environment. The intermittent plagues cannot be explained by that fact alone but neither can they be explained without it.

A new biometrical phase character in locusts.

THE solitary and the swarming phases of the same species of locusts can be distinguished by coloration and by biometrical characters1. Among the latter, the ratio E/F of the elytron length (E) to the posterior femur length (F) has been generally used2, but no proper statistical investigation of the relative merits of various measurements and ratios exists. Careful measurements of all suitable parts of the body have now been undertaken on samples of the desert locust, Schistocerca gregaria (Forsk.), taken from wild populations of a very low density (phase solitaria), and from swarms (phase gregaria), and the data analysed statistically. None of the twenty direct measurements of body parts proved to be suitable, as the frequency distribution polygons for the two phases overlapped widely. The E/F ratios also showed an overlap which made its use uncertain. Moreover, a comparison of E values in the two extreme phases showed that the elytron-length varied, according to the phase, in an opposite direction in the two sexes, thus:

Presence of Reddish Pigment in Eggs and Ovarioles of the Desert Locust, and its Probable Phase Significance

I NOTICED some time ago that in the desert locust, Schistocerca gregaria (Forskal), several eggs had a reddish tinge owing to the presence of pink pigment superficially on the egg-chorion, while others lacked this pigment. Generally, in an egg-pod all the eggs are either pink or non-pink, though exceptionally both kinds may occur in the same pod. Hatchings from some 185 pink eggs (from five different egg-pods) and 406 non-pink eggs (from ten different pods) gave the following kinds of first-stage hoppers: (a) Pink eggs: 54 per cent gregaria (black pattern), 22 per cent intermediate and 24 per cent solitaria (green); (b) non-pink eggs: 25 per cent, 17 per cent and 58 per cent respectively. These proportions suggest that pink eggs produced a majority of phase gregaria hoppers, though it must be mentioned that hatchings from five pods (172 eggs) were contrary to this suggestion.

Problems of Growth of the African Migratory Locust

General Growth.Generally, females have higher rates of growth than males. The phases, however, do not show appreciable differences in the rate. The pronotum has for increase in length the highest values which decrease throughout the instars (whereas the constants for the other parts remain fairly stable up to the fifth instar).Dyar's rule was applied for the growth in length of the middle femur and the width of the head, and it was found that the rule holds good for these parts.Przibram's rule, as modified by Bodenheimer, holds true for the growth in length of the different parts and shows the occurrence of latent cell-divisions varying from one (width of head and of pronotum) to four (length of pronotum). The number of latent cell-divisions keeps fairly constant in both phases.For wet weight Przibram's principle is inapplicable, owing to the large percentage of differences between the actual and calculated values.Gregarious males are heavier than solitary males up to the third stadium ; gregarious females are heavier than solitary females up to the third stadium ; fourth, fifth and adult stadia being characterized by higher values in wet weight for solitary females than for gregarious females. Females have higher rates of increase in wet weight than males. No significant differences exist in the rates of increase between gregarious and solitary individuals. In the fifth-adult stadium all the rates decrease except in gregarious females, which show a rise.Gregarious insects have higher values in dry weight than solitary insects, except solitary females in the adult stadium. The coefficients are higher for females than for males.The rates of increase reach the highest values in the second-third stadium of gregarious insects and solitary females, whereas solitary males have their highest value in the fourth-fifth stadium.With the exception of solitary females, all the rates of growth in dry weight decline in the fifth-adult stadium.The rates of growth of the hind legs obtained from the cube-roots of their wet weights are compared with the rates of linear growth of the hind femora. Their variation throughout the instars seems to be in opposite directions. Therefore it is suggested that the rates of growth in wet weight of the hind legs and the rates of growth in length of the respective hind femora are independent of each other.Growth of the parts.The application of the exponential allometry formula y=bxα to the data on dimensions of the parts of Locusta shows the existence of negative, positive and almost isometric growth.The pronotum has the highest value for the growth in length relatively to the growth in length of the middle femur ; the lowest value pertains to the growth in width of the head.Males have higher values than females ; phase gregaria exhibits higher growth-ratios than phase solitaria.With the exception of the hind femur the growth-ratios decline throughout the instars. The greatest decline pertains to the growth in length of the pronotum.A growth-gradient exists in Locusta with the highest value in the pronotum. The middle femur divides the growth-gradient into two parts : an anterior part with values decreasing with the growth of the insect, and a posterior part whose values increase with its growth.Effects of the amputation of the hind tibiae on crowded locusts.The effects obtained by mutilating both hind tibiae of three hundred first instar hoppers of Locusta migratoria migratorioides and placing them in a crowded condition are compared with the effects obtained by crowding a batch of the same number of first instar unoperated insects.The insects with their hind tibiae cut off did not develop as far as those of the control batch ; the differences in dimensions are greater for the hind femur than for the other parts of the body.In the experimental batch the hind femur, as a consequence of its useless condition, became extremely short as compared with the elytra, bringing the ratio E/F to a high value (over 1·950), thus leading to a false interpretation.The occurrence of the black-orange coloration in both batches suggested that both developed towards phase gregaria. This coloration was stronger and more uniform in the control batch than it was in the experimental batch. Thus the control animals developed into a better gregarious type.

On the Ecology of Acrididae near Lake Chad

1. The shore of Lake Chad was suspected of being a reservation of both the Migratory Locust and the Red Lcoust. In 1931 a preliminary survey of the shore was made, as a result of which it was tentatively concluded that about one-half or less of the shore of British Chad may offer conditions suitable for the production of swarms of the Migratory Locust from the solitary phase. The Red Locust was present only in the southern half of the shore. A village named Kalkala, at the south-western corner of the Lake, was selected as the most suitable locality in which to carry out ecological research.2. The ecology of the two species of locusts and of about 60 other species of ACRIDIDAE was studied at Kalkala during the first six months of 1933. A description is given of agricultural and climatic conditions in the Kalkala area and some notes on the hydrography of Lake Chad are included. The vegetation, soils, fauna and microclimates of the habitats frequented by ACRIDIDAE are described.3. Collections of Acrididae were made each month in all the principal habitats. It was found that the Acridinae occurred principally in the wettest habitats and that this subfamily exhibited a small degree of ecological plasticity. The Oedipodinae consisted chiefly of geophilous species which were most abundant on bare soil in farm-land. The Pyrgomorphinae were most abundant in two non-gramineous habitats, but were not uncommon in Cynodon dactylon; one species was associated with Calotropis procera. The Catantopinae showed a greater degree of ecological plasticity than did any of the other subfamilies; the majority of the species encountered were most abundant in the drier habitats.4. Bionomical notes are given for the majority of the species of Acrididae met with in 1931 and 1933 in the Chad area. Evidence was obtained that many species of Catantopinae have a prolonged imaginal diapause. Certain species of Acridinae and Catantopinae are characterised by an embryonic diapause during the hottest months of the year, and one species of Pyrgomorphinae has a nymphal diapause during the early part of the dry season.5. The Red Locust frequents tall grass habitats from November to the end of April, the adults then gradually move to short grass and farm-land and begin to breed in late June. The imaginal diapause lasts from early October to late July. Biometrical examinations of adults and other data indicate that the Red Locust is in phase transiens (congregans). There is no evidence that swarms have left the Chad area. It seems probable that conditions in this area are unsuitable for the production of phase gregaria.6. The solitary phase of the Migratory Locust was present in the survey area throughout the six months; it was never numerous and decreased steadily in numbers from January to June in spite of the fact that it was breeding from late February to June. The decrease in numbers is thought to have been due, chiefly, to the attacks of the Carmine Bee-eater and to bush fires.Phase transiens (dissocians) was found until mid-March; there is no doubt that most of the locusts present were derived from the survivors of hopper bands which had been baited or trenched in the autumn of 1932. Swarms arrived in late May and early June and repopulated the area. The principal habitats of the Migratory Locust were Cynodon dactylon, Brachiaria ramosa and Chloris gayana. The scarcity of this species in the southern half of Chad indicated that this area is unlikely to be a reservation; but research over a number of years is necessary to confirm this opinion.

The Phases of the Rocky Mountain Locust Melanoplus Mexicanus (Saussure)

Dr. Faure has shown experimentally (1932) that the brown locust, Locustana pardalina, of South Africa exists under two phases, the solitary phase and the swarm phase. Each of the individuals of the solitary phase, which live in isolation like most common grasshoppers, is a representative form of the phase solitari-r. Each of the individuals of the swarm phase, which come together in great dense swarms and then migrate over the country, is a representative of the phase gregari-r. The nymphs of the phase gregaria differ markedly from the nymphs of the phase solitaria in coloration, while the adults of gregaria differ in several morphological characters from the adults of the phase solitaria. Dr. Faure, by means of an ingenious series of experiments, has been able to transform the progeny of the solitaria phase into the phase gregaria. There is, therefore, now no doubt of the fact that the transformation of this grasshopper from one phase into the other phase occurs in nature when the conditions are present to bring it about. It has been suggested recently by several authors that our Rocky Mountain locust Melan-oPlus spretus, now apparently extinct, was the long winged migratory (gregaria) phase of our common grasshopper Melan-oplus (atlanis) mexican-us. Dr. Faure conceived the idea of attempting, by his experimental methods used so successfully with the brown locust of South Africa, to transform M. mexican-us which he surmised to be the solitaria phase into M. spretus, the phase gregaria. The following paper embodies the results of Dr. Faure's observations on M. mexican-us in rearing experiments carried out at Saint Paul, Minnesota, during l\'lay, June, and July 1932.