SEARCH

SEARCH BY CITATION

Keywords:

  • Desert locust;
  • maternal effect;
  • phase change;
  • phenotypic plasticity;
  • population density;
  • Schistocerca gregaria

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Abstract. Phase characteristics of locusts from parents that experienced different population densities were investigated under field conditions in Morocco. The density experienced by adults induced a marked phase change in colour, behaviour and morphometry of their offspring. A high-density subpopulation gave rise to a preponderance of black hatchlings that exhibited a high level of aggregation as later stage nymphs and showed gregarious morphometric features as adults, whereas a low-density subpopulation produced a majority of green hatchlings with a lesser tendency to group as final-instar nymphs and more solitarious morphometry as adults. The constrained isolation of insects from the low-density subpopulation, or crowding of insects from the high-density subpopulation, resulted in a behavioural and morphometric change towards even more solitarious characteristics in the former and more pronounced gregarious characteristics in the latter, relative to field-caught insects of the same age. These results from the field are consistent with those in the laboratory and provide more evidence for the dual roles of an individual locust's experience of crowding as well as that of its parents in density-dependent phase change.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The outstanding characteristic of all locust species is their ability to exhibit density-dependent phase polymorphism, involving graded changes in a suite of characters, including behaviour, colour, reproduction, development, morphometry and endocrine physiology (Dale & Tobe, 1990; Pener, 1991). These form a continuum between two extreme phases, solitaria and gregaria (Uvarov, 1966). At low densities, individuals are generally scattered, cryptically coloured, relatively inactive and avoid one another except to mate. At high densities, however, they become brightly coloured and actively aggregate forming cohesive, persistent, gregariously behaving units, i.e. bands of nymphs and swarms of adults (Roffey & Popov, 1968).

The basis of swarm formation is the behavioural change in individual locusts that takes place within a matter of hours as a result of crowding (Roessingh & Simpson, 1994; Bouaïchi et al., 1995; Roessingh et al., 1998; Simpson et al., 1999). This change in behaviour is stimulated principally by physical contact (Roessingh et al., 1998; Hägele & Simpson, 2000; Simpson et al., 2001) and is auto-catalytic. As individuals become crowded, gregarization occurs, which causes locusts to aggregate actively, which further stimulates gregarization. This can ultimately result in the generation of very large groups. Likewise, when previously aggregated individuals become separated, they begin to solitarize, reducing their tendency to aggregate, and so promoting further solitarization. These positive feedback mechanisms have the effect of driving the phase change to either of the two extreme forms, with associated changes in colour, morphometry and physiology (Uvarov, 1977; Pener, 1991).

One of the most important features of continuous phase change in locusts is the fact that the offspring exhibit some of the phase characteristics of their mother, and hence phase change is a cumulative process that crosses from one generation to the next (Faure, 1932; Albrecht, 1955, 1959; Papillon, 1960; Uvarov, 1966). Several studies have illustrated a carry-over from one generation to the next of phase characteristics such as colour, morphometry, weight and ovariole number (Gunn & Hunter-Jones, 1952; Hunter-Jones, 1958; Albrecht, 1959; Papillon, 1970), and recently the phenomenon and mechanisms of trans-generational transfer of behavioural phase state have been elucidated (Islam et al., 1994a, b; Bouaïchi et al., 1995; McCaffery et al., 1998; Simpson et al., 1999; Hägele et al., 2000).

While a great deal is now known about behavioural phase change in the laboratory, manipulative field studies are relatively few (e.g. Kennedy, 1939; Ellis & Ashall, 1957; Roffey & Popov, 1968; Bouaïchi et al., 1996; Despland & Simpson, 2000a; Sword et al., 2000). The present paper reports results from a field study in Morocco to explore aspects of the accumulation of phase characteristics in a natural desert locust population. Other data from the same study appeared in Bouaïchi et al. (1996). Two subpopulations were studied, both of which are thought to have originated from the same immigrant population. The low-density subpopulation was found in an area of contracted native vegetation, while the high-density subpopulation occurred in a nearby area of cultivation. The initial stage of the study involved assessing the density and distribution of adults, egg pods and nymphs in these two areas. Next, hatchlings were collected from both field sites and their colour assayed as they emerged in situ from egg pods, to discover whether differences occurred between the subpopulations in relation to the local density of adults and/or the density of egg pods in the area immediately surrounding the pod from which hatchlings emerged. Nymphs were then reared in mesh cages, either in denser crowds than occurred in the field (high-density subpopulation insects) or alone (low-density subpopulation nymphs). The tendency of these insects to aggregate was measured at the final nymphal stadium as an indicator of behavioural phase state, and morphometric ratios were recorded as adults. The behaviour and morphometry of these insects was compared with those of similarly aged insects collected from the field, to establish whether rearing in cages at higher (high-density subpopulation) or lower (low-density subpopulation) densities than in the field caused an enhancement of the difference in phase between insects from the two subpopulations.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Study area

Field studies were carried out in Morocco, Ziz Valley, Tafilalet district, on the south-east side of one sand dune: Erg Chabbi (31°03′N, 03°56′W). According to climate and vegetation classification, Tafilalet is considered as an arid zone. The vegetation is described as ‘contracted vegetation’ (Bouaïchi, 1996), where agricultural plant growth (mainly barley and wheat) is limited to wadis (dry river beds) and depressions that channel rainfall. Native annual species such as Pulicaria crispa (Compositae), Emex spinosa (Polygonaceae), Hyoscyamus muticus (Solanaceae) and Lotus glinoides (Leguminosae) provide partial cover, interspersed with shrubs, including Panicum turgidum, Aristida pungens and A. plumosa (all Poaceae), and Tamarix articulata (Tamaricaceae). As the vegetation persists much longer in the depressions than elsewhere during summer, it provides an ideal habitat for desert locusts and has long been known as home to a solitarious population. The valley has experienced many locust outbreaks and supports locust breeding during plague periods. Gregarization only rarely occurs, and seems to be dependent upon the influx of large numbers of individuals from the winter breeding ground. For instance, in 1995, exceptional immigration into the local population led to gregarization and the beginning of swarm formation (Bouaïchi, 1996; personal observation).

Locusts

Hoppers tested in the present experiments were the offspring of a partially swarming population of adults originating from the winter breeding that occurred in the north-east of Mauritania in 1994. The morphometric ratios of their parents fell in the solitarious range according to Dirsh (1953). The colour of the first- and fifth-instar nymphs (i.e. green and/or brown) also indicated at least partial solitarization. This population will be referred to as the low-density subpopulation. Some 200 locusts from this subpopulation were reared in isolation from the egg stage under semifield conditions in 20-cm-long × 20-cm-wide × 20-cm-high cages.

On the other side of the sand dune, particularly in wheat and barley crops, mature adults of nearly the same morphometric measurements as the parents of the low-density subpopulation nymphs were seen at a high density during oviposition (12 per m2). Their offspring exhibited gregarious behaviour, such as marching in bands, and were bright yellow with black patterning. Some 800 such second-instar nymphs were captured, kept in four cages (2 m long × 2 m wide × 0.8 m high) and provided daily with fresh Lotus and Emex. This population will be referred to as the high-density subpopulation.

Population assessments

In order to estimate the population size of adults in the field, a series of 25 transects of 10 m length and 1 m width were sampled in an area of cereal cultivation and also in an area of short grass which accommodated, respectively, the high- and low-density subpopulations. An observer counted the number of locusts flushed out as he walked a transect. Quadrat counting was used to sample egg-pod density. A preliminary survey was made to determine the presence of egg-pods in both locations. A total of 25 sample areas, each of 1 m2, was examined by digging over the topmost 2–5 cm of soil to expose the tips of the froth tubes. The nearest neighbour method was used to assess the spatial distribution of egg-pods for subsequent correlation with offspring colour. Quadrat counting of 1 m2 was used to sample nymphal populations on 25 occasions at both sites. Samplings were all performed in a central area across a small drainage channel in the cereal cultivation land and across a wadi in the short grass site.

Morphometrics

Morphometric analysis provides additional evidence of the progressive change in phase during upsurge breeding sequences. The morphometric elements used in the study, as described by Dirsh (1953), are those most commonly measured for desert locusts, namely elytron length (E), length of posterior femur (F) and maximum width of head (C). The F/C ratio is generally regarded as the most diagnostic indicator for differentiating between solitariform and gregariform phases (Dirsh, 1951, 1953). Males and females have been treated separately since they differ in shape. Morphometric characters were measured for adults taken from each of the following groups: (i) low-density subpopulation parents (37 females and 57 males); (ii) adult offspring from low-density subpopulation parents kept in isolation from the day of hatching (82 females and 50 males); (iii) field-caught adult offspring from low-density subpopulation parents (104 females and 50 males); (iv) high-density subpopulation parents (114 females and 98 males); (v) adult offspring from high-density subpopulation parents, maintained in a crowd since the second stadium in cages (63 females and 47 males); (vi) field-caught adult offspring from high-density subpopulation parents (96 females and 123 males); and (vii) adults taken from swarming immigrant populations (56 females and 36 males) in the highland boundary between Morocco and Algeria.

Hatchling colour

The colour scores used were based on the ground colour, and the extent and intensity of dark patterns (Islam et al., 1994a). These were as follows: 1, ground colour uniformly green with no black pattern; 2, ground colour green with some black markings but not more than 30% of the body surface; 3, ground colour green or olive but with extensive black markings, ranging from 30 to 60% of the body surface, with prominent femoral melanin stripes; 4, pale ground colour almost obscured by black markings ranging from 60 to 80% of the body surface; 5, ground colour entirely obscured by heavy black markings on more than 80% of the body surface.

The distance that separated each egg-pod from its nearest neighbour was measured. Egg-pods less than 1 m apart were scored in five categories of 20-cm intervals, while pods situated over 1 m distance apart were combined into a single category for subsequent analysis. Egg-pods were covered with 10-cm-high × 2-cm-diameter plastic tubes with minimal disturbance to the surrounding soil and were provided with an expanded metal perch for the hatchlings to climb. After hatching was completed the offspring were chilled for 1 h, to slow them down, and their colour scores were then recorded. Colour scores of a total of 6076 hatchlings from 96 egg-pods laid by high-density subpopulation females in cereal cultivation areas and 3065 hatchlings from 41 egg-pods laid by low-density subpopulation females in the short grass site were recorded on the day of emergence.

Extent of grouping

Observation arenas were created on bare, level ground using 30-cm-high galvanized metal as a perimeter fence. Four such arenas were constructed and used simultaneously, with field assistants providing extra observations. An approximate measure of the tendency of insects to aggregate (a key feature of behavioural gregarization) is provided by the number of insects within a body length of each individual. This was recorded for each locust in the group of 10 at 5-min intervals throughout the 4-h treatment period. The mean value for the group, termed the ‘Association Index’ (AI), was then calculated and used as an estimate of the collective crowding demonstrated under the experimental conditions. This is similar to the ‘Grouping Index’ used by Heifetz et al. (1994) and is defined mathematically as:

  • image

where Ni is the number of other locusts within one body length of locust i and n is the total number of insects in the assay (see also Bouaïchi et al., 1996).

Statistical procedures

In these experiments several hatchlings from a single egg-pod were tested, and therefore main effects and interaction terms were tested against the effect of egg-pod, i.e. F ratios were derived by using the mean sum of squares for egg-pods as a denominator and the effect of egg-pod was tested against the residual (see Brown & Melamed, 1990).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Density and distribution

The immigrating swarm which settled in the cultivated land was estimated to be at least 0.6 km2 in area and was of medium density (11.8 ± 0.98 locusts per m2). As a result of the transects it became apparent that ovipositing adults were concentrated in and around the larger drainage channel systems. The data show that the density of adults was consistently higher in those areas where the vegetation cover was less dense and the soil moisture higher than in other squares. The majority of these adults were bright yellow and were fully mature. Dissection of a sample of females for examination of the ovaries showed that some of them had laying marks at the bottom of their ovarioles, which indicates that they had previously laid their first eggs elsewhere. The surveys indicated that the density of eggs deposited by this subpopulation was 6.1 ± 0.68 pods per m2 over the sampling area (0.02 km2). From these pods emerged small and moderately dense hoppers bands (25 nymphs per m2).

On the other study area, the short grass site, the immigrant population of ovipositing adults was scattered, reaching a density of 1.2 ± 0.04 locusts per m2 over 0.2 km2. Owing to emigration and ageing, the number of adults was apparently declining. A total of 20 egg-pods were found in 25, 1-m2 quadrats over a sampling area of 0.02 km2, which illustrated the rarity of egg-pods in comparison with the high-density subpopulation. The egg-pod density (0.8 ± 0.21 pods per m2) and also the high proportion of eggs which failed to hatch due to soil desiccation led to a very low density of nymphs (1 final-instar nymph per m2).

A Kolmogorov–Smirnov two-sample test based on the cumulative distribution of insects per sampling area showed that the frequency of adults as well as egg-pods and nymphs differed significantly between the subpopulations (P < 0.001 in each case), which in turn differed significantly from the expected normal distribution.

Morphometry

The F/C ratio was examined in adults from both subpopulations and their offspring maintained under either isolated or crowded conditions. The distribution of F/C ratio of both sexes of adults from the two subpopulations falls clearly within the solitarious range according to Dirsh (1953) (Fig. 1a,b). The F/C ratios of females bred from these adults, either in the wild or under crowded conditions in cages, was significantly lower (i.e. more gregarious) than those of their parents and than those of the low-density subpopulation (P < 0.001, multiple post hoc comparison using Student–Newman–Keuls test) (Fig. 1a). Maintaining males reared from high-density subpopulation parents under crowded conditions in cages resulted in lower morphometric indices than exhibited by similarly aged offspring in the wild (P < 0.001). The opposite effect was found when such males were reared under isolated conditions (Fig. 1b).

image

Figure 1. Frequency distribution of values for the morphometric ratio F (length of hind-femur) to C (maximum width of head) of (a) females and (b) males caught from low- and high-density field populations or reared in a crowd or in isolation under field conditions.

Download figure to PowerPoint

Hatchlings colour

A two-way analysis of variance was used to test the effect of parental origin and egg-pod density on hatchling colour. The coloration of the hatchling within an egg-pod was much less variable than between pods, thus making egg-pod a significant variable (P < 0.001). Results indicated a relationship between the density experienced by parents as adults and the median colour score of their offspring within the egg-pod (F1,124 = 4.71, P = 0.032) (Fig. 2). The high-density subpopulation produced hatchlings with dark pigmentation, whereas the low-density subpopulation produced green hatchlings. Egg-pod density was found not to influence the colour of the newly emerged nymphs (F5,124 = 1.06, P = 0.387), nor was the interaction between parental and the egg-pod density significant (F5,124 = 1.25, P = 0.292).

image

Figure 2. Frequency histograms of values for the colour score of individual hatchlings from low- and high-density field subpopulations.

Download figure to PowerPoint

Grouping behaviour

The mean values for ‘grouping index’ at 5-min intervals across the 2-h treatment period, and the cumulative ‘grouping index’ across the entire 2-h treatment, are presented in Fig. 3. Results from an analysis of variance, using 5-min means for ‘grouping index’ as the dependent variable, rearing conditions of low and high subpopulation densities as treatments and time throughout the 2-h treatment as a repeated measure, showed a significant main effect of subpopulation density on the behaviour of final-instar nymphs (F3,28 = 2.98, P = 0.048). Nymphs from low-density subpopulation parents and reared in isolation or bred under field conditions at low-density aggregated significantly less than did nymphs from high-density subpopulation adults. Grouping activity of nymphs from high-density subpopulation parents was higher when nymphs were maintained in cages under crowded conditions than when bred in the wild (P = 0.002, Multiple post hoc comparison using Student–Newman–Keuls test).

image

Figure 3. Mean (± SE) cumulative values for ‘grouping index’ across the entire 2-h test period for nymphs from low-density subpopulation parents, either reared in isolation or bred under field conditions, and nymphs from the high-density population reared in a crowd or caught from the high-density field subpopulation.

Download figure to PowerPoint

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Based on local knowledge and regular surveys by operatives from Centre National de Lutte Antiacridienne, Morocco, it is thought that the locusts in our study probably originated from a single immigrant population, with adults from the low-density subpopulation being remnants of insects which had settled in the cultivated area.

The results from our field study are fully consistent with what is known of the mechanisms and processes controlling aspects of phase change, in particular reinforcing the fact that changes in colour, behaviour and morphometry are influenced both by an individual's experience of crowding, as well as that of its parents (e.g. Islam et al., 1994a,b; Bouaïchi et al., 1995).

Hatchlings produced by high-density subpopulation parents were dark in colour, and later-instar nymphs, either kept in a crowd or bred under the same conditions as their parents, showed a greater tendency to form groups than did the nymphs from low-density parents. Hatchlings from parents from the low-density subpopulation were lighter in colour and, as final-instar nymphs, avoided each other and grouped less frequently. The constrained isolation of insects from the low-density subpopulation, or crowding in cages of insects from the high-density subpopulation, resulted in a morphometric change towards solitarious characteristics in the former and gregarious characteristics in the latter. Over-crowding insects from the high-density subpopulation in a cage, rather than leaving them to breed in the field, had a marked effect on their behaviour as final-instar nymphs, and also on their morphometry as adults. The opposite trend was found, but to lesser degree, when locusts from the low-density subpopulation were kept in individual cages.

One aspect of our results is of interest in the context of the mechanisms of maternal transfer of phase state. We found that the colour of the hatchlings from the different subpopulations was not influenced by the density of egg pods in the area immediately surrounding where they emerged, as represented in statistical analyses as the distance to the next nearest egg pod. The implication is that it was the degree of crowding experienced by adult females, either at the time of oviposition or sometime earlier, which influenced hatchling state, rather than interpod interactions (mediated, for example, by volatile chemicals). Adult females have a ‘memory’ of how recently they have been crowded, with the degree to which their offspring emerge behaviourally gregarized being a function of how recently the mother was crowded before oviposition (Bouaïchi et al., 1995). It has been reported previously from laboratory studies that the density of egg pods during incubation has less influence on gregarization of developing hatchlings than does female crowding (McCaffery et al., 1998). The accessory glands are involved in the production of maternally produced compounds that are released with the egg foam in response to crowding and result in gregarization of developing hatchlings (Hägele et al., 2000). This gregarizing agent is water soluble (hexane and acetone extracts of foam lack any activity, while there is partial activity in ethanol extracts and high activity in aqueous extracts), and is only effective if added to solitarious eggs (or washed from gregarious eggs) within hours of laying (McCaffery et al., 1998). These characteristics and recent HPLC, NMR and MS analyses (unpublished) are not consistent with the recent suggestion that C8-ketones are the gregarizing agent (Malual et al., 2001).

In a recent study carried out in Mauritania, Despland & Simpson (2000a) manipulated the small-scale pattern of vegetation in field arenas and found that small populations of solitarious adult locusts housed in the arenas subsequently produced hatchlings whose behavioural phase state reflected the degree of clumping of food plants. It had been previously shown in laboratory and field experiments (Bouaïchi et al., 1996; Despland & Simpson, 2000b; Despland et al., 2000) and through individual-based modelling (Collett et al., 1998) that the small-scale distribution of food plants is a critical factor in determining the behavioural phase state of individuals and local populations of desert locusts. The Mauritania experiment (Despland & Simpson, 2000a) showed that this effect can in turn be transmitted to the next generation. Our present data support that conclusion. The low-density subpopulation existed in an area of sparse but more or less uniformly distributed food and shelter plants, which would be expected to prevent group formation. In contrast, the high-density subpopulation was concentrated in an area of cereal cultivation, promoting crowding and thus gregarization of hatchlings.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

A. Bouaïchi was supported by grants from the United Nation Development Programme and funding for field work research was provided by the International Fund for Agriculture Development, Rome, to whom we are very grateful. Special thanks go to the Moroccan government for granting A.B. study leave and for logistical support in carrying out field work in Morocco. We are grateful to M. L. Idrissi Raji from the National Centre of Locust Control, Morocco, for his invaluable assistance with the field work.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  • Albrecht, F.O. (1955) La densité des populations et la croissance chez Schistocerca gregaria (Forsk.) et Nomadacris septemfasciata (Serv.); la mue d'ajustement. Journal d'Agriculture Tropicale et Botanique Appliquées, 2, 109192.
  • Albrecht, F.O. (1959) Facteurs internes et fluctuations des effectifs chez Nomadacris septemfasciata (Serv.). Bulletin de Biologie Franco-Belge, 93, 414461.
  • Bouaïchi, A. (1996) The behavioural and environmental bases of gregarization in the adult desert locust Schistocerca gregaria (Forskål).PhD Thesis, University of Oxford, 177 pages.
  • Bouaïchi, A., Roessingh, P. & Simpson, S.J. (1995) An analysis of the behavioural effects of crowding and re-isolation on solitary-reared adult desert locusts (Schistocerca gregaria) and their offspring. Physiological Entomology, 20, 199208.
  • Bouaïchi, A., Simpson, S.J. & Roessingh, P. (1996) The influence of environmental microstructure on the behavioural phase state and distribution of the desert locust Schistocerca gregaria. Physiological Entomology, 21, 247256.
  • Brown, S.R. & Melamed, L.E. (1990) Experimental Design and Analysis. Quantitative Applied Social Sciences, 74, 6164.
  • Collett, M., Despland, E., Simpson, S.J. & Krakauer, D.C. (1998) Spatial scales of desert locust gregarization. Proceedings of the National Academy of Sciences, USA, 95, 1305213055.
  • Dale, J.F. & Tobe, S.S. (1990) The endocrine basis of locust phase polymorphism. Biology of Grasshoppers (ed. by R. F.Chapman & A.Joern), pp. 393414. John Wiley & Sons, New York.
  • Despland, E., Collett, M. & Simpson, S.J. (2000) Small-scale processes in desert locust swarm formation: how vegetation patterns influence gregarization. Oikos, 88, 652662.
  • Despland, E. & Simpson, S.J. (2000a) Small-scale vegetation patterns in the parental environment influence the phase state of hatchlings of the desert locust. Physiological Entomology, 25, 7481.
  • Despland, E. & Simpson, S.J. (2000b) The role of food distribution and nutritional quality in behavioural phase change in the desert locust. Animal Behaviour, 59, 643652.
  • Dirsh, V.M. (1951) A new biometrical phase character in locusts. Nature, 167, 281282.
  • Dirsh, V.M. (1953) Morphometrical studies on phases of the desert locust (Schistocerca gregaria, Forskål). Anti-Locust Bulletin, 16, 134.
  • Ellis, P.E. & Ashall, C. (1957) Field studies on diurnal behaviour, movements and aggregation in the desert locust (Schistocerca gregaria Forskål). Anti-Locust Bulletin, 25, 194.
  • Faure, J.C. (1932) The phase of locusts in South Africa. Bulletin of Entomological Research, 23, 293424.
  • Gunn, D.L. & Hunter-Jones, P. (1952) Laboratory experiments on phase differences in locusts. Anti-Locust Bulletin, 12, 129.
  • Hägele, F.H., Oag, V., Bouaïchi, A., McCaffery, A.R. & Simpson, S.J. (2000) The role of female accessory glands in maternal inheritance of phase in the desert locust Schistocerca gregaria. Journal of Insect Physiology, 46, 275280.
  • Hägele, F.H. & Simpson, S.J. (2000) The influence of mechanical, visual and contact chemical stimulation on the behavioural phase state of solitarious desert locust (Schistocerca gregaria). Journal of Insect Physiology, 46, 12951301.
  • Heifetz, Y., Applebaum, S.W. & Popov, G.B. (1994) Phase characteristics of the Israeli population of the migratory locust, Locusta migratoria (L.) (Orthoptera: Acrididae). Journal of Orthoptera Research, 2, 1520.
  • Hunter-Jones, P. (1958) Laboratory studies on the inheritance of phase characters in locusts. Anti-Locust Bulletin, 29, 132.
  • Islam, M.S., Roessingh, P., Simpson, S.J. & McCaffery, A.R. (1994a) Parental effects on the behaviour and colouration of nymphs of the desert locust Schistocerca gregaria. Journal of Insect Physiology, 40, 173181.
  • Islam, M.S., Roessingh, P., Simpson, S.J. & McCaffery, A.R. (1994b) Effects of population density experienced by parents during mating and oviposition on the phase of hatchling desert locusts, Schistocerca gregaria. Proceedings of the Royal Society, London, (B), 257, 9398.
  • Kennedy, J.S. (1939) The behaviour of the Desert Locust (Schistocerca gregaria, Forsk.) (Orthopt.) in an outbreak centre. Transactions of the Royal Entomological Society, London, 89, 385542.
  • Malual, A.G., Hassanali, A., Torto, B., Assad, Y.O.H. & Njagi, P.G.N. (2001) The nature of the gregarizing signal responsible for maternal transfer of phase to the offspring in the desert locust Schistocerca gregaria. Journal of Chemical Ecology, 27, 14231436.
  • McCaffery, A.R., Simpson, S.J., Islam, M.S. & Roessingh, P. (1998) A gregarizing factor present in the egg pod foam of the desert locust, Schistocerca gregaria. Journal of Experimental Biology, 201, 347363.
  • Papillon, M. (1960) Etude préliminaire de la répercussion du groupement des parents sur les larves nouveau-nées de Schistocerca gregaria Forsk. Bulletin Biologique, 93, 203263.
  • Papillon, M. (1970) Influence du groupement des adultes sur leur fécondité et sur le polymorphisme de leur descendance chez le criquet pèlerin Schistocerca gregaria Forsk. Colloque International CNRS (‘L’influence des stimuli externes sur la gamétogenèse des insectes'), 189, 7186.
  • Pener, M.P. (1991) Locust phase polymorphism and its endocrine relations. Advances in Insect Physiology, 23, 179.
  • Roessingh, P., Bouaïchi, A. & Simpson, S.J. (1998) Effects of sensory stimuli on the behavioural phase state of the desert locust, Schistocerca gregaria. Journal of Insect Physiology, 44, 883893.
  • Roessingh, P. & Simpson, S.J. (1994) The time-course of behavioural phase change in nymphs of the desert locust, Schistocerca gregaria. Physiological Entomology, 19, 191197.
  • Roffey, J. & Popov, G.B. (1968) Environmental and behavioural processes in a desert locust outbreak. Nature, 219, 446450.
  • Simpson, S.J., Despland, E., Hägele, B.F. & Dodgson, T. (2001) Gregarious behavior in desert locusts is evoked by touching their back legs. Proceedings of the National Academy of Sciences, USA, 98, 38953897.
  • Simpson, S.J., McCaffery, A.R. & Hägele, B.F. (1999) A behavioural analysis of phase change in the desert locust. Biology Reviews, Cambridge Philosophical Society, 74, 461480.
  • Sword, G.A., Simpson, S.J., El Hadi, O.T.M. & Wilps, H. (2000) Density-dependent aposematism in the desert locust. Proceedings of the Royal Society, London, 267, 6368.
  • Uvarov, B. (1966) Grasshoppers and Locusts, Vol. I. University Press, Cambridge.
  • Uvarov, B.P. (1977) Grasshoppers and Locusts, II. Centre for Overseas Pest Research, London.

Accepted 28 January 2003