Pener1991, Locust Phase Polymorphism and Its Endocrine

Locust Phase Polymorphism and its Endocrine
Relations
M. P. Pener
Department of Zoology, The Hebrew University of Jerusalem, 91904 Jerusalem, Israel
1 Insect polymorphism and its endocrine aspects 1

1.1 Polymorphism 1
1.2 Polymorphism and endocrine factors 3
2 Phase polymorphism 4
2.1 Locusts 4
2.2 Some other insects 7
3 Phase characteristics and related endocrine eEects 8
3.1 Morphology, morphometrics and anatomy 8
3.2 Colouration 12
3.3 Reproduction 21
3.4 Hopper development 26
3.5 Physiology, biochemistry and molecular biology 28
3.6 Cytology 30
3.7 Behaviour and activity 31
4 Endocrine organs, hormones and their role in phase transformation 37
4. I The corpora allata and juvenile hormone 37
4.2 The prothoracic (=ventral) glands and ecdysteroids 45
4.3 Neurosecretory cells, corpora cardiaca and neurohormones 48
5 Pheromones 49
6 Concluding remarks 52
References 55
Addenda 75
1 insect polymorphism and its endocrine aspects
1.1 POLYMORPHISM
The term polymorphism roughly means that distinct morphological dif-

ferences, reflecting and often including physiological, behavioural and/or
oecological differences, occur simultaneously or recurrently among con-
specific individuals. Although the phenomenon is easily recognized and well
known in many insect orders, its exact definition runs into difficulties. For
example, most authors would not apply the term polymorphism to sexual
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2 M. P. PENER
dimorphism, that is to morphological difference(s) other than in the genitalia

between males and females, neither to a sequence of different stages in the
course of metamorphosis (larva, pupa, adult). Some others, however, may
extend the meaning of polymorphism to include these cases. For a compre-
hensive overview, definitions and related terminology the paper of Richards
(1961) with its open discussion and the recent articles of Hardie and Lees
(1985) as well as of Pener (1985) may be consulted.
In many instances, polymorphism is under the strict control of the
genotype. This “genetic polymorphism” (Ford, 1961) is independent of
environmental factors, except for long-term effects through selection pres-
sure. In contrast, immediate environmental factors, such as photoperiod,
temperature, humidity, diet, and/or population density, often play a major
role in the determination of the actual morph, although obviously the
potential to exhibit such polymorphism in response to extrinsic factors is
genetic. Moreover, the genotype may modify the phenotypic responses to
environmental cues and the genetic ability to express environmentally
controlled polymorphism is itself subject to selection pressure.
In some cases, morphologically similar conspecific insects exhibit environ-
mentally induced major physiological and/or behavioural differences.
Michener (196 1) suggested calling such insects polyphenic rather than
polymorphic. Liischer (1976b) extended the meaning of “polyphenism” to
include morphological differences. Hardie and Lees (1985, p. 443) defined
polyphenism “. . . as the occurrence of two or more distinct phenotypes
which can be induced in individuals of the same genotype by extrinsic
factors.” This definition makes the term polyphenism practically synony-
mous with the older usage of environmentally regulated polymorphism. The
latter includes physiological and behavioural “polymorphism”, as well as
“facultative polymorphism” as used by Nijhout and Wheeler (1982), all
contrasting to “genetic polymorphism” (see above). Although from the
etymological standpoint “polyphenism” is more correct, I prefer the older
term, “polymorphism”, because it is deeply rooted in the literature.
Locust phase polymorphism is environmentally regulated, but it is
regarded as a “continuous polymorphism”. This term (see Kennedy, 1956,
1961) means that a continuous range of intermediates exists between the two
extreme phases. This subject will be discussed later (see Section 2.1), but its
definition again presents some difficulties because continuous “trivial”
variations, exhibited by all insects, for example in body length, are never
considered to be polymorphism. Although in the case of continuous poly-
morphism the differences between the extremes are more marked and the
range covered by the intermediates is much wider than in trivial variations,
attempts to make definitions which clearly separate the two phenomena run
into quantitative difficulties and arbitrariness. How much difference and how
LOCUST PHASE POLYMORPHISM 3
wide a range of intermediates are needed for unequivocal distinction? It does

not help that in the case of continuous polymorphism a given population,
made up from individuals which have experienced similar environmental
conditions, usually covers only a limited part of the full range. A population
of a species exhibiting only trivial variations may also cover only an
environment-dependent part of the full range. For example, body length
(trivial variation) of a population which has experienced food shortage
(environmental factor), may well be smaller than that of a population with
abundant food. These two populations may respectively cover the lower and
upper parts of the full range of this trivial variation.
1.2 POLYMORPHISM AND ENDOCRINE FACTORS
In environmentally controlled insect polymorphism (including physiological

and behavioural “polymorphism”), extrinsic cues induce sensory and/or
nutritional inputs. These are somehow coupled to the mechanisms which
make a “decision” to prefer a certain morph over the other(s), then
substantiate this preference in the course of development. Components of the
endocrine system are usually involved in these mechanisms and are often
major factors in the control of polymorphism.
The first studies on hormonal effects on insect polymorphism were carried
out on locusts by P. Joly (1949, 1951). Although he drew some preliminary
misconclusions, these were soon corrected (P. Joly and L. Joly, 1954; L. Joly,
1954; P. Joly, 1956; P. Joly et al., 1956). From the mid 1950s onward,
publications on endocrine effects on insect polymorphism became more
frequent. Up to the early 1960s most of them were devoted to locust phase
polymorphism, culminating in the comprehensive experimental works of L.
Joly (1 960) and Staal(l961). Even in this early period, however, some studies
already dealt with endocrine aspects of other kinds of polymorphism. For
example, colour polymorphism in the grasshopper, Acrida turrita, was found
to be affected by the corpora allata (P. Joly, 1952) and brain implantation
was reported to influence wing polymorphism in the cricket, Gryilus campes-
Iris (Sellier, 1955). Toward the turn of the decade, the first experimental
studies of endocrine effects on caste polymorphism in lower termites
(Luscher, 1961 and some further references therein) and on wing polymor-
phism in aphids (Lees, 1961) appeared. Although differences in the volume of
the corpora allata (CA) between queens and workers of the honey bee, Apis
mellifera, had been reported quite early (Lukoschus, 1955, and other
contemporary publications by the same author), the subject of endocrine
effects on caste determination in Hymenoptera gained momentum only
about 15 years later. Advances in the endocrine aspects of polymorphism in
4 M. P. PENER
aphids and social insects (termites, bees, ants) were summarized in a book
edited by Liischer (1 976a).
More recently, endocrine effects on insect polymorphism were reviewed by
Nijhout and Wheeler (1982) and Hardie and Lees (1985). Other recent
reviews, dealing with more restricted aspects of the subject, are those of Lees
(1983) on aphids, Pener (1983) on locust phases, relevant sections in the
articles of Brian (1979) and of De Wilde and Beetsma (1982) on social insects,
and a section on wing and flight related polymorphism in Pener’s (1985)
chapter.
2 Phase polymorphism
2.1 LOCUSTS
The theory of locust phases was formed by Uvarov (1921) in a taxonomic

revision of the genus Locusta. He concluded that L. migratoria and L. danica,
previously regarded as two distinct species, are respectively the swarming and
the solitary forms or “phases” of the same species; these forms are capable of
transforming into one another and are connected by intermediate forms. He
also claimed that the South African brown locust, Locustana pardalina, has
similar swarming and solitary phases. The phase theory was soon extended to
other locust species and phase transformation was verified both experimen-
tally and by field evidence (for a comprehensive study see Faure, 1932).
Within the first decade which followed Uvarov’s (1921) paper, the termino-
logy was formalized. The swarming crowded phase and the more sedentary
isolated one were given the latinized names “gregaria” and “solitaria”,
respectively. The intermediates were named as phase “transiens”, and some
authors even made the distinction between “congregans” and “dissocians”.
At this time, the term phase was used in three senses: ( 1 ) as a loosely
formalized taxonomical unit at the intraspecific level; (2) as an oecological
concept in relation to population density, separating migrating swarms or
hopper bands of locusts from those found in isolation or at intermediate
densities, and as an explanation, or even as “The Cause”, of the periodicity
of locust outbreaks; and (3) as a biological phenomenon or status, to
separate the different forms of the continuous density-dependent locust
polymorphism, with the overt or implicit understanding that various phases
differ not only morphologically, but also in other (physiology, behaviour,
etc.) aspects.
The relationship and the extent of correlation between taxonomical,
oecological and biological (polymorphism) concepts of locust phases led to
confusion resulting in much argument. The taxonomical concept, still
retained for example in Key’s (1950) review, was gradually abandoned also
by Uvarov (1 966) himself, though the latinized names are often used even
today because of historical reasons. It also became increasingly evident (see
contemporary reviews by Key, 1950; Kennedy, 1956, 1961, 1962; Gunn,
1960) that locust outbreaks are not caused by phase transformation; phase
change does not precede but follows changes in population density. When
locusts exhibiting “solitaria” morphology and colour but “gregaria” be-
haviour had been found in migrating bands or swarms (see references in the
reviews above), the oecological and biological (polymorphism) concepts of
the term phase were largely uncoupled. Today most authors agree that locust
phases do not designate migrating or non-migrating locusts; they are used to
characterize locust polymorphism, and the differences in locomotor activity
(see Section 3.7) are considered to be one phase characteristic among others.
This does not mean that locust phase polymorphism, locust migration and
the periodical appearance and disappearance of locust outbreaks are not
correlated; moreover, these phenomena presumably co-evolved. But their
correlation is less rigid than it was regarded some decades ago. The better fit
of the different phases to live in relative isolation or in groups in the field may
be considered as oecological aspects of the phase polymorphism or even as
oecological phase characteristics.
According to present views, typical locust species show density-dependent
phase changes in morphology, colouration, reproduction, development,
physiology, biochemistry, molecular biology, cytology, behaviour and oeco-
logy. The extreme phases are usually named by the non-latinized terms
“gregarious” and “solitary” (or “solitarious”). Full-scale phase differences
seem to be limited to the field. Locusts reared in the laboratory under
conditions of crowding and in isolation respectively only approach the
characteristics of the gregarious and solitary phases. Such laboratory popu-
lations are often named as “crowded” and “isolated”, instead of “gregar-
ious” and “solitary”, though this distinction is not consistent in the litera-
ture. As already stressed, locust phase polymorphism is continuous. Not only
are all kinds of intermediates found between the extreme phases, but phase
transformation itself is continuous and its induction is not instar-specific. In
other words, phase characteristics can be shifted in either direction, and the
direction of the shift is reversible in any stadium (except for eggs in the
ground), all in response to appropriate changes in density. Some phase
characteristics, such as behavioural patterns and some components of adult
colour, respond within the same instar to changes in density. Other charac-
teristics, like hopper colouration, exhibit changes in the next and/or subse-
quent instars. Some phase characteristics, for example the colour of the
hatchlings, are affected by parental density. Phase transformation is cumu-
lative, a phase shift starting in an instar progresses in the following ones and
6 M. P. PENER
also in the next generation; a full-scale phase transformation may take

several generations. Many density-dependent phase characteristics, such as
colour and morphometrics, are also affected by further environmental
factors, especially by humidity and temperature. Different locust species
show somewhat different phase characteristics and the amplitude of the
change of a given phase characteristic is often species-dependent and
sometimes sex-dependent. Phase polymorphism of locusts, phase characteris-
tics and the amplitudes of the changes in phase characteristics were compre-
hensively surveyed in Uvarov’s (1966) and Albrecht’s (1967) books. Other
reviews on the subject within the last two decades include those by May
(1971), Nolte (1974), Cassier (1974), and Pener (1983).
1 have defined locusts as short-horned grasshoppers (Orthoptera: Acridi-
dae) which “. . . meet two criteria: 1) They form at some (rather irregular)
periods dense groups comprising huge numbers, bands of hoppers and/or
swarms of winged adults which migrate; and 2) they are polymorphic in the
sense that individuals living separately differ in many characteristics from
those living in groups” (Pener, 1983, p. 379). The first criterion is based
rather on the same considerations which were somewhat dissociated from
phase above; but now it is used for the definition of locusts and not of locust
phases. In fact, this criterion is much older; it fits even the description of the
locusts in the Old Testament, for example as the plague inflicted on the
Pharaoh and the People of Egypt (Exodus, Chapter 10, Verses 4-19),
presently attributed to the desert locust (Schistocevca gregaria). The second
criterion is phase polymorphism as discussed above. Typically locust species
satisfy both these interrelated, but not completely correlated, criteria.
Many species of acridids tend to aggregate, and/or to migrate, and/or to
exhibit more or less rudimentary phase polymorphism (see Uvarov, 1966, pp.
369-375, 1977, pp. 142-1 50; Jago, 1985). Thus, the borderline between
gregarious grasshoppers and locusts is not very strict. For example, species of
the genus Melanoplus (Catantopinae, here and below, Uvarov’s 1966 classifi-
cation is used for the subfamilies) exhibit some phase polymorphism (Dingle
and Haskell, 1967 and references therein), but they are still regarded as
gregarious or migratory grasshoppers. The Australian plague locust, Chor-
toicetes terminifera (Oedipodinae), and the Moroccan locust, Dociostaurus
maroccanus (Gomphocerinae), are considered to be locusts, even though the
amplitude of their phase polymorphism is less extreme than that of some
other locusts. A few New World species of the genus Schistocerca (Cyrtacan-
thacridinae), such as the Central American S. piceiforms and the South
American S. cancellata, are also regarded as locusts; owing to taxonomical
confusion, these have been often named as S. paranensis and S. americana,
respectively, in the literature (for taxonomical considerations see Jag0 et al.,
1979; Harvey, 1981). The most typical locust species are: (1) the migratory
locust, Locusta migratoria (Oedipodinae), with its various subspecies, most

of which have recently been considered to be just geographical races,
although the subspecies status, L. m. migratorioides, is retained for all non-
diapausing populations from the tropics and from the southern hemisphere
(Farrow and Colles, 1980); (2) the brown locust, Locustana pardalina
(Oedipodinae), from South Africa; ( 3 ) the red locust, Nomadacris septemfas-
ciata (Cyrtacanthacridinae), from Central and South Africa; and (4) the
desert locust, Schistocerca gregaria (Cyrtacanthacridinae), for a few years
incorrectly named as S. americana gregaria (rectified by Jago et al., 1979),
from tropical and subtropical areas of the Old World extending from the
west coast of Africa to about the eastern border of India. These four species
will be referred to below only by their generic names.
Different locust species belong to several different subfamilies. This
situation probably indicates that locust phase polymorphism evolved several
times, by convergent evolution, within the family of acridids. The species-
dependent differences, both in certain phase characteristics and in the
amplitude of their changes, may well be explained by this assumption. As
already mentioned, many acridids exhibit tendencies of aggregation, mig-
ration and more or less rudimentary phase polymorphism (Uvarov, 1966,
1977; Jago, 1985). Typical locust species probably constitute only evolution-
ary culminations of these tendencies. Also, extreme phase polymorphism is
found only in a relatively small number of acridid species; other kinds of
polymorphism, such as non-density-dependent colour polymorphism (re-
views by Rowell, 1971; Fuzeau-Braesch, 1985), are exhibited by a much
larger number of species. It seems that evolution often led to the incorpora-
tion of colour polymorphism into the more complex phase polymorphism,
but again such incorporation probably occurred independently in different
locust species, or at least in different subfamilies. Altogether, locust phase
polymorphism, a highly complex phenomenon when any single species
is considered, becomes even more complicated when species-dependent
differences are taken into account.
2.2 SOME OTHER INSECTS
Density-dependent continuous polymorphism also occurs in some other

insects. The term phase polymorphism has often been employed to cover
such cases. The phenomenon is especially well known in several species of
Lepidoptera (see Faure, 1943a,b; Matthee, 1945, 1946, 1947; Long, 1953;
Iwao, 1962; as examples of earlier publications). There is no comprehensive
review on lepidopteran phase polymorphism, but the reader may consult
some recent research articles for up-to-date information (e.g. Tojo et al.,
8 M. P. PENER
1985a,b; Simmonds and Blaney, 1986; Fescemyer and Hammond, 1986;

Fescemyer et al., 1986). These reveal that the term phase is used in a double
sense, in relation to polymorphism exhibited mostly by larvae and to
migratory tendencies (flight) of the adults. As in locusts (see Section 2.1),
these two phenomena are surely interrelated, but it remains to be established
how strictly they are correlated. The endocrine regulation of lepidopteran
phase polymorphism is outside of the scope of the present review, but it may
be mentioned that juvenile hormone (JH) is involved in this regulation (Yagi,
1976; Yagi and Kuramochi, 1976; Tojo et al., 1985a; Fescemyer et al., 1986;
Fescemyer and Hammond, 1988). Nevertheless, as in locusts (see Section
4.l), JH may not necessarily constitute the sole endocrine factor in the
control of lepidopteran phase polymorphism (cf. Tojo et al., 1985a).
Density-dependent continuous polymorphism has also been found in some
other insects, for example in Tettigoniidae (Chopard, 1949; Verdier, 1958;
Robinson and Hartley, 1978), in Phasmida (Key, 1957) and in Gryllidae
(Fuzeau-Braesch, 1960).
3 Phase characteristics and related endocrine effects
Any characteristic which shows density-dependent changes in locusts is

considered to be a “phase characteristic”. Such phase characteristics, reflect-
ing differences between gregarious and solitary locusts, are found (and
obviously often intermingled) in morphology, anatomy, colour, reproduc-
tion, development, physiology, biochemistry, molecular biology, cytology,
behaviour and oecology. There are so many phase characteristics that they
cannot be fully surveyed in the present review. Only major, or recently
discovered ones, especially those which were subject to studies on hormone-
phase interrelations, will be discussed below. For a comprehensive treatment
of phase characteristics and an extensive list of references the reader is
referred to Uvarov’s (1966, 1977) and Albrecht’s (1967) books.
3.1 MORPHOLOGY, MORPHOMETRICS AND ANATOMY
In locusts, as in other acridid species, adult males are smaller than adult
females. However, the relative difference in body size between the two sexes
may be phase dependent, or conversely, the relative differences in body size
between the phases may be sex dependent. In Locusta, Schistocerca and
Numaducris solitary or isolated females are somewhat larger than conspecific
gregarious or crowded ones, but in the males of these species the situation is
reversed. Thus, in these cases, the differences in size between the females and
the males is smaller in the gregarious than in the solitary phase. However, in
Locustana, Dociostaurus maroccanus and Chortoicetes terminifera gregarious
adults of each sex are larger than conspecific solitary adults of the same sex.
The differences in body size between gregarious and solitary locusts have not
been claimed to be affected by endocrine factors.
The pronotum is high, its median carina is convexly arched and so forms a
crest in late hoppers and adults of solitary Locusta, but is rather straight or
even slightly concave in gregarious hoppers and adults of this species (Fig. 1).
Similar, but much less marked, differences may exist also in other locusts (see
Faure, 1932, measurements of Locustana; and Dirsh, 1953, drawings of
Schistocerca). No endocrine effects on phase-related differences in the shape
of the pronotum have been claimed, and P. Joly (1956) and P. Joly et al.
(1956) explicitly stated that the median carina of the pronotum does not
change its gregarious shape after implantation of extra CA into crowded
Locusta. These authors concluded, therefore, that this phase characteristic
does not seem to be dependent on the CA.
FIG. 1 Lateral view of the pronotum in adults of Locusta: (a) solitary or isolated
locusts; (b) and (c) gregarious or crowded locusts. Linear magnification, c. x 4.5.
The morphological differences between gregarious and solitary locusts are

mainly quantitative and are usually studied by measurements of various
parts of the body and their relative comparisons. Up to the late 1950s only
10 M. P. PENER
simple morphometrical ratios were employed, especially the E/F ratio (length
of the fore wing : length of the hind femur) and the F/C ratio (length of the
hind femur : maximum width of the head). The latter, introduced by Dirsh
(1951, 1953), is considered to be a better parameter for expression of phase
differences. The F/C ratio is higher, whereas the E/F ratio is lower, in solitary
than in gregarious locusts (cf. Dirsh, 1951, 1953; Uvarov, 1966).
P. Joly and L. Joly (1954) and P. Joly (1956, 1962) reported that
implantation of extra CA into crowded hoppers of Locusta leads to a
decrease of the E/F ratio after the moult to the sixth instar (which is the adult
in normal development of this species). These authors even obtained
“hypersolitary” E / F ratios and they related the results to a “solitarizing”
effect of the CA. Staal(l961) obtained similar results, but he related them to
metathetelic disturbances in metamorphosis rather than to a phase shift. P.
Joly (1962) found no effect of implanted CA on the F/C ratio in Locusta.
However, in more comprehensive experiments, Staal (1961) observed a
rather complex situation, finding the following effects on the F/C ratio in
crowded Locusta: (A) an increase (of this ratio) in the metamorphic moult
from normal fifth-instar hoppers to normal (sixth-instar) adults; (B) an
increase in the adults obtained from hoppers isolated after hatching; (C) an
increase in the adults obtained after implantation of extra CA into second-
instar hoppers; but (D) a decrease in the often metathetelic sixth-instar
locusts obtained after implantation of extra CA into young fifth-instar
hoppers. From these results Staal (1 961) concluded that although early
implantation of extra CA and isolation both cause a somewhat parallel
increase of the F/C ratio, the isolated (solitary) locusts do not seem to be
simply slightly metathetelic or neotenous forms of the crowded ones. Owing
to the fact that the F/C ratio increases during normal metamorphosis to the
adult, prevention of this increase, that is F/C values lower than in the normal
adult, would be characteristic of metathetely or neoteny. Indeed, such lower
values are obtained after implantation of CA into the young fifth-instar
hoppers. Isolation, however, causes an increase of the F/C ratio, just the
opposite to the shift expected in metathelic creatures.
Implantation of ventral glands (VG), equivalent in acridids to the prothor-
acic glands of other insects, into first- or second-instar hoppers of Locusta led
to some disturbances in metamorphosis (Staal, 1961). A portion of the
locusts had already reached adult morphology by the fifth instar. These
adults were somewhat smaller than normal (sixth-instar) adults, but they
exhibited typical adult E/F and almost adult F/C ratios. A smaller portion of
the locusts did not show such precocious metamorphosis; they became fifth-
instar hoppers with hypertrophied wing buds. They then moulted to giant
adults which exhibited very high, “hypergregarious”, E/F ratios (Staal, 1961;
Staal and De Wilde, 1962). Carlisle and Ellis (1962) reported that a positive
correlation exists between the size of the ventral glands and the F/C ratio in
Schistocerca.
Although these simple morphometrical ratios are still used, they were
rightly criticized by several authors who introduced into phase morpho-
metrics more complicated, but also more correct and informative, statistical
methods based on multivariate analysis (Albrecht and Blackith, 1957;
Blackith and Albrecht, 1959; Stower et al., 1960; Symmons, 1969; Lauga,
1976a,b; reviews by Blackith, 1972; Lauga, 1977a). Stower et a/. (1960),
employing discriminant functions, showed that non-density-dependent
environmental factors also affect phase-related morphometrics; in very
general terms, high temperatures shifted the morphometrical results toward
the solitary phase in Schistocerca. High temperatures and increasing day-
length (Albrecht and Lauga, 1978), as well as high humidity (Albrecht and
Lauga, 1979) also induced a “solitarizing” effect on the morphometrics of
Locusta. Unfortunately, these advanced statistical techniques have not been
employed for investigating effects of endocrine factors on phase morpho-
metrics. A notable exception is Lauga’s (1977b) study, which is related,
however, to morphometrics of hatchlings (see Section 3.3.3). Thus, relevant
knowledge is practically limited to endocrine influences on the simple
morphometrical ratios (see above). These indicate that endocrine factors may
affect phase morphometrics, but separation of the effects into disturbances of
metamorphosis and into phase shifts run into difficulties and the interpre-
tation of the results are not sufficiently clear.
Solitary adults of Schistocerca and Nomadacris have usually one more
stripe in the compound eyes than conspecific gregarious adults. The number
of eye stripes in the adult of these species is equal to the number of instars
including the adult instar itself (see Albrecht, 1955, and further references
therein). Thus, the difference reflects the fact that solitary locusts of these
species usually have an additional hopper instar (see Section 3.4).
The sternal hairs of adult Locusta are longer in insects reared under
crowding and under dry conditions; implantation of extra CA leads to a
decrease of the length of these hairs (Staal, 1961). However, as the sternal
hairs are much shorter in hoppers than in adults, it is again difficult to
distinguish between metathetelic disturbances and a phase shift.
In Locusta, isolated adults and fifth-instar hoppers have more basiconic
and coeliconic sensilla on the antennae than the respective crowded locusts
(Greenwood and Chapman, 1984). This finding may indicate that isolated
locusts do not constitute a slightly metathetelic form of the crowded ones,
because the number of antenna1 sensilla markedly increases from the fifth-
instar hopper to the adult; thus, metathetelic adults would be expected to
have fewer sensilla. However, no actual experiments were carried out on the
possible effects of endocrine factors on this phase characteristic.
12 M. P. P E N E R
Cassier and Delorme-Joulie (1976) and Cassier (1977) reported that

crowded adult males of Schistocerca have a thicker epidermis
(= hypodermis) and more numerous gland cells (which presumably produce
the so-called “maturation-accelerating pheromone”; see Section 3.3.1) than
isolated adults or crowded adult females. They claimed that solitary or
gregarious characteristics of the epidermis of adult males are determined by
the endocrine balance at about the moult from the fourth to the fifth instar
( = from the penultimate to the last hopper instar in crowded Schistocerca).
The presence of ecdysone alone, or of both ecdysone and JH, at this moult
was supposed to induce at the next moult (to the adult), gregarious-type or
solitary-type male epidermis, respectively. These conclusions were drawn
from experiments which included allatectomy, CA implantation, injection of
JH or of ecdysone, but all endocrine manipulations were carried out on
crowded locusts. Unfortunately, these authors did not allatectomize isolated
locusts at the postulated critical period (close to the moult from the
penultimate to the last hopper instar) to investigate whether the epidermis
differentiates to the gregarious-type or to the solitary-type in the adult male.
Since nymphs have a thin epidermis with few gland cells, it is possible that the
results obtained with the crowded locusts reflect metathetelic disturbances in
metamorphosis rather than a real phase shift. Investigating gland cells in the
abdominal epidermis of adults and fifth-instar hoppers of Locusta, Ali (1987)
also found differences between crowded and isolated locusts; this study,
however, did not test the possible influences of endocrine factors.
The number of ovarioles i s higher in female hatchlings obtained from eggs
laid by isolated mothers in Locusta (Albrecht et al., 1958, 1959), Nomadacris
(Albrecht, 1959) and Schistocerca (Papillon, 1960). Endocrine effects on this
characteristic will be discussed in relation to reproduction (see Section 3.3.3).
Some further differences in the morphology of gregarious and of solitary
locusts, such as the armature of the hind femur and hind tibia in adults of
Schistocerca and Locusta, and the number of stridulatory pegs on the fore
wing of adult Locusta, were listed by Uvarov (1966, and references therein;
see also Fuzeau-Braesch et al., 1973, for a later publication). The effect of
endocrine factors on these differences are not known.
3.2 COLOURATION
3.2.1 General aspects, hoppers and associated hopper-adult features
Acridids frequently exhibit environmentally regulated or phenotypic colour

polymorphism (reviews by Uvarov, 1966; Albrecht, 1967; Rowell, 1971;
Fuzeau-Braesch, 1972, 1985), also termed polychromatism (Fuzeau-Braesch,
1985). Three major types of such colour polymorphism occur in this family:
( I ) “homochromy”, that is adaptation of the colour to that of the neighbour-
ing background; ( 2 ) “green-brown’’ polymorphism; and (3) phase or density-
dependent colour polymorphism. An acridid species may show none of them,
or only one type, or a combination of two, or even all three types, and often
there are differences between hoppers and adults of the same species.
Hoppers of Locusta constitute a well-investigated example of a highly
complex case. In this species, the three types of colour polymorphism are
superimposed one upon another in a kind of hierarchy (Fig. 2). First-instar
hoppers, originating from eggs laid by gregarious or crowded females, are
dark, and crowded hoppers in the later instars are dirty orange with black
patterns. In contrast, hatchlings from eggs laid by solitary or isolated females
are light grey, and solitary hoppers have a uniform colour without black
patterns (Faure, 1932; Gunn and Hunter-Jones, 1952; Hunter-Jones, 1958).
This is the density-dependent or phase colour polymorphism and it stands at
the highest level of the hierarchy; the gregarious colour excludes further
kinds of colour polymorphism. Solitary hoppers exhibit the so-called “green-
brown” polymorphism; under high humidity they are uniformly green,
whereas under low humidity the colour is uniform but not green, although
not necessarily “brown” (Faure, 1932; Staal, 1961; Albrecht, 1964, 1965).
The green colour excludes the third type of colour polymorphism, the
“homochromy”, which stands at the lowest level of the hierarchy. Under low
humidity, solitary hoppers adjust their colour- whitish-cream, straw yellow,
beige, buff, brown, grey, black or intermediate shades-to match the colour
of the underlying background in the field, or the inside colour of the cages/
containers in the laboratory (Faure, 1932; Hertz and Imms, 1937; Albrecht,
1965).
Locustana also shows all three kinds of colour polymorphism; their
hierarchical order and the environmental factors which affect colour poly-
morphism in this species seem to be similar to those in Locusta (cf. Faure,
1932). In contrast, Schistocerca (Hunter-Jones, 1958; Stower, 1959) and
Nomadacris (Faure, 1932; Michelmore and Allan, 1934; Lea and Webb,
1939; Burnett, 1951) exhibit mostly phase colour polymorphism. In Schisto-
cerca, first-instar hoppers originating from eggs laid by solitary or isolated
females are rather uniformly light pale green; this colour becomes more
intense, often emerald green, without black patterns, in later instars of
solitary hoppers. First-instar hoppers from eggs laid by gregarious or
crowded females are dark with little light areas (practically black); gregarious
hoppers are creamish with black patterns in the second and third instars and
bright yellow with black patterns in the later ones. Hunter-Jones (1962)
observed that isolated hoppers of Schistocerca kept under high humidity are
uniformly green without black patterns, whereas those kept under dry
14 M. P. PENER
(PHASE COLOUR -
isolation - Solttary colour
(uniform colour)
I
black patterns)
factor ( 'GREENIBROWN'
I POLYMORPHISM )
Block- black
I llght -Whitish cream
BACKGROUND ( 'HOMOCHROMY')
More or less respective shades of these colours
FIG. 2 Diagrammatic presentation of the three different kinds of superimposed

colour polymorphism in hoppers of Locusta rnigrutoriu. The environmental factors
which exert the major effect on each type of colour polymorphism (in parentheses) are
boxed. The appropriate changes in the environmental factors are underlined, whereas
the actual colour(s) exhibited by the hoppers are not. Endocrine effects on colour are
encircled. For further details, see text. CA, corpora allata; CC corpora cardiaca; JH,
juvenile hormone; NSC, neurosecretory cells.
conditions show a wide colour variation-green, yellow-green, olive green,

shades of brown, as well as other colours-and also exhibit some of the black
patterns of the gregarious hoppers. Stower (1959) found brown solitary
hoppers of Schistocerca with vestigial black patterns in dry field habitats. The
non-green solitary hoppers in dry environments may be regarded as a
"brown" form of a somewhat limited humidity-dependent green-brown
polymorphism, but this consideration does not account for the vestigial
black patterns. On the other hand, the reduced black patterns may reflect an
incomplete phase colour change under dry conditions, but this explanation
disregards the fact that the bright yellow component of the gregarious colour
is entirely missing. Obviously, these two interpretations are not mutually
exclusive. Hoppers of Nomadacris also exhibit a clear phase colour polymor-
phism and possibly a limited green-brown polymorphism; the details are
rather parallel to those observed in hoppers of Schistocerca, including a
tendency of retention of reduced black patterns in non-green solitary hoppers
(Faure, 1932; Michelmore and Allan, 1934; Lea and Webb, 1939; Burnett,
1951).
Even the relatively rigid gregarious colouration of locust hoppers is further
influenced by factors unrelated to density. Low temperatures increase the
black patterns, whereas high temperatures reduce them both in the field
(Stower, 1959) and in the laboratory (Dudley, 1964). At intermediate
densities great variations of intermediate colourations are observed (see for

example Stower, 1959, colour plates). Both green-brown polymorphism and
homochromy are subject to considerable individual variations; results of
field observations or of laboratory experiments often reveal a distinct
phenotypic dominance of a certain colouration, but usually some minority of
the population shows deviations from this dominant colouration. Also,
changes in density, or in other environmental factors, experienced by a
certain hopper instar, do not necessarily result in an immediate full-scale
colour change; the next instar may exhibit various intermediate colourations,
and stabilization of the colour may occur only in later instar(s). Considering
all these factors and effects, almost endless variations exist in the actual
colouration of locust hoppers (see colour plates by Faure, 1932; Stower,
1959).
All three types of phenotypic colour polymorphism in acridids are due to
“morphological colour changes” (cf. Raabe, 1982, 1983; Fuzeau-Braesch,
1985), that is the visible colouration changes due to alterations in synthesis,
oxidation-reduction, degradation, etc., of one or more pigments. Insect
pigments or biochromes (recent reviews by Needham, 1978; Fuzeau-Braesch,
1985) are well investigated, both in relation to acridids and their colour
polymorphism, including locust phase colour polymorphism (reviews by
Goodwin, 1952; Nolte, 1965; Uvarov, 1966; Albrecht, 1967; Rowell, 1971;
Fuzeau-Braesch, 1985). Nevertheless, as outlined by Rowell (1971) and
Fuzeau-Braesch (1989, clarification of the exact relation between pigments
and actual (=visible) colouration runs into considerable difficulties.
According to present concepts (see reviews above), four groups of pig-
ments make major contributions to the visible colouration of locusts. These
are the melanins, ommochromes (formerly also termed insectorubin), bile
pigments and carotenoids. Some other pigments, such as pterins, may also
play some role (cf. Nolte, 1965; Bouthier, 1966).
The green colour of solitary hoppers under high humidity is attributed to a
mixture of a blue bile pigment and yellow caroteinoid(s) (Goodwin and
Srisukh, 1951; Goodwin, 1952), or to a green bile pigment alone (Passama-
Vuillaume, 1965), all linked to proteins. The former view was accepted by
most authors, including Dadd (1961) who obtained blue or greenish-blue
locusts on a carotenoid-free diet, and Rothschild et al. (1977). Rowell (1971)
has pointed out that the two views may be somewhat reconciled by assuming
that the bile pigment (mesobiliverdin-protein complex) is sufficiently labile
to change between blue and green.
The black patterns of the gregarious hoppers are attributed to cuticular
melanins overlying dark areas of epidermal ommochromes; these two groups
of pigments show, therefore, a close spatial association in this case (Nicker-
son, 1956; Fuzeau-Braesch, 1965, 1966). The same pigments seem to be
16 M. P. PENER
responsible in Locusta also for the dark-blackish colour of the “homo-

chrome” solitary insects obtained on black background, though in this
instance the ommochromes may predominate and the black colour is less
restricted to well-defined patterns. Interestingly, daily repeated short (1 min)
treatments of crowded Locusta with CO, induces solitary characteristics,
including solitary colouration and disappearance of the black patterns, but
these “solitarized” locusts are as able to exhibit black homochromy as normal
isolated ones (Fuzeau-Braesch and Nicolas, 198I ; and references therein).
The situation is unclear for the pigments responsible for the yellow or
orange component of the gregarious hcppers on the one hand, and for the
“brown” colour shades of the solitary “homochrome” hoppers on the other.
Various authors have advocated a definite role of one or more pigments in
different or even in the same species, and if all the relevant publications are
considered, practically all the major groups of pigments have been claimed to
play a role. For details and discussion of the often controversial findings and
conclusions, the reader is referred to Rowell’s (197 1) comprehensive review.
The effects of endocrine factors on locust colouration have usually been
investigated only at the level of visible colours, leaving the effects on the
pigments open to speculations. Such speculations are frequent in the
literature, but their value is very limited due to the lack of firm knowledge on
the exact relationships between visible colours and pigments (see above).
Experimental work on the hormonal effects on the pigments is much needed;
meanwhile, however, a meaningful discussion is necessarily restricted to
visible colouration.
Implantation of extra CA, or administration of JH or JH analogues, to
crowded hoppers induce the green solitary colour (Fig. 2). This effect was
first demonstrated in Locusta (P. Joly and L. Joly, 1954; L. Joly, 1954; P. Joly
et al., 1956) and was amply reconfirmed in both Locusta (L. Joly, 1960: Staal,
1961; P. Joly, 1962: P. Joly and Meyer, 1970; NEmec et at., 1970; Fuzeau-
Braesch, 1971; Roussel, 1975d, 1976a,b; Couillaud et al., 1987) and Schisto-
cerca (Novak and Ellis, 1967; Roussel and Perron, 1974; Mordue (Luntz),
1977). Even green isolated hoppers became greener after implantation of
extra CA (Ellis and Novak, 1971), and injection of JH to isolated non-green
(homochrome) hoppers of Locusta also induced a green colour (Nicolas,
1977). Surgical allatectomy of green isolated hoppers led to high mortality,
but available results indicated loss of the green colour after such an operation
(L. Joly, 1960; Staal, 1961). Employing precocene-induced chemical allatec-
tomy (Pener et al., 1978), these results were reconfirmed by M. P. Pener and
J. De Wilde (unpublished); chemical allatectomy of green isolated Locusta
hoppers led to the disappearance of the green colour. In these experiments,
however, the resulting colouration was similar to that of the “brown”
homochrome hoppers, and so markedly different from the gregarious
colouration! Thus, although the relationship between JH and green colour

seems to be absolute, endocrine manipulations involving CA/JH in isolated
Locusta hoppers shifts one solitary characteristic to another, from green to
homochrome after chemical allatectomy as in the experiments of M. P. Pener
and J. De Wilde (unpublished), or from homochrome to green as in Nicolas’
(1977) study.
The green-colour promoting effect of experimentally induced JH surplus in
crowded Locusta is correlated with a marked regression, up to complete
disappearance, of the black patterns after the next moult(s). However, the
mechanism underlying the black-pattern reducing effect of JH is unknown; it
may be direct, or mediated through a negative interaction with the black-
colour inducing neurosecretory factor (see below), and/or the green colour
may exert a negative feedback at the level of the epidermis on the production
of the pigments responsible for the black colour.
It must be emphasized that the green-colour inducing effect of CA/JH is
not confined to locusts and phase polymorphism. Many acridids from
different subfamilies exhibit green-brown polymorphism without any den-
sity-dependent colour polymorphism (cf. Uvarov, 1966; Rowell, 1971) and
JH promotes the green colour also in these cases. Implantation of extra CA
into hoppers of Acrida turrita (Acridinae) induced green colour (P. Joly,
1952) and similar treatment led to similar results (Rowell, 1967) in Humbe
tenuicornis, Gustrimargus africanus (both Oedipodinae) and Acanthacris
rujicornis (Cyrtacanthacridinae). Green adults were even obtained in A .
ruficornis, despite the fact that such adult colouration has not been observed
in natural populations. Moreover, JH also promotes green colour in non-
acridid insects, especially in larvae of Lepidoptera (review by Raabe, 1983;
for a later work see Fescemyer and Hammond, 1988). Bioassays for J H were
even based on the green-colour inducing effect of the hormone in larvae of
Manduca sexta (Truman et a[., 1973; Fain and Riddiford, 1975), and a black
larval mutant of this species was shown to be caused by a reduction in J H
titres, due to a reduced CA activity (Safranek and Riddiford, 1975; Kramer
and Kalish, 1984).
The existence of an endocrine factor which promotes the black colour in
locusts was first claimed by Nickerson (1954, 1956), who injected haemo-
lymph of crowded Schistocerca hoppers into isolated ones and obtained an
increase of the gregarious black patterns. Injection of haemolymph from
isolated to crowded locusts had no effect on the colour. Staal(l961) observed
an increase of the black patterns after implantation of extra corpora cardiaca
(CC) into hoppers of Locusta, noting that the relevant factor from the CC
may be identical with the haemolymph factor found by Nickerson. Staal’s
findings were confirmed and the factor from the CC was traced back to some
neurosecretory cells (NSC) in the protocerebrum (Girardie and Cazal, 1965;
18 M. P. PENER
Girardie, 1974; Bouthier, 1976). However, this NSC-CC factor, or a factor of

similar origin (Fig. 2), also promotes black colour in isolated Locusta
(Nicolas and Ismai‘l, 1978), and thus it may be involved in the control of the
black homochrome response.
Like the effect of JH on green colour, the black-colour promoting effect of
this NSC-CC factor does not seem to be restricted to locusts or phase
polymorphism. A factor from the same organs is responsible for the black
homochrome response of the grasshopper Oedipoda coerulescens (Moreteau-
Levita, 1972a,b; Moreteau, 1975), which exhibits marked homochromy but
neither green-brown nor phase colour polymorphism. A neurohormonal
factor also promotes dark or black colour in some non-acridid insects, but
the site(s) of synthesis and/or release of this factor depends on the species
(Raabe, 1982, 1983, and references therein), and there is no clear evidence
that this factor is identical in all species. Bursicon, itself a neurohormone,
also affects darkening. Padgham (1976b) reported that bursicon induces
“melanization” (darkening) and sclerotization in crowded Schistocerca
hatchlings; the hormone is also present in pale hatchlings, but in these it only
induces sclerotization. These findings indicate that the integument of the
dark and pale hatchlings reacts differently to the same hormone. According
to Vincent (1972) bursicon is present in the brain, CC and ventral nerve cord
of Locusta, but it is released from the last abdominal ganglion. In contrast,
Padgham (1976a) claims that in Schistocerca hatchlings a melanizing factor,
presumably bursicon, is released from neu.rosecretory axon terminals in fine
nerves posterior to the metathoracic ganglion, possibly due to some signal
originating from the prothoracic ganglion. Clearly, more work is needed on
bursicon production and release, on its role in darkening, as well as on its
relation to the NSC-CC darkening factor in locusts.
Partial extirpation of the ventral glands (VG), equivalent in acridids to the
prothoracic glands (PG) of other insects, was claimed to induce gregarious
colouration in isolated Schistocerca (Ellis and Carlisle, 1961; Carlisle and
Ellis, 1962). In contrast, following partial extirpation of the VG, or after
implantation of extra VG, Staal (1 961) observed no appreciable colour
changes in Locusta. Since the VG (or PG) secrete ecdysone (or immediate
precursors which are rapidly converted to ecdysone; cf. Warren et al., 1988),
the fact that ecdysteroid titres do not differ markedly between isolated and
crowded locusts (see Section 4.2) seems to agree with Staal’s findings.
3.2.2 Adults
Green solitary adults, usually obtained from green hoppers, are well known
in Locusta and Locustana (Faure, 1932). After the first few days following
fledging Locusta adults are no longer able to become green (Albrecht, 1965),
but green adults may show fading of this colour under dry conditions
(Albrecht, 1965), or after being transferred to a crowd of adults (Pener,
1976b). Homochromy is more restricted in solitary adults of Locusra than in
hoppers, but the black homochrome response of isolated adults is still
marked (see colour plates by Fuzeau-Braesch, 1965, 1985). Solitary adults of
Schistocerca and Nomadacris are not green, even if they are obtained from
uniformly green hoppers, and adults of these species d o not show homo-
chromy.
Gregarious or crowded locusts exhibit a quite consistent course of colour
changes during adult life strongly associated with sexual maturation. Solitary
or isolated adults do not show such changes, or, as in Locusta, the colour
change is limited to the hind wings. Crowded fledglings of Schistocerca are
pink, but after a few days the colour turns to pinkish-beige, then to beige or
brown. Eventually females become yellowish and males bright yellow after
the onset of full sexual maturation (Chauvin, 1941; Norris, 1954; Pener,
1967a). Somewhat similar courses of colour change also occur in gregarious
or crowded adults of Nomadacris (Michelmore and Allan, 1934), Locustana
(Faure, 1932) and Locusta. In Locusta, the development of the bright yellow
coiour over the body is restricted to crowded males (for a detailed system
scoring the yellow colour see Pener et al., 1972); crowded females show
yellowing only on the hind wings. Isolated Locusta do not become yellow
over the body, but both sexes show marked yellowing of the hind wings
(Pener, 1976b). In all cases the yellow colour coincides with sexual matu-
ration. Beside density, temperature also affects yellowing being more intense
at higher temperatures.
The yellowing of crowded adult locusts depends completely on the CA and
the J H they produce. Allatectomy of last-instar hoppers or of young adults
prevents yellowing, whereas reimplantation of CA or administration of J H
reinduces it in Schistocerca (Loher, 1961; Pener, 1965b, 1967a,b; Odhiambo,
1966a; Amerasinghe, 1978b, Pener and Lazarovic;.i,1979), Locusta (Girardie,
1966; Girardie and Vogel, 1966; Pener et al., 1972; Pener, 1976b) and
Nomadacris (Pener, 1968). Allatectomy of sexually mature yellow adults
results in the fading of the yellow colour (Pener, 1965b). The yellowing
restricted to the hind wings of isolated Locusta adults also depends on JH;
after allatectomy it does not take place (Pener, 1976b). However, despite this
absolute relationship between CA, J H and yellowing, JH is not the primary
factor responsible for the differences in the yellow colour between gregarious
and solitary adults. Isolated adults may have higher JH titres than crowded
ones (see Section 4.1), nevertheless they d o not become yellow. Moreover,
implantation of extra CA into isolated adults does not induce yellowing,
whereas transfer of isolated adults into newly formed crowds does, even
without implantation of extra CA (Pener, 1976b). Thus, J H is necessary but
20 M. P. PENER
not sufficient for yellowing to occur, and the epidermis and/or the relevant
pigment system(s) react differentially to J H in crowded and isolated adults.
Goodwin (1952, and references therein) related the colour of crowded
fledglings, pink in Schistocerca and grey-brown in Locusta, to ommochromes
(under the name insectorubin) and claimed that the yellow colour of the
crowded adults is due to accumulation of carotenoids, especially p-carotene,
in the integument. This claim has been widely cited as an established fact
(Nolte, 1965; Uvarov, 1966; Fuzeau-Braesch, 1985), but the situation may be
more complicated. Allatectomy of crowded adult Schistocerca males affected
ommochrome and purine content of the integument (Ballan-Dufrangais,
1978). Moreover, unpublished results (J. Gross, M. P. Pener and M.
Rothschild) showed that p-carotene content in the integument of allatecto-
mized non-yellow males increases similarly to that in normal yellow males of
crowded Schistocerca. Again, more experimental work is needed to clarify
the role of pigments underlying the visible yellow colour of gregarious adult
locusts and to reveal the role of J H at the level of the pigments.
3.2.3 Some conclusions
The available experimental evidence clearly demonstrates that endocrine

factors do affect several major components of locust colouration. Neverthe-
less, none of these factors seem to play a physiologically primary causal role
in locust phase colour polymorphism. By inducing yellow colour in crowded
adults, JH promotes a gregarious characteristic, but the competence of the
adult’s integument to become yellow is governed by some density-dependent
unknown intrinsic factor(s). The lack of response of isolated adults to the
yellow-colour inducing effect of the JH cannot be explained by the assump-
tion that the relevant competence of the adult integument was already fixed
by endocrine events during hopper development, because simple transfer of
isolated adults to a crowd changes the competence and leads to yellowing. By
inducing green colour in hoppers and fledglings, J H promotes solitary
characteristics, but the effect is not restricted to locusts since it exists also in
other acridids which show “green-brown” polymorphism without any den-
sity-dependent phase colour polymorphism. Moreover, the very existence of
the “brown” homochrome forms of solitary locusts demonstrates that the
green colour is not a necessary characteristic of the solitary phase. Rele-
vantly, promotion of this “brown” solitary colour by JH has never been
observed (cf. Pener, 1976b). The black-colour promoting NSC-CC factor
again may not be confined to locusts, because it seems to play a role also in
the black homochrome response of grasshoppers which show no phase
colour polymorphism.
Phase colour polymorphism is much less frequent in acridids than “green-

brown” polymorphism or homochromy, and each major locust species is
taxonomically closely related to many acridids which exhibit the latter types.
It seems, therefore, that some not necessarily simple mechanisms, which
control “green-brown” polymorphism by CA activity and JH titres, and
black colour by the NSC-CC factor in grasshoppers, were “co-apted” during
evolution to play partial roles in a more complex phase colour polymor-
phism. The increasing JH titres in the adults, primarily related to reproduc-
tion, might have also been so “co-apted” for inducing yellow colouration
with sexual maturation in gregarious locusts. Although the phase-dependent
adaptive advantage of this yellow colour is not clear, again many non-locust
acridids show adult colour changes in relation to sexual maturation (see
Uvarov, 1966). It must be emphasized, however, that no coherent picture
accounting for all aspects of locust phase colour polymorphism emerges even
by addition of all these partial mechanisms.
3.3 REPRODUCTION
3.3.1 Maturation and maturation-accelerating pheromone
The period elapsing between fledging and sexual maturation is shorter in

isolated than in crowded Locusta (Norris, 1950; Pener, 1976a), but the
situation is reversed in Schistocerca (Norris, 1952; Papillon, 1968). Norris
(1964) related this difference to a differential balance of two counteracting,
possibly pheromonal, effects. In both species, presence of mature males
accelerates the maturation of young adults, but that of young males retards
maturation. In Locusta, the inhibitory effect is more prominent and/or longer
lasting, whereas in Schistocerca the activatory effect dominates. Under
crowding, therefore, change-over from inhibition to acceleration occurs
relatively later in Locusta than in Schistocerca. In both species, however,
these counteracting effects result in a more or less synchronous sexual
maturation of the crowded locusts. This synchrony may be considered as an
advantage for gregarious adults because, to be adapted for living in swarms,
their activities, for example migratory flight or reproduction, should be
synchronized.
The maturation-accelerating effect exerted by mature males on young
adults in Schistocerca (Norris, 1954) was shown to be due to a CA-dependent
production of a maturation-accelerating pheromone (Loher, 1961; Ameras-
inghe, 1978’0); in fact, the presence of allatectomized males, or of allatecto-
mized females, inhibits the maturation of young adult males (Norris and
Pener, 1965). From histological and ultrastructural studies on the number of
22 M. P. PENER
gland cells in the epidermis (see also Section 3.1) and the state of activity of
these cells, Cassier and Delorme-Joulie (1 976) and Cassier (1977) concluded
that isolated adult Schistocerca males do not produce maturation-accelerat-
ing pheromone. In contrast, Amerasinghe (1978a) observed that sexually
mature non-yellow isolated males and yellow crowded males (see Section
3.2.2) equally accelerate the maturation of young males and concluded that
the isolated males also produce maturation-accelerating pheromone. How-
ever, the experimental findings on which these controversial conclusions are
based do not seem to exclude the possibility that crowded adult males may
produce more pheromone than isolated ones, and so the difference in
pheromone production is possibly quantitative. In any case, under complete
isolation the pheromone cannot exert an actual effect on other locusts.
3.3.2 Male sexual hehaviour
A further reproduction-related phase characteristic is that crowded Locusta

males exhibit markedly more intense mating behaviour than isolated ones
(Pener, 1976a). Male mating behaviour is known to be affected by the CA in
some acridids (review by Pener, 1986), but in Locusta the effect is phase
dependent. Allatectomy drastically reduces the intensity of this behaviour in
crowded males, but has only minor effects in isolated ones (Pener, 1976a). In
this instance, therefore, by elevating the intensity of the sexual behaviour in
crowded males, the CA (or JH) promotes a gregarious phase characteristic.
However, as in the case of induction of yellow colour in adult males (see
Section 3.2.2), J H does not constitute a primary physiological causal factor
for the phase-related differences in the intensity of male sexual behaviour.
Implantation of extra CA into isolated males does not affect the eventual
intensity of this behaviour and so does not elevate it to the level shown by
crowded males (Pener, 1976a). Thus, the target organs (presumably the
nervous system in this case) again seem to respond differentially to JH in
crowded and isolated Locusta.
3.3.3 Female reproductive parameters and maternal effects on hatchlings
The reproductive potential or fecundity of isolated females is higher than

that of crowded ones in Locusta (Norris, 1950; Albrecht et al., 1958),
Nomadacris (Albrecht, 1959; Norris, 1959) and Schistocerca (Papillon, 1960,
1970). This difference is primarily because parental density markedly affects
the number of ovarioles developing in the embryo; in female hatchlings
originating from eggs laid by isolated females of Locusta (Albrecht et al.,
1958, 1959), Nomadacris (Albrecht, 1959) and Schistocerca (Papillon, 1960),
this number is higher than in those originating from eggs of conspecific
crowded females. The effect of the density is cumulative; the number of

ovarioles is highest in locusts kept under isolation for several consecutive
generations (Albrecht et al., 1958; Albrecht, 1959; Injeyan and Tobe, 1981a).
For example, Injeyan and Tobe (1981a) reported that the average number of
ovarioles was 110 in crowded females of Schistocerca, and it increased to 130
and 154 in the second and fourth generation of isolated locusts, respectively.
However, despite the differences in the number of ovarioles, the average
weight of an egg pod (Albrecht et al., 1958) and the average vitellin content
per ovary (Injeyan and Tobe, 1981a) are about equal in crowded and isolated
females, because the eggs of the latter are smaller and lighter. Thus, the
number of eggs per pod laid by isolated females is higher at the expense of
egg size and vitellin content per egg. Consequently, hatchlings from eggs laid
by isolated females are smaller and morphometrically different (see also
Section 3.1) from those originating from crowded females (Lauga, 1974,
1976b). The colour differences between isolated and crowded hatchlings (see
Section 3.2.1) are also related to maternal density and/or to the differences in
egg (and hatchling) size (Hunter-Jones, 1958; Papillon, 1960, 1968).
The number of ovarioles constitutes a theoretical upper limit for the
number of eggs in an egg pod, but in practice the latter is markedly lower
because usually a considerable portion of the oocytes are resorbed before
completing development. The proportion of such resorbed oocytes is higher
in crowded than in isolated females; thus, the actual number of eggs per egg
pod in crowded females in even less than that expected due to their fewer
number of ovarioles (Injeyan and Tobe, 1981a). The rate of egg laying
(number of egg pods produced per female per week), the total number of
pods laid during the life span of a female, and proportion of viable eggs (per
cent of eggs which hatch) are also distinctly lower in crowded than in isolated
Locusta (Norris, 1950; Albrecht et al., 1958). Similar differences between
crowded and isolated females also exist in other locusts, although for some of
these reproductive parameters they may be less extreme (Schistocerca:
Norris, 1952; Papillon, 1970; Nomadacris: Albrecht, 1959).
Although the differences in the reproductive potential between crowded
and isolated locusts are well demonstrated, certain factors, related more to
the experimental methods than to real phase characteristics, may contribute
to these differences. Isolated locusts are handled individually in laboratory
cultures and they experience no competition for food or for egg laying space.
It is known, for example, that as the number of egg pods laid into the same
oviposition vessel in the laboratory increases, the viability of the eggs
decreases (Chamberlain, 1980). Also, as isolated locusts are usually kept in
small containers, they may spend less time and energy in searching for
oviposition vessels. These presumably better conditions may reduce the
number of oocytes resorbed, and increase the rate of egg laying, as well as the
24 M. P. PENER
proportion of viable eggs in the isolated locusts. Owing to these better

conditions and/or to real phase differences, the life span of isolated adults is
longer than that of crowded ones (Norris, 1952, 1959; Pener, 1976a; for a
contradicting result see Norris, 1950; and for the experimental difficulties in
comparing the life span of isolated and crowded locusts see Albrecht, 1967,
p. 60). The longer life span of isolated adults may account for the higher total
number of pods produced. On the other hand, it seems unlikely that such
handling-dependent factors play a causal role in the difference of the
ovariole-number in the progeny.
Oocyte development strictly depends on the CA and JH in locusts (L. Joly,
1960; Highnam et al., 1963; Pener, 1965b, 1967a; Strong, 1965; Girardie,
1966; Roussel, 1975d, 1976a,b; Lazarovici and Pener, 1977), as well as in
other acridids (see table IV-2- 1 by Engelmann, 1983). Allatectomy of
sexually mature females results in rapid resorption of the developing oocytes
(Pener, 1965b, 1967a). JH induces vitellogenin production in the fat body
(Chen et al., 1976, 1979; Abu-Hakima, 1981; Wyatt et al., 1987) and mediates
vitellogenin uptake by the developing oocytes (Ferenz et al., 1981). Thus, J H
is necessary to induce and maintain the female’s reproduction implying that
more active CA and/or higher JH titres are responsible for the higher
fecundity of isolated females. In regard to fecundity, therefore, JH may
promote solitary characteristics. The relevant experimental findings should
be examined separately for the so-called ”immediate” and “transmitted”
effects. The former term covers effects on the adult females, whereas the latter
means effects becoming overt in the hatchlings, that is effects “transmitted”
to the progeny.
Considering the “immediate” effects, implantations of two pairs of active
extra CA into crowded adult Locusta females led to increased fecundity; the
number of eggs per pod, rate of egg laying and total number of pods laid
were higher than in the controls (Cassier, 1965a). However, unilateral
allatectomy, or unilateral allatectomy coupled with severance of the allatal
nerve of the remaining gland, in isolated Locusta females reduced these
parameters (Cassier, 1966a,b). Thus, the trends observed after implantation
of extra CA were similar to those induced by isolation, whereas surgical
treatments, presumably reducing JH titres, led to effects similar to those
caused by crowding. However, this parallel may be coincidental and the
results of the endocrine manipulations may be related to the vitellogenetic-
gonadotropic effects of the CA without any phase shift. The life span is
longer in isolated than in crowded adults (see above and also Cassier, 1965a),
but implantation of extra CA, claimed to induce solitary characteristics, also
shortened the life span of the adult females (Cassier, 1965a). Implantations of
three pairs of CA into isolated Locusta females was reported to decrease the
number of eggs per pod, though implantation of 15 pairs led to an increase
(Albrecht and Cassier, 1964). Only the latter finding was included in Cassier’s
(1 970) summary paper. Implantation of extra CA into crowded adult females
of Schistocerca reduced the life span and some of the reproductive para-
meters, but it increased the number of eggs per pod (Cassier and Papillon,
1968). According to Injeyan et al. (1981), high J H titres in both crowded and
isolated Schistocerca females may reduce the viability of the eggs and so
lower the proportion of those which hatch. Furthermore, Albrecht et al.
(1958) found that the relationship between density and reproductive poten-
tial is not simple in Locusta. Females crowded as hoppers then isolated as
adults produced more eggs (c. 1500 eggs per female) than those kept
continuously under isolation (c. 1000 eggs), whereas females isolated as
hoppers then crowded as adults produced even fewer eggs (c. 150) than
continuously crowded ones (c. 300 eggs). In the light of these findings, phase-
dependent “immediate” differences in female fecundity may have a more
complex causal relation than a simple effect exerted solely by adult density on
adult CA activity.
Although CA activity and J H are undoubtedly necessary for oocyte
development in locusts and other acridids (see above), the exact relationships
between these endocrine factors and the quantitative aspects of various
reproductive parameters are not fully understood. Injecting exogenous J H
into allatectomized females of Locusta, LazaroviGi and Pener (1977)
observed that with increasing doses the rate of oviposition increased, but the
number of eggs per pod was unaffected. Couillaud et al. (1984) found that
pre-severance of the allatal nerves (NCAI, or NCAI and 11) drastically
reduced the JH biosynthetic activity of the CA in crowded Locusta, but had
no effect on the rate of growth of the first generation of oocytes. These
authors concluded that the reduced amount of JH produced by the dener-
vated CA is sufficient for normal vitellogenic growth of the oocytes, but
surprisingly in subsequent work (Couillaud et al., 1985) the lower activity of
the denervated CA was found to be correlated with a higher JH titre in the
operated females. The latter finding throws doubts on the interpretation of
Cassier’s (1 966a,b) results; Cassier assumed that unilateral allatectomy and
unilateral allatectomy coupled with severance of the allatal nerve reduce J H
titres. Couillaud et al. (1987) reconfirmed the lower activity of the CA after
pre-severance of the NCAI; despite the very low activity, such glands induced
considerable vitellogenic oocyte growth after being implanted into allatecto-
mized females, though the rate of this growth was somewhat lower than that
obtained after implantation of “control” (without pre-severance of the
NCAI) C k . Assessing JH biosynthetic activity of the CA of isolated and
crowded Schistocerca females, Injeyan and Tobe (1981b) found a substan-
tially higher glacd activity during the first half of the first gonotrophic cycle
and a corresponding earlier appearance of vitellogenin in isolated females;
26 M. P. PENER
nevertheless, the completion of the cycle was delayed in these females in

comparison with crowded ones. Among several feasible explanations of these
results is the possibility that density may alter the responsiveness of the target
tissues (fat body and/or oocytes in this case) to the J H (Injeyan and Tobe,
1981b).
In conclusion, regarding the “immediate” effects of the CA/JH on
reproductive parameters, the evidence is not clear enough conclusively that a
higher activity of the CA and/or an increased J H titre promote the relevant
solitary phase characteristics.
Regarding the “transmitted” effects, Cassier (1965a) found that implan-
tation of extra CA into crowded adult females of Locusta led to lower
weights, a higher proportion of light coloured individuals and a higher
number of ovarioles in hatchling progeny, all solitary characteristics (see
above). Unilateral allatectomy of isolated mothers resulted in an increased
weight of the hatchlings (Cassier, 1966a), and unilateral allatectomy com-
bined with severance of the allatal nerve yielded similar results and also
induced darkening in some hatchlings (Cassier, 1966b). Implantation of
extra CA into crowded Locusta mothers shifted the morphometrics of the
hatchlings to approach those of hatchlings obtained from eggs laid by
isolated females (Lauga, 1977b). Similar implantations also increased the
number of ovarioles in female hatchlings, though this increase was much
smaller than that induced by isolation of the mothers (Lauga, 1976b).
Implantation of extra CA into crowded mothers of Schistocerca resulted in a
decrease of weight and in a shift toward a green hatchling colour (Cassier and
Papillon, 1968). On the other hand, Injeyan et al. (1979) reported that
exogenous J H treatment of the eggs obtained from crowded Schistocerca
females caused disturbances in embryogenesis and hatching, but did not
induce solitary characteristics in the hatchlings.
Although the evidence that the CA and J H promote solitary characteristics
seems firmer for the “transmitted” than for the “immediate” effects, the
complex relationship between CA activity and haemolymph J H titres after
surgical manipulations (cf. Couillaud et al., 1985) prevents clear conclusions
being drawn. Also, as already outlined by Cassier (1965a) and Lauga
(1976b), differences in CA activity and/or J H titres may exert effects on other
endocrine organs and these may also affect phase characteristics.
3.4 HOPPER DEVELOPMENT
In Schistocerca and Nomadacris, as well as in some non-locust acridids, a

stripe is present in the compound eye of the first-instar hoppers and at each
consecutive moult an additional stripe appears at the anterior margin of the
eye, while the earlier stripe(s) move(s) backwards (see Uvarov, 1966; and
references therein). Thus, the number of eye stripes in an adult (usually six or
seven in Schistocerca and seven or eight in Nomadacris) is equal to the
number of instars, including the adult instar itself, in the life history of that
adult. Actual observations on the number of moults (mostly in the labora-
tory), or just counts of the number of eye stripes (mostly in field popula-
tions), revealed that in isolated laboratory breedings, or in solitary field
populations, Schistocerca and Nomadacris tend to add an “extra” nymphal
instar, thus they usually moult once more than conspecific crowded or
gregarious locusts (Burnett, 1951; Albrecht, 1955; and references therein).
Albrecht (1955) concluded that in these two species, the density of the
parents by affecting the weight and size of the hatchlings determined the
number of nymphal instars in the progeny. Hatchlings originating from eggs
laid by isolated mothers are smaller (see Section 3.3.3), and subsequently
they undergo an extra nymphal instar. Although the correlation between
hatchling size and the extra instar is clear, some findings of Injeyan and Tobe
(198la) indicate that the hopper density experienced after hatching may also
affect the number of instars. Isolating hatchlings obtained from eggs laid by
crowded Schistocerca mothers, these authors observed that about 25% of the
nymphs underwent an extra moult, that is an extra instar. In consecutive
generations of isolated Schistocerca, the proportion of locusts exhibiting the
extra nymphal instar increased to c. 90%, but failed to reach 100% within six
generations. Isolated females showed the extra nymphal stage more fre-
quently than did isolated males (Injeyan and Tobe, 1981a).
Moulting and metamorphosis are controlled by hormonal factors and the
difference in the number of instars between solitary and gregarious locusts
may reflect a somewhat different programming of related endocrine events.
Owing to the extra instar, the metamorphosis of the solitary locusts may be
regarded as retarded and the state of the solitary adult as somewhat
neotenous; these considerations led to the assumption that higher JH titres
may be responsible for the extra nymphal instar in solitary locusts (Kennedy,
1956). However, there is no solid experimental evidence to support this
theory. Although JH biosynthetic activity in the CA was found to be
somewhat higher in isolated than in crowded penultimate and last-instar
hoppers of Schistocerca (Injeyan and Tobe, 1981b), this fact itself does not
demonstrate a causal role of the JH in the induction of the extra nymphal
instar. In many acridids that do not show phase polymorphism, the number
of instars is subject to individual variations. In some instances the larger
females have one instar more than the smaller males, and in phylogenetically
more advanced groups and/or in groups having a smaller size the number of
nymphal instars is fewer (cf. Uvarov, 1966, pp. 286289). However, there is
no evidence which relates these differences to the overall differences in CA
28 M. P. P E N E R
activity or in JH titres. Furthermore, the case of Locusta indicates that there

may be no relationship between a higher J H titre and an extra nymphal
instar, or if such relationship exists, it cannot be easily reconciled with the
green-colour inducing effect of the J H (see Section 3.2.1). Both crowded and
isolated Locusta undergo five nymphal instars. However, an extra nymphal
instar can be obtained by isolating both mothers and offspring and keeping
the offspring under low humidity; neither isolated hoppers originating from
crowded mothers (even kept under low humidity) nor isolated hoppers kept
under high humidity (even if they originate from isolated mothers) exhibit
this extra instar frequently (Albrecht, 1965). But because of the low humidity
experienced by the offspring, the hoppers which undergo the extra instar are
all “brown”; high humidity, which induces green colour in isolated hoppers
(see Section 3.2. l), actually prevents (!) the extra instar. The assumption that
a higher J H titre is responsible for the extra instar in these “brown” isolated
hoppers seems to contradict the green-colour promoting effect of JH. Since
the latter is amply demonstrated (see Section 3.2. l), one has to assume either
that there is no causal relation between the higher JH titre and the extra
instar, or that environmental humidity alters the response of the integument
to J H (cf. discussion by Pener, 1976b) so drastically that the higher titre
which induces the extra moult is insufficient to induce green colour under low
humidity, whereas the lower titre which prevents the extra moult under high
humidity is sufficient to d o so.
3.5 PHYSIOLOGY, BIOCHEMISTRY AND MOLECULAR BIOLOGY
The rate of oxygen consumption is higher in crowded than in isolated

Locusta (Butler and Innes, 1936; Blackith and Howden, 1961; Roussel,
1963a) and Schistocerca (Gardiner, 1958; Pener, 1965a), though in first-
instar hoppers this difference is not always clear. Chauvin (1941) found that
the amplitude of the respiratory movements was higher in crowded than in
isolated Schistocerca hoppers. Allatectomy reduced 0, consumption in
crowded adult females of Locusta independently of ovarian development
(Roussel, 1963b), thus the effect of allatectomy was somewhat parallel to that
of isolation. Implantation of extra CA into crowded hoppers of Locusta did
not alter the rate of 0, consumption, in spite of inducing a green solitary
colour (Roussel, 1963a). Thus, for 0, consumption, either the CA promote a
gregarious characteristic, or at least phase-dependent differences in 0,
consumption are not affected by the CA.
The life span of isolated adults is longer than that of crowded ones (see
Section 3.3.3). Allatectomy drastically increases the longevity of adult locusts
(Wajc and Pener, 1969; Pener, 1972). This effect of allatectomy is clear in
both isolated and crowded Locusta adults, whereas implantation of extra CA

results in a slight decrease of the adult life span under both conditions of
density (Pener, 1976a). In this case, therefore, J H deficiency (allatectomy)
seems to promote a solitary characteristic (longer life span). However,
although both allatectomy and isolation shift the life span in the same
direction, the operation induces a much larger shift than the change in
density (cf. Pener, 1976a).
In the last two hopper instars and in the adult, heartbeat frequency is
higher in isolated than in crowded Locustu (Roussel, 1972a,b, 1973, 1975a;
Queinnec, 1973). Allatectomy decreased heartbeat frequency under both
conditions of density, but allatectomized isolated locusts exhibited a higher
rate than allatectomized crowded ones; in fact, the relative difference was
even more marked in allatectomized than in normal locusts, because the
decrease induced by allatectomy was smaller in isolated insects (Roussel,
1975b,c). Thus, although CA and J H affect heartbeat frequency, they do not
seem to be responsible for the relevant phase difference, and Roussel(1975c)
concluded that the target organ, presumably the heart itself, of isolated and
crowded locusts may respond differentially to JH.
Investigating some biochemical parameters in crowded and isolated fifth-
instar hoppers of Locusta and Locustana, Matthee (1945) found no signifi-
cant density-dependent differences in lactic acid content per wet body weight,
but observed a higher uric acid content of the haemolymph in isolated
hoppers of both species. The p H of the haemolymph, measured only in
Locusta, did not differ significantly between isolated and crowded hoppers.
However, the fat content of the body was significantly higher in crowded
hoppers of both species. Blackith and Howden (1961) also found a higher fat
content in hatchlings originating from eggs laid by crowded females of
Locusta, Schistocerca and Nomaducris than in those originating from conspe-
cific isolated females. These results on the fat content may be related by some
circumstantial evidence to the CA; allatectomy leads to an increase of fat
content in adult male locusts (Odhiambo, 1966b; Strong, 1968), thus the
effects of crowding and allatectomy-induced JH-deficiency on fat content are
somewhat parallel. However, this parallel may be coincidental because
gregarious locusts are more active than solitary ones, but allatectomy seems
to reduce locomotor activity (see Section 3.7.2) and the effect of allatectomy
on fat content may be explained by an accumulation of non-utilized fat. No
data are available on the effect(s) of CA on fat content in isolated locusts.
Marty et al. (1972) found some differences in haemolymph proteins
between crowded and isolated albino mutants of Locustu. Nolte (1977)
recorded that the cyclic AMP content of the testis is lower in isolated than in
crowded fifth-instar hoppers and young adults of Locusta.
30 M. P. P E N E R
Genin et al. (1986) have shown that there are differences in cuticular
hydrocarbons between crowded and isolated Locusta. In a subsequent paper
(Genin et al., 1987), phase-dependent differences were also found in the
aliphatic ethers of the cuticular waxes in the same species. Possible endocrine
effects on these differences, however, have not been investigated.
Recently, Colgan (1987) has studied developmental changes of isoen-
zymes, mostly associated with glycolysis, in Locusta. Offspring of crowded
mothers were either isolated, or placed in a small crowd, less than an hour
after hatching, and the effect of hopper density was investigated on six
enzymes. In spite of limited developmental stages (first two nymphal instars)
and a limited period (only 14 days) during which the hoppers experienced the
different densities in these experiments, there were two major findings: (1) the
aldolase phenotype found in hatchlings and in crowded hoppers was replaced
by a novel isoenzyme in the isolated hoppers; and (2) the levels of two
glycerol-3-phosphate dehydrogenase isoenzymes were higher in the isolated
than in the crowded hoppers. Feeding of young crowded hoppers on JH1
solution, or injection of JH1, failed to induce the appearance of the novel
aldolase isoenzyme which was found to be induced by isolation. These
experiments (Colgan, 1987) are the first efforts to investigate phase polymor-
phism at a molecular level, presumabIy reflecting changes in the underlying
gene expression.
3.6 CYTOLOGY
One or two supernumerary chromosomes, termed B chromosomes, are often

present in Locusta (Lespinasse, 1973, 1977). The proportion of locusts with
such B chromosomes is different in different geographical strains of the
species and is subject to selection within the same strain (Lespinasse and
Nicolas, 1975, 1981). However, daily repeated 1-min exposure to CO,
promotes solitary characteristics in crowded Locusta (review by Fuzeau-
Braesch and Nicolas, 1981). Correlating these phenomena, Lespinasse and
Nicolas (1975, 1981) found that the higher the B chromosome frequency in
different geographical strains or in selected laboratory populations of the
same strain, the more intense was the “solitarizing” effect of the CO,. These
authors suggested that races or populations with higher B chromosome
frequency have a greater flexibility for phase change.
Nolte (1964a,b, 1967, 1968, 1974, and some of his other publications)
reported that in Locusta, Locustana and Schistocerca chiasma frequency is
higher in gregarious than in solitary field populations; in the laboratory
crowding increases, whereas isolation decreases, chiasma frequency. How-
ever, Dearn (1974a,b) found no evidence that there is any relationship
between phase status, or density, and chiasma frequency in Schistocerca and

Locusta and strongly criticized Nolte’s methods and findings. This debate is
still open, but it may be added that Nolte (1967, 1968) regarded albino
locusts as an extreme solitary phase, because they d o not have gregarious
black patterns (see Section 3.2.1) and show low chiasma frequency largely
unaffected by density. Although chiasma frequency is indeed low in albino
strains of Schistocerca and Locusta (Dearn, 1977) and obviously (by the
definition of the term “albino”) they do not have black patterns even when
crowded, these albinos do exhibit density-dependent changes in other phase
characteristics (Pener, 1965a; Dearn, 1977) and so they cannot be considered
as extreme solitary locusts unresponsive to density.
Except for a claim by Nolte (1968) that injection of haemolymph from
crowded to isolated hoppers increased chiasma frequency, nothing is known
about possible endocrine effects on cytological phase characteristics, nor
about relations between such phase characteristics and endocrine events.
3.7 BEHAVIOUR AND ACTIVITY
3.7.1 Hoppers
When locust populations reach high densities in the field, the hoppers form
large groups, termed “bands”. The individual hoppers within the band
exhibit more or less synchronous activities and they show positive reactions
to one another, that is they actively aggregate (Ellis and Ashall, 1957; review
by Uvarov, 1977). In the laboratory, experimental parameters reflecting the
tendency to aggregate, such as proportion of locusts forming groups or the
per cent of time spent in groups, were much higher for hoppers which had
been kept under crowded conditions than for those which had been main-
tained under isolation (Ellis, 1959, 1962a,b; and references therein); in the
latter case, the values of these parameters did not exceed those expected by
random distribution. It was also discovered that group formation strongly
depends on an habituation to “being touched”, which is acquired by
crowded hoppers a day or two after hatching and “learned” by isolated ones
after being placed into a crowd (Ellis, 1962a,b, 1963a,b; Ellis and Pearce,
1962). Experimentally induced “training” in aggregation enhanced aggrega-
tion behaviour in previously isolated Locusta hoppers and 4 h of such
training increased the aggregation behaviour of isolated Schistocerca hop-
pers to the level observed in continuously crowded ones (Ellis, 1963b). Thus,
a change in behaviour leading to active aggregation is apparently the first
phase characteristic to be affected by crowding.
32 M. P. PENER
The most characteristic and impressive activity of a hopper band in the

field is marching (Uvarov, 1977). The general impression created by a
marching band is that all hoppers are moving all the time in the same
direction; but detailed data (Ellis and Ashall, 1957; Stower, 1963) reveal that
only a portion of the hoppers show actual displacement at any given time, an
individual hopper often halts, and the direction of the displacement of
different individuals or of small groups within the band is not necessarily
parallel. The aggregation behaviour of the marching hoppers presumably
keeps the band coherent; hoppers advancing beyond the edge of the band
were frequently observed to turn back and rejoin the main bulk (Ellis and
Ashall, 1957; Stower, 1963; for further references see Uvarov, 1977).
Marching can be induced and studied in the laboratory where crowded
hoppers march around the floor of the cage in circles (Ellis, 1950, 1951).
Isolated hoppers placed among crowded ones, or into a newly formed crowd,
also march, but they spend much less time marching and march more slowly
than crowded hoppers (Ellis, 1950, 1951). Crowding of previously isolated
hoppers leads to an increase of marching behaviour within 24 h, which may
be related to the habituation to “being touched” and to the induction of
active aggregation behaviour (see above); however, a longer period of
crowding, 15-16 days, is needed to bring the intensity of marching behaviour
of these hoppers to the level shown by continuously crowded ones (Ellis,
1964). This long-term effect may be related to slower physiological adap-
tations to the high activity needed for fully intense marching. In any case,
locomotor activity is much higher in gregarious than in solitary hoppers.
Carlisle and Ellis (1963) reported that injections of ventral ( = prothoracic)
gland extracts temporarily reduced the marching activity of Locusta hoppers.
Haskell and Moorhouse (1963) bathed ventral nerve cord preparations of
crowded Schistocerca adults in the haemolymph of fifth-instar hoppers and
observed by electrophysiological techniques that haemolymph taken within
12 h of the moult, or at actual ecdysis, reversibly depressed the activity of
metathoracic motor neurons, but enhanced interneuron activity in the
ventral nerve cord. Haemolymph taken from hoppers in the mid-intermoult
period had no such effects. These findings were correlated with the fact that
the locomotor activities of hoppers are low close to the ecdysis, but high in
the intermoult period. An extract from Bombyx pupae containing ecdysone
and 20-hydroxyecdysone induced effects similar to those observed with
hopper haemolymph taken about the time of the moult. Haskell and
Moorhouse (1963) suggested that the effects are due to ecdysteroids, whose
level was then assumed to be high at ecdysis. This explanation, however, is
not consistent with more recent findings which clearly and uniformly show
that body or haemolymph ecdysteroid levels of locust hoppers are high at
about two-thirds to four-fifths of the intermoult period, but practically nil
close to the actual moult (Wilson and Morgan, 1978; Hirn et al., 1979; Baehr
et ul., 1979; Gande et al., 1979). Thus, the effects reported by Haskell and
Moorhouse (1963) may not be caused by ecdysteroids, but by some other
factor(s) in the haemolymph of moulting or close-to-moult hoppers. It is
more difficult to explain the results obtained with the Bombyx extract, but the
authors themselves pointed out that the minimum effective dose was very
high and the extract was impure. It is possible, therefore, that some
impurities caused the effects, or that the presumably very high concentration
of ecdysteroids induced some coinciding pharmacological effects.
3.7.2 Adults
The final moult within a hopper band in the field is usually more or less
synchronized and the resulting adults remain together, now forming a
“swarm” (see Uvarov, 1977). Locusts in a swarm show active grouping or
aggregation behaviour, best demonstrated in field studies on migratory
flights (see below). Crowded adult locusts also show aggregation behaviour
in the laboratory (Gillett, 1972) and the parameters reflecting the intensity of
this behaviour are higher for crowded than for isolated adults (Gillett, 1973).
Norris (1963, 1970) reported that crowded Schistocerca females exhibit a
clear group behaviour in egg laying which may be related to a pheromonal
factor. Nothing is known about possible endocrine influences on the aggrega-
tion behaviour of adult locusts.
A major behavioural difference between solitary and gregarious adult
locusts in the field is the migratory group flights of the latter. Extensive
studies on Schistocerca (Rainey, 1963, 1976; and references therein; Waloff,
1972; review by Uvarov, 1977) revealed that the actual displacement of a
flying locust swarm depends mainly on atmospheric air currents, but active
aggregation behaviour of the locusts is a major factor keeping the swarm
coherent. Smaller groups or “streams” of locusts within the swarm fly
together in the same direction, but different streams are oriented to different
directions, so the orientation of the individual locusts in different parts of the
swarm may be effectively random and not parallel to the direction of the
displacement of the whole swarm. However, when a stream of locusts flies, or
is carried away by local air turbulances, beyond the edge of the swarm, the
insects change orientation and fly back into the swarm. It may be recalled
that hoppers in bands show a somewhat similar behaviour (see Section 3.7.1).
Because of the intense migratory flights, gregarious adults are considered to
be more active than solitary ones, though the latter may also make quite long
individual flights by night (see Uvarov, 1977, p. 74). Laboratory studies on
flight performance of Schistocerca confirmed that crowded adults fly much
34 M .P. PENER
more intensely than isolated ones (Michel, 1970a,b, 1980a,b); thus, in

relation to flight the former are indeed more active than the latter.
The results and conclusions of numerous studies on the effects of the CA
or JH on locust flight activity (Wajc and Pener, 1971; Goldsworthy et al.,
1972; Michel, 1973a; Wajc, 1973; Lee and Goldsworthy, 1975, 1976; Kutsch,
1983) were recently summarized (table 2 by Pener, 1985), and discussed
together with some unpublished data. This discussion (Pener, 1985) reveals
that the experimental results are controversial and cannot be amalgamated
into a decisive picture. Different authors employed different conditions and
experimental parameters for measuring flight activity, and these differences
may well contribute to the apparent conflicts. However, the controversy itself
indicates that the CA or JH probably do not play a cardinal regulatory role
in locust flight, though minor effects, some of them possibly mediated by
differential physiological ageing of allatectomized and control locusts (cf.
Lee and Goldsworthy, 1975), may not be excluded. Allatectomy of adult
Schistocerca males was reported to reduce spontaneous locomotor activity
(Odhiambo, 1965, 1966~).However, allatectomy leads to a complete absence
of male sexual behaviour in this species (Pener, 1986; and many references
therein) and the reduced “spontaneous locomotor activity” may be
explained, at least partially, by the lack of some movements which are related
to sexual behaviour but not recognized as such, for example searching
movements of the male for finding a female. Nevertheless, some data indicate
that allatectomized males are rather sluggish (Wajc and Pener, 1969) and that
the CA exert a stimulatory effect on the excitability of locusts (Cassier, 1963,
1964a,b, 1965b). If the questionable conclusion that CA and J H stimulate
flight and/or locomotor activity and/or excitability of adult locusts is
accepted, it would be in accord with a higher activity of the glands and/or
higher JH titres in the more active gregarious or crowded locusts.
Michel (1972a) implanted ventral glands (VG), taken from 5-day-old
isolated adults of Schistocerca into 20-day-old crowded ones and observed a
considerable but temporary decrease in flight activity of the recipients.
Similar implantations of presumably degenerating VG taken from 5-day-old
crowded adult donors have less effect, or no effect at all. From these results
Michel (1972a) concluded that the VG exert an inhibitory effect on locust
flight activity and suggested that the persistence of the VG in isolated adults
(cf. Carlisle and Ellis, 1959; Cassier and Fain-Maurel, 1969a) may be
responsible for their reduced flight activity. In the light of the controversial
results in different studies on the effect of the CA on locust flight and related
methodological problems (see above), this single report on the effect of the
V G on flight activity requires independent confirmation.
Michel and Bernard (1973) reported that electrocoagulation of the pars
intercerebralis (PI), including the median neurosecretory cells (MNSC),
drastically reduced flight duration in Schistocerca males, but implantation of

the PI, or of whole brains, did not improve flight. In contrast, Goldsworthy
et al. (1973) found no effect on flight performance after electrocoagulating
the PI-MNSC in mature (18-25-day-old) Locusta males. In a later study,
Goldsworthy et al. (1977) observed that electrocoagulation of the PI-MNSC
of newly fledged (I-day-old) Locusta males moderately reduced flight per-
formance tested on day 19 and administration of a synthetic JH to the PI-
coagulated locusts partially restored flight performance. These authors
suggested, therefore, that the PI-MNSC most likely affect flight activity by an
activatory effect on the CA. Such an overall activating effect of the PI on the
CA is well demonstrated in locusts (see Section 4.3). Goldsworthy et al.
(1977) also observed that electrocoagulation of parts of the brain in the
immediate lateral vicinity of the MNSC reduced flight performance more
drastically than did electrocoagulation of the median area presumably
comprising only the-MNSC. In conclusion, there is no clear evidence that a
neurohormonal factor originating from the MNSC is directly involved in the
regulation of locust flight activity. Recently, Diederen et al. (1988) found that
during a single l-h period of flight, stainable neurosecretory material and
label originating from injection of radioactive amino acids, both increased in
the PI and storage lobes of the corpora cardiaca (CC) of crowded Locusta. In
contrast, Highnam and Haskell (1964) reported that daily repeated flight
induced/enhanced release of stainable neurosecretory material from the
MNSC and CC, and led to an increase of CA volume and oocyte growth in
crowded and isolated Schistocerca and in crowded Locusta, but not in
isolated adults of the latter species.
Michel (1972b, 1973b) claimed that the storage lobes ( = neurohaemal
part) of the CC promote sustained flight, whereas the glandular lobes do not
affect flight in Schistocerca. The former part of this claim has not received
decisive confirmation, and circumstantial evidence (cf. Diederen et al., 1988)
may indicate that it is not valid, at least in Locusta, whereas the latter part
was decisively disproved and amply criticized (see Mordue and Goldsworthy,
1974; and references therein). The glandular lobes of the CC were found to
exert a crucial effect on locust flight (Goldsworthy et al., 1972, 1973; Jutsum
and Goldsworthy, 1977); these lobes produce adipokinetic hormones (AKH)
in locusts (reviews by Stone and Mordue, 1980; Goldsworthy, 1983;
Beenakkers et al., 1985a,b; Orchard, 1987), which control the major meta-
bolic events necessary to provide fuel and energy for sustained flight.
Presently three AKHs and their chemical structure are known from locusts,
AKHI from both Locusta and Schistocerca, AKHII of Schistocerca, and
AKHII of Locusta, the latter two differing only by one amino acid (Siegert et
al., 1985; see also Orchard, 1987). All of them belong to a “family” of insect
and crustacean small peptide neurohormones with similarities in their
36 M. P. PENER
chemical characteristics. The vast literature on AKH cannot be reviewed

here; detailed studies, especially with AKHI, revealed that the hormone
promotes formation and release of diacylglycerol from the fat body, activates
glycogen phosphorylase in the fat body, induces marked hyperlipaemia in the
haemolymph, changes the lipophorin profile of the haemolymph resulting in
a much improved lipid transport and stimulates diacylglycerol oxidation in
the flight muscles (see reviews above).
In conclusion, all major endocrine organs have been claimed to affect
locust flight activity. However, the only thoroughly investigated and unequi-
vocal effects are those of the glandular lobes of the CC and of AKHs secreted
by them. In the light of this fact, and of 20 years of intensive related research,
it is astonishing that nothing is known about AKH in isolated locusts!
Possible differences in AKH production, AKH content of the CC, rate of
AKH release and haemolymph titre, as well as possible differences in
adipokinetic responses (that is the response of the target systems to AKH),
may well be responsible, or may contribute, to the differences in flight activity
between crowded and isolated locusts, but this subject has not been investi-
gated.
Besides its other functions as a neurotransmitter and a neuromodulator in
insects, including locusts (see Evans, 1982), octopainine may exert a general
excitatory effect (Orchard, 1982). Rough handling and other irritations
(Orchard et al., 1981), or flight (Goosey and Candy, 1980) quickly elevate
haemolyniph octopamine levels, and it seems that the octopamine induces
some rapid adipokinetic-like responses which occur mostly or partially
before the AKH-induced slower and more prolonged adipokinetic responses
take place (Orchard et al., 1981, 1982; Orchard and Lange, 1983, 1984;
review by Orchard, 1987). Octopamine may also stimulate the process of
oxidation in the flight muscles (see Goldsworthy, 1983). Fuzeau-Braesch and
David (1978), Fuzeau-Braesch et al. (1979) and Benichou-Redouane and
Fuzeau-Braesch (1982) reported that the octopamine content of whole heads
and of various components of the nervous system is higher in isolated than in
crowded fifth-instar hoppers and adults of Locusta. Treatment of crowded
locusts with CO,, which induces “solitarizing” effects, increased octopamine
content to the level found in isolated ones (see also Fuzeau-Braesch and
Nicolas, 1981). In contrast, Morton and Evans (1983) obtained no dif-
ferences in octopamine levels of nervous tissue, muscles, or whole heads
between crowded and isolated Schistocerca adults. These authors strongly
criticized the work of Fuzeau-Braesch and David (19’78) and of Fuzeau-
Braesch et al. (1979), and in relation to the controversy between their results
and those of Benichou-Redouane and Fuzeau-Braesch (1982), they implied
that the differences may be related to high individual variations; they also
cited the opinion of Fuzeau-Braesch and David, as a personal communica-

tion, that the differences in the results are likely to be due to differences in
methodology and/or in the species of locusts used.
Octopamine receptors in the brain were reported to be less sensitive in
isolated than in crowded Locusta (David and Fuzeau-Braesch, 1979).
Dopamine content was found to be about five times higher in crowded
than in isolated Locusta, but no significant differences were found in
noradrenaline content (Fuzeau-Braesch, 1977a,b).
4 Endocrine organs, hormones and their role in phase

transformation
4.1 THE CORPORA ALLATA A N D JUVENILE HORMONE
Staal(l961) reported that the volume of the CA is larger in isolated than in

crowded adults of Locusta, except in adult males kept under low humidity.
However, the results of Staal (1961, appendix 1) also showed a marked
interaction between density and humidity; in crowded locusts the humidity
had little effect on the volume of the CA, whereas in isolated ones high
humidity led to a considerable increase in gland volume. In another
experiment of the same study, CA volumes measured in the fifth instar were
found to be larger in hoppers which had been kept isolated from the later
part of the third instar than in those which had been maintained conti-
nuously under conditions of crowding. Thus, differences in density exper-
ienced during one (the fourth) instar were sufficient to affect gland volume.
Highnam and Haskell (1964) studied CA volume and its increase during
the sexual maturation of adult female locusts under various experimental
conditions. These authors found that the maximum volume of the CA, as
related to oocyte length, was quite similar in isolated flown and unflown and
in crowded flown females of Locusta kept without males. However, the major
increase in gland volume occurred at a smaller oocyte length in the crowded
flown females than in the isolated (flown or unflown) ones. The steepest
increase in this species was observed in unflown crowded females kept
without males, and maximum gland volumes in this group greatly exceeded
those in the other three groups. Thus, again an interaction was found, in this
case between the effects of density and flight (=intense locomotor activity)
on CA volume. The results obtained by Highnam and Haskell (1964) in
Schistocerca were somewhat different. In adult females kept without males,
the maximum volumes of the CA were quite similar in unflown isolated,
flown isolated and unflown crowded locusts and a little smaller in flown
crowded ones, but the increase in gland volume was steeper in the crowded
38 M. P. PENER
than the isolated females. The highest gland volumes and steepest increase
were found in crowded females kept with mature males producing matu-
ration-accelerating pheromone (see Section 3.3.1); such females also showed
the shortest period of sexual maturation. Regardless of density and flight,
maximum volume of the CA in adult Schistocerca females coincided with 4-
6 mm length of the proximal oocytes.
Measuring CA volume in the penultimate and last-instar female hoppers
and in adult females of Schistocerca, Injeyan and Tobe (1981b) recorded
consistently larger volumes in isolated than in crowded locusts. These
findings somewhat differ from those of Highnam and Haskell (see above),
but direct comparison may not be justified because the isolated locusts of
Injeyan and Tobe were reared for two or more generations under strict
isolation and all exhibited an extra hopper instar (see Section 3.4), whereas
Highnam and Haskell separated their locusts from a crowded stock only at
the moult to adult.
Dale and Tobe (1986) found larger CA volumes in isolated than in
crowded adult females of Locusta during the first 8 days after fledging.
Considering that sexual maturation is quicker in isolated than in crowded
Locusta adults (see Section 3.3. l), these results correlate well with density-
dependent differences in maturation time. Unfortunately: these authors did
not report on CA volumes in older females and it is probable that the
experiments were stopped before the CA of the belatedly maturing crowded
females completed growth. Thus, it cannot be decided whether maximum
gland volumes, or only the rate of increase in gland volumes were different
between the crowded and isolated locusts.
Altogether, it seems that CA volume is larger in isolated than in crowded
locusts. However, this conclusion is obscured by non-density-dependent
effects (humidity, flight) on the volume of the glands. Also, except for the
results of Injeyan and Tobe (1981b) in Schistocerca females, the various
findings in adult locusts may reflect density-dependent changes in the rate of
sexual maturation, rather than an effect of density on CA volumes per se.
Finally, it must be kept in mind that differences in CA volume do not
necessarily parallel differences in gland activity (see Feyereisen, 1985; Tobe
and Stay, 1985).
Injeyan and Tobe (1981b) reported that JH biosynthetic activity of the
CA, assessed by radiochemical assay in vitro (for details and references in
relation to this technique see Tobe and Stay, 1985), was higher in isolated
than in crowded penultimate and last-instar female hoppers of Schistocerca.
In the same study, the activity of the CA was found to be slightly lower in
crowded than in isolated adult Schistocerca females, but major differences
were temporal; the isolated locusts exhibited relatively higher rates of J H
synthesis earlier in the first gonotrophic cycle. This earlier activity of the CA
correlated well with a shorter period from fledgling to first appearance of the
vitellogenic oocytes in the isolated females. However, in spite of the initially
higher gland activity, vitellogenic oocyte development was slower in the
isolated females, and eventually the crowded females completed the first
gonotrophic cycle earlier than the isolated ones. JH biosynthetic activity of
the CA was similar in crowded and isolated adult Locusta females within the
first 5-6 days after fledging, but on day 8 gland activity was much higher in
the isolated locusts (Dale and Tobe, 1986). As no data were presented for
older females, the difference found in the 8-day-old females may be related to
the shorter maturation time of isolated Locusta adults. Recently, Dale and
Tobe (1988) found that addition of the calcium ionophore A23187 to the
medium significantly increased in vitro J H biosynthetic activity and/or
release in CA taken from 3-, 5- and 8-day-old adult crowded Locusta females.
A23187 had a similar effect on glands of isolated females, but the increase
was not statistically significant at any of these ages. These results constitute
an additional CA and J H related difference between crowded and isolated
adults. As one possible and/or partial explanation of these findings, the
authors suggested that incubation in the ionophore resulted in a significant
elevation in JH I11 production rates by CA of crowded locusts only because
“initial” rates, that is without the ionophore, were lower in these locusts.
Again, no females older than 8 days were investigated.
Employing the Galleria bioassay, L. Joly and P. Joly (1974) and L. Joly et
al. (1977) found higher haemolymph JH titres in isolated than in crowded
fourth- and fifth-instar hoppers of Locusta. These authors have also observed
that in isolated young Locusta adults J H titres increased much more rapidly
with age than in crowded ones, but detailed inspection of their text and tables
reveals that maximum values were only slightly higher in the isolated locusts.
Using the more reliable method of gas chromatography-mass spectrometry,
Dale and Tobe (1986) found low J H 111 titres in I-day-old adult Locusta
females and no differences between isolated and crowded locusts at this age.
The titres were much higher on day 4, and the increase was approximately
twice as great in isolated than in crowded females. Lack of data for older
females again prevents a determination of whether the latter result reflects a
genuinely higher titre in the isolated locusts, or just an earlier increase of the
titre in correlation with their earlier sexual maturation. Fuzeau-Braesch et al.
(1982) assessed JH titres in last-instar hoppers and adults of Locusta,
comparing crowded, isolated green, isolated homochrome (light coloured),
and artificially “solitarized” (by CO,, cf. Fuzeau-Braesch and Nicolas, 1981)
locusts. Except for higher J H 111titres in the artificially “solitarized” (= CO,
treated) locusts, no clear differences were found; thus, these authors con-
cluded that their results do not confirm the assumption that isolated locusts
have higher J H titres, and consequently differences in JH titres may not be a
40 M. P. PENER
primary cause of locust phase transformation. However, Fuzeau-Braesch et

al. (1982) employed a radioimmunoassay for assessing J H titres, the accuracy
of which is subject to criticism (cf. Granger and Goodman, 1983; Tobe and
Stay, 1985). Also, Fuzeau-Braesch et al. (1982) claimed to find J H I and J H I1
in their locusts, but when more reliable physicochemical methods are
employed, no J H I or I1 can be detected in Locusta (Huibregtse-Minderhoud
et al., 1980; Bergot et al., 1981; Pener et al., 1986), or in other orthopteroid
insects (Loher et al., 1983). In fact, occurrence of JH I, I1 or 0 has been
demonstrated convincingly only in Lepidoptera (Schooley et al., 1984). Thus,
the results of Fuzeau-Braesch et al. (1982) may not be accepted without
doubts.
Judging all the available data, it seems that CA activity and J H titres are
higher in isolated than in crowded locusts, but this conclusion is still open to
some doubts, especially in relation to adults. As already outlined (see above
and Section 3.3.1), sexual maturation is quicker in isolated than in crowded
Locusta adults and JH is necessary for this maturation. The higher CA
activity and higher JH titres in isolated as compared to those in crowded
Locusta adults of the same chronological age ( = equal number of days after
fledging) found by L. Joly and P. Joly (1974), L. Joly et al. (1977) and Dale
and Tobe (1986, 1988), may just reflect an earlier increase of gland activity
and of hormone titres in the isolated locusts. Thus, for a more meaningful
comparison of isolated and crowded adults, CA activity and/or J H titres may
be related not to chronological age but rather to physiological events, such as
per cent of increase in oocyte length, during at least the whole first
gonotrophic cycle, and preferably during several consecutive cycles. Unfor-
tunately, no such data are available for Locusta adults. The more compre-
hensive data of Injeyan and Tobe (1981b) on Schistocerca indicate that the
differences in CA activity between isolated and crowded adult females are
mostly temporal.
Even if we accept without restrictions that CA activity and J H titres are
higher in isolated than in crowded locusts, such differences do not necessarily
prove a primary causal role of CA/JH in phase change. Table 1, summarizing
the effects of CA/JH on phase characteristics, clearly shows that CA/JH
promote solitary features in many instances, but promote gregarious
features, or do not exert a relevant effect, in many others. Also, in some
instances, an effect assumed to be exerted on phase may have alternative
interpretations (see for example “E/F morphometric ratio” in Table 1).
Moreover, as already outlined (Pener, 1976a,b, 1983, 1985; Roussel, 197%;
Injeyan and Tobe, 1981b; Hardie and Lees, 1985), the response of various
target organs to J H may be different in isolated and crowded locusts (see for
example “yellow colour in adults” in Table 1).
TABLE I Effects of the CA and/or JH on locust phase characteristics. Phase characteristics, for which no experimental findings nor
circumstantial evidence are available in relation to an effect of CA/JH, are not included in the table
Phase characteristics In relation to the given phase characteristic, the Remarks, notes, doubts; Details and
investigated (in parentheses: CA/JH* see text for details references
difference between phases") are given in
section
Promote Promote Do not exert
solitary gregarious an effect, or
feature(s) feature(s) the effect is
not clear
1 . E/F morphometric ratio + Effect may be related to 3.1

(higher in G) disturbed metamorphosis
2. F/C morphometric ratio +? +? Different authors draw 3.1
(higher in S) somewhat different
conclusions
3. Shape of pronotum + 3.1
(convex in S, straight or
concave in G)
4. Sternal hairs (longer in G) + Effect may be related to 3.1
disturbed metamorphosis
5. Thickness and number of -c Effect may be related to
gland cells in epidermis of disturbed metamorphosis
adult male (more
numerous in G)
6. Green colour (absent in + Green colour is not a 3.2.1-2-3
G, may be present in S) necessary characteristic of
the solitary phase, effect is
not restricted to locust
phase polymorphism
TABLE 1 Continued
Phase characteristics In relation to the given phase characteristic, the Remarks, notes, doubts; Details and
investigated (in parentheses: CA/JHb see text for details references
difference between phasesa) are given in
section
Promote Promote Do not exert
solitary gregarious an effect, or
feature(s) feature(s) the effect is
not clear
7. “Homochrome” + CA/JH induce green colour 3.2.1

colouration (absent in G, in homochrome hoppers,
may be present in S) thus shift one solitary
characteristic to another
8. Black patterns in hoppers +? Effect may be due to green 3.2.1
(present in G, absent in S colour induction, or due to
except in black interactions with a black
homochromy) colour promoting
neurosecretory factor
9. Yellow colour in adults Target organ (epidermis) of 3.2.2-3
(present in G, absent in S isolated and crowded
except on hind wings of adults reacts differently to
Locustu) CA/JH
10. Intensity of male sexual Target organ (nervous 3.3.2
behaviour (more intense in system?) of isolated and
G) crowded adults may react
differently to CA/JH
11. Fecundity of adult females +? +? Results are open to 3.3.3
(higher in S) different interpretations
12. Adult life span + 3.3.3 and 3.5
(longer in S)
13. Adult reproduction; +? Conclusion is open to 3.3.3
effects “transmitted” slight doubts; not all
to the progenyc experimental data support
the conclusion
14. Number of hopper instars +? +? The claim that CA/JH may 3.4
= number of eye stripes induce an extra hopper (see also 3.1)
in some species (higher in instar is entirely theoretical;
S of some species) some experimental data do
not support this claim
15. Rate of 0, consumption +? +? 3.5
(higher in G)
16 Heartbeat frequency + CA/JH do affect heartbeat 3.5
(higher in S) frequency, but this effect is
not responsible for phase
differences
17 Fat content (higher in G) +? Evidence is entirely 3.5
circumstantial
18. Isoenzymes in hoppers +? J H treatment did not 3.5
(some qualitative and induce isoenzymes which
quantitative differences were induced by isolation;
between G and S) as a “negative” result, it is
not entirely conclusive
19. Adult flight and/or +? +? Experimental data and 3.7.2
spontaneous locomotor evidence are not clear
activity (higher in G)
G = gregarious or crowded locusts; S = solitary or isolated locusts.

Although every effort was made to present an objective picture, this task is practically impossible when results are conflicting or open to different
interpretations. Some other authors may prefer removal or insertion of a question mark (which reflects some uncertainty) in relation to some effects.
These include: weight of hatchlings (higher in G), colour of hatchlings (differences between G and S), number of ovarioles in female hatchlings (higher in
S) and morphometrics of hatchlings (hatchlings of S are smaller and morphometrical analyses show differences between G and S ) .
44 M .P. PENER
The view that higher CA activity or higher J H titres induce the solitary
phase in locusts is rather deeply rooted in the literature (Kennedy, 1956,
1961, 1962; May, 1971; Cassier, 1974, and many other publications; for a
more recent review firmly holding this opinion see Nijhout and Wheeler,
1982). The reason for this situation may be because most of the cases in
which CA/JH promote (or are assumed to promote) solitary characteristics
were discovered and recognized earlier and received more attention, as well
as wider publication, than those cases in which CA/JH promote (or are
assumed to promote) gregarious characteristics. However, almost three
decades ago P. Joly (1962, p. 77) had already concluded that the “. . .
problem of physiological determination of locust phases cannot be explained
on the basis only of differential activity of the corpora allata”. The
information compiled in Table 1 of the present review indicates that this
conclusion is valid even today.
It may be assumed that the “phase status” in a particular instar is fixed by
CA activity and/or JH titres in the previous instar(s). For example, adult
phase characteristics may be fixed by J H titres in the hopper stage(s), or
phase characteristics of first-instar hoppers may be fixed by J H titres in the
adult mothers, etc. According to this assumption, differences in CA activity
and/or JH titres in a certain instar lead to “pre-conditioning” of some target
organ(s) to react differentially to J H in a subsequent instar. Although this
assumption may be valid in some cases in relation to some phase characteris-
tics, it cannot be held for all cases and for all phase characteristics. For
example, we have already detailed that JH induces yellow colour in crowded
adults, but does not do so in isolated ones (see Section 3.2.2). However, the
lack of yellowing in isolated adult males of Locustu cannot be explained by
the assumption that higher JH titres experienced during isolated hopper life
fixed the competence of the adult’s epidermis not to respond by yellowing to
the JH, because transfer of isolated adults to a crowd changes this com-
petence and results in yellowing (Pener, 1976b; see also Section 3.2.3). The
three simple experimental facts, amply demonstrated in Locustu, that: (1) the
body of the adult males does not become yellow as long as they are kept
isolated, (2) the CA/JH are necessary for the induction of yellow body colour
in crowded adult males, and (3) crowding of previously isolated adult males
does induce yellow body colour, cannot be reconciled with the assumption
that lack of yellowing in isolated males is solely a result of a higher J H titre in
any instar.
Nijhout and Wheeler (1982) advocated a major role of J H in the control of
locust phase polymorphism. However, their review is focused on a model of a
JH-induced gene-switching mechanism as the basis of insect polymorphism
and the conclusions drawn may be biased by preference for the model. As far
as locust phase polymorphism is concerned, these authors disregarded or
ignored almost all the evidence which may contradict the model. Some
experimental findings indicate that the period of sensitivity to green-colour
inducing and metamorphosis controlling effects of JH is different within a
hopper instar (see, for example, Joly, 1968, pp. 290-294; NEmec et al., 1970;
NEmec, 1971; De Wilde, 1975) and some authors (NEmec et al., 1970; NEmec,
1971; De Wilde, 1975) simply extended the findings related to green-colour
induction to a general idea of an overall phase determining effect. Following
this attitude, Nijhout and Wheeler (1982, p. 116) have stated that “it is clear
now that the JH-sensitive period for the determination of larval in contrast to
adult characters occurs at a different time than the JH-sensitive period
for solitary versus gregarious phase determination” and again (p. 117)
“. . . phase differentiation depends largely on the presence or absence of JH at
a critical period . . .”. One may wonder when the “critical period” is for JH to
affect, for example, pronotal shape (which is not influenced by JH), or non-
green (homochrome) solitary hopper colour, or competence of the adult
epidermis to become or not to become yellow. Eventually, by referring to the
black-colour-promoting neurosecretory factor (see Section 3.2. I), even Nij-
hout and Wheeler (1982) admit that the development of phase characteristics
does not depend exclusively on JH.
In conclusion, the differences in CA activity and J H titres, presumably
existing between isolated and crowded locusts, may constitute an additional
physiological phase characteristic responding to density. At the same time
these differences may also cause appropriate changes in some, but not in all
phase characteristics. Very probably, CA activity and J H titres stand not at
the beginning, but somewhere in the middle, of a chain of events and
physiological causal factors which are responsible for phase transformation.
Thus, the hypothesis that the solitary phase is just a neotenous form induced
by permanent or even specifically timed higher J H titres seems to be at best
an oversimplification.
4.2 THE PROTHORACIC ( = VENTRAL) GLANDS AND ECDYSTEROIDS
The prothoracic glands, often termed “ventral glands” (VG), of acridids are
located ventrolaterally in the posterior part of the head (P. Joly et al., 1956;
Strich-Halbwachs, 1959; Staal, 1961). These glands are somewhat diffuse,
not compact and there is no easy way to reach them. It is thus difficult to
ensure their complete removal by surgery. Nevertheless, the results of a
comprehensive study on the effects of ventral-glandectomy and implan-
tations of VG carried out by Strich-Halbwachs (1959) in Locusta (see also,
Strich-Halbwachs, 1954, 1958; Strich, 1955; Halbwachs et al., 1957) agreed
well with the concept that these glands control moulting. However, Staal
46 M. P. PENER
(1961) was unable to confirm this conclusion, probably because of imperfect

removal of the glands. Hoffmann and Koolman (1974) observed no moult
after careful extirpation of the VG and, using the Calliphora bioassay, they
did not detect ecdysone activity in homogenized tissues of ventral-glandecto-
mized fifth-instar Locusta hoppers. Hirn et al. (1979) obtained ecdysteroid
production by VG of Locusta in vitro, and more recently Reichhart and
Charlet (1986) found that addition of brain-corpora cardiaca extracts to the
medium enhanced ecdysone production by VG in vitro, presumably due to
the presence of an ecdysiotropic factor (prothoracicotropic hormone?) in
these tissues. Thus, there is no doubt that the VG of acridids and the
prothoracic glands of other insects are the same organs.
Ellis and Carlisle (1961) reported that the VG are larger in isolated than in
crowded young adults of Schistocerca, but they did not describe the method
of measuring the size of these diffuse and irregularly shaped glands. In an
earlier report, Carlisle and Ellis (1959) observed that the VG degenerate in
crowded adults of Locusta and Schistocerca, but persist in isolated adults of
these species. Later work on Locusta somewhat modified this claim. Cassier
and Fain-Maurel (1968) and Fain-Maurel and Cassier (1969) found that
under long days (LD= 16 : 8) the VG degenerate, but under short days
(LD= 12 : 12) they persist in crowded Locusta adults. However, in isolated
green adults the VG persist under high humidity but degenerate in non-green
isolated adults kept under dry conditions (Cassier and Fain-Maurel, 1969a).
Moreover, the persisting VG of the green isolated adults show cyclic
ultrastructural changes in correlation with cycles of oocyte development
(Cassier and Fain-Maurel, 1969b), though it has not been demonstrated that
such persisting glands actually produce ecdysone. Cassier (1969) related the
persistence of the VG in crowded adults kept under short days and in isolated
adults kept under high humidity to a “hyperactivity” of the CA in such
locusts. However, the physiological importance (if any) of the persisting VG
in adult locusts is not clear and later Cassier (1974) considered that this
persistence is rather a result than a cause of some phase change. Kiiqiikekgi
(1969) found that the VG in developing embryos of Schistocerca were
somewhat smaller in those originating from isolated mothers than in those
originating from crowded ones, but the difference did not exceed that
expecied due to the smaller size of eggs and embryos from isolated mothers
(see Section 3.3.3).
Although suitable techniques for testing ecdysone biosynthetic activity of
the VG in vitro are available (cf. Hirn et al., 1979; Reichhart and Charlet,
1986), such techniques have not been utilized to investigate possible dif-
ferences in VG activity between isolated and crowded locusts. Several
independent studies, however, demonstrate that ecdysteroid titres are simi-
lar, or at least not markedly different, between crowded and isolated Locusta
(L. Joly et al., 1977; Ismail et al., 1979; Fuzeau-Braesch et al., 1982) and
Schistocerca (Wilson and Morgan, 1978).
Only few publications claim an effect of the VG on phase characteristics.
Ellis and Carlisle (1961) and Carlisle and Ellis (1962) reported a positive
correlation between the F/C morphometric ratio (see Section 3.1) and the
size of the VG in Schistocerca, and observed that partial extirpation of the
VG promoted gregarious colouration in hoppers of Schistocerca, though not
in Locusta. The same authors (Carlisle and Ellis, 1963) also found reduced
marching behaviour in crowded Locusta hoppers after injection of VG
extracts (see Section 3.7. I), and Michel (1972a) observed that implantation
of presumably active VG decreased flight activity in Schistocerca adults. All
these reports would indicate a “solitarizing” effect of the VG. Finally,
Haskell and Moorhouse (1963) claimed that ecdysteroids reduce the activity
of certain motor neurons, an effect which seems to agree with the lower
locomotor activity of solitary locusts. However, the results of Haskell and
Moorhouse (1963) were probably not caused by ecdysteroids, or they were
caused by a pharmacological effect of a presumably very high concentration
of ecdysteroids (for details see Section 3.7.1), and Michel’s (1972a) findings
may need further confirmation (see Section 3.7.2).
In Locusta, Staal(l961) did not find an appreciable effect of implanted VG
on colour, nor on the F/C and E/F morphometric ratios, except in some
“giant adults” which exhibited very high “hypergregarious” E/F ratios (see
Section 3. l), probably reflecting disturbances in metamorphosis rather than
a shift toward the gregarious phase. KiiGiikekSi (1969) observed no clear
relation between VG in embryos and colour of hatchlings in Schistocerca.
The investigations of Strich-Halbwachs (1954, 1959) and Halbwachs et al.
(1957) were focused on the effect of VG on moulting rather than on possible
phase changes, but as far as information relevant to phase may be gained
from these studies, the VG did not affect E/F and F/C ratios, nor colour, in
Locusta (see also the discussion of Strich-Halbwachs’ results by Girardie and
Joly, 1968).
In the light of the similarity of ecdysteroid titres in crowded and isolated
locusts (see above), it seems unlikely that the VG and ecdysteroids play a
major ’causal role in locust phase transformation. This conclusion leaves the
reports of Ellis and Carlisle (1961), Carlisle and Ellis (1962, 1963) and Michel
(1972a) unexplained, except if one assumes that the VG produce some other
hormone(s) beside ecdysteroids (cf. L. Joly et al., 1969; Hoffmann and
Weins, 1974; L. Joly and Schneider, 1976; see also discussion by Wilson and
Morgan, 1978; and a recent article by Charlet et al., 1988), and that these
“other hormones” affect phase.
48 M. P. PENER
4.3 NEUROSECRETORY CELLS, CORPORA CARDIACA A N D NEUROHORMONES
The activity of the CA is regulated by complex neurosecretory and nervous

signals from the brain (reviews by Raabe, 1982; Feyereisen, 1985; Tobe and
Stay, 1985). In locusts, the overall effect of the brain on the CA is activatory;
an allatotropin, presumably a neurohormone, seems to be a major factor in
this activation (see reviews above and later studies by Gadot and Apple-
baum, 1986; Gadot et al., 1987a,b), though further neurosecretory and/or
nervous activating and inhibitory effects may also be involved in the
regulation of locust CA activity (cf. Tobe and Stay, 1985; and a later study by
Baehr et al., 1986). The activity of the prothoracic glands in insects is also
controlled by the brain, primarily by the prothoracicotropic hormone(s)
(reviews by Raabe, 1982; Bollenbacher and Granger, 1985). In agreement
with this concept, Reichhart and Charlet (1986) have shown that brain-CC
extracts exert an ecdysiotropic effect on the VG of Locusta in vitro. It seems,
therefore, that any effect on phase polymorphism which may be related to
differential activity of the CA and/or the VG in solitary and gregarious
locusts, may be retraced to corresponding superimposed differences in the
regulatory activity of the brain or brain and CC. Since neurohormones seem
to play a major role in the control of CA and VG activity, they may be
involved in the regulation of phase polymorphism as much as the CA or VG
themselves, though the effect(s) of such neurohormones on phase may be
considered as indirect. However, possible phase-related differences in neuro-
hormones which activate or inhibit CA or VG activity, have never been
investigated.
Highnam and Haskell (1964) studied the amount of neurosecretory
material in the pars intercerebralis neurosecretory cells (PI-NSC) and CC of
isolated and crowded adult females in relation to oocyte growth and the
effect of flight upon maturation in both Schistocerca and Locusta. Generally,
they found that experimental conditions which led to slow maturation of the
oocytes also led to the accumulation of neurosecretory material in the PI-
NSC and CC system. Conditions which enhanced oocyte maturation also
promoted the release of neurosecretory material from this system. These
correlations, however, do not reveal underlying causal relationships and do
not clarify even possible indirect effects (CA activity?) of neurosecretion on
phase.
Other, possibly more direct, neurohormonal effects on phase polymor-
phism have also been poorly investigated. There is evidence that an NSC-CC
neuroendocrine factor promotes the black patterns which are characteristic
of gregarious hoppers, but the identity of this factor is unknown; it may also
be involved in the control of the black homochrome response of solitary
hoppers and may not be limited to locusts (for details see Sections 3.2.1 and
3.2.3). The relationship between biogenic amines which may function as

neurohormones and locust phase polymorphism is unclear; certain experi-
mental findings are controversial (see Section 3.7.2) and even if phase-
dependent differences exist in some biogenic amines, their causal role and
mode of involvement in phase change are as yet obscure.
The fact that repeated short daily treatment with CO, induces solitary
phase characteristics in crowded Locusta may also be considered as an
indication that neural factors are involved in phase change (review and
interpretation by Fuzeau-Braesch and Nicolas, 1981). The nervous system
seems to be a probable target organ for the CO,, but the actual effect(s) may
be neurosecretory, nervous, or both.
Bernays (1980) suggested that a factor from the CC reduces locomotor
activity in crowded hoppers of Locusta. The role of this putative factor in
behaviour-related phase differences has not been investigated, though it may
be assumed, as a working hypothesis, that this factor promotes the more
sedentary behaviour (no marching, inferior flight performance, see Sections
3.7.1 and 3.7.2, respectively) of solitary locusts. Alternatively, absence of this
factor may promote the more active gregarious behaviour.
As already outlined (see Pener, 1985; and Section 3.7.2), despite extensive
studies and hundreds of research articles on AKH in crowded locusts, there is
not a single publication devoted to AKH in isolated ones and nothing is
known on possible AKH-related differences between gregarious and solitary
locusts.
All the available information constitutes only circumstantial evidence,
intermingled with speculations, about the role of neurohormones in the
regulation of locust phase polymorphism. The lack of more solid and exact
evidence is mainly because the subject has not received sufficient attention
and experimental efforts.
5 Pheromones
Pheromones are often classified as “primers” and “releasers”; the latter have
short-term effects and trigger preprogrammed behaviour in the receiving
animal, whereas primer pheromones induce long-term effects, changing the
physiology and/or behaviour of the receiving animals so that they become
physiologically (or even morphologically) different and/or react differently to
environmental stimuli from those animals which have not been exposed to
the primer (Wilson and Bossert, 1963; for a more recent review see Weaver,
1983). Endocrine factors may regulate production of, and/or responsiveness
to, both kinds of pheromones, but only primers may induce endocrine
changes. Although a preprogrammed behaviour induced by a releaser may
50 M. P. PENER
also affect subsequent behaviour and physiology, including endocrinology,

of both the releaser producing and receiving animals, in such cases (for
example, successful copulation mediated by some sex pheromone) not the
releaser itself, but the pheromone-induced execution of the behaviour causes
long-term physiological effects. This classification of the pheromones into
releasers and primers is useful, but in some cases no easy distinction can be
made, or a pheromone may act as both a releaser and a primer (see
maturation-accelerating pheromone, below).
The relationship between locust phases and pheromones may be two-fold;
phase may affect pheromone production and/or reception, or (primer)
pheromones may affect locust phase changes. The presumably chemotactile
( = contact) pheromonal factor which promotes group behaviour in oviposi-
tion of Schistocerca (and possibly of Locusta) females (see Section 3.7.2)
seems to be a releaser. Production of this pheromone may be affected by
phase, because there is some evidence that isolated locusts probably produce
less of this pheromone than crowded ones (Norris, 1970). Nothing is known
about the possible involvement of endocrine factors in the production or the
reception of this pheromone. Gillett et al. (1976) were unable to demonstrate
that there are other releaser pheromones which have marked or consistent
effects in promoting immediate aggregation in Schistocerca, and concluded
that visual and/or mechano-tactile factors play a more important role in
locust grouping than chemical ones. However, more recent findings (Fuzeau-
Braesch et al., 1988) may somewhat modify this conclusion (see below).
The CA/JH-dependent maturation-accelerating pheromone produced by
sexually mature adult Schistocerca males (see Section 3.3.1) seems to be both
a releaser and a primer. It was reported to induce the “vibration reaction” in
mature and immature adults of both sexes (Loher, 1961). Amerasinghe
(1978a) confirmed this effect of the pheromone on mature males, but not on
immature ones. By inducing the “vibration reaction” the pheromone acts as
a releaser. However, regarding its maturation-accelerating effect (see Section
3.3. l), the pheromone acts as a primer; it presumably accelerates reproduc-
tion-related adult development of the endocrine system. The double involve-
ment of the CA/JH in this system is interesting; they affect pheromone
production in a male and they are affected by the pheromone in the receiving
locust. If other effects of crowding (such as initial inhibition of maturation in
both Locusta and Schistocerca and maturation acceleration by mature
Locusta) are also pheromonal (see Section 3.3.1), these may also be con-
sidered as primers. There is some dispute about whether differences in
production of maturation-accelerating pheromone between isolated and
crowded mature Schistocerca males (see Section 3.3.1) d o exist, but no claim
has been made that this pheromone, or other putative maturation-affecting
pheromones, play a causal role in phase transformation.
Based on results indicating the promotion of gregarious black hopper

colouration (Nolte, 1963) and increase in long-term gregarious behaviour
(Gillett, 1968; Ellis and Gillett, 1968), a so-called “gregarization pheromone”
was found to be produced by locusts. This pheromone seems to be a primer
(Gillett, 1968), and it was proposed to induce or intensify gregarious phase
characteristics. Subsequent reports on this “gregarization pheromone”,
however, are somewhat controversial.
Nolte et al. (1970, 1973) and Nolte (1974, 1976) have concluded that the
gregarization pheromone is produced in the crop of the alimentary tract,
is present in the faeces of hoppers and it is actually 5-ethyl-guaiacol
( = 2-methoxy-5-ethylphenol); they named it “locustol”. Nolte (1977) even
postulated that locustol somehow promotes the production of cyclic AMP,
and the latter promotes transformation from solitary to gregarious phase.
Nolte and co-workers regarded chiasma frequency as a major and decisive
phase characteristic (see Section 3.6), and unfortunately tested the effect of the
gregarization pheromone or locustol mostly or only on this parameter.
Chiasma frequency, however, may not be a good phase indicator (see Section
3.6) and phase-related conclusions based on this parameter need further
independent support. Also, Nolte (1977) drew his conclusions on the relation-
ships between locustol, cyclic AMP and phase from circumstantial evidence,
again using chiasma frequency as the main parameter. Although in this study
some other parameters were also employed, the results obtained for these are
not very convincing; for example, the differences in the mean F/C ratios varied
between 3.25 and 3.47 in different experimental groups of “solitary controls”,
and this range was larger than the differences induced by injection of locustol
(from 3.25 to 3.11, or from 3.37 to 3.25, or from 3.46 to 3.34, in different
experimental groups) or of cyclic AMP (from 3.46 to 3.35).
On the other hand, Gillett (1975a,b) reported that a gregarization phero-
mone in Schistocerca affects some phase characteristics, such as colour or
certain components of behaviour, but it has no or doubtful influence on some
other phase characteristics including morphometrics and number of eye
stripes (=number of instars, see Section 3.4). Like Nolte’s group (see above),
Gillett and Phillips (1977) also found that the faeces of the hoppers constitute
the source of a “gregarizing” factor, but they showed in the same study that
the faeces of the adults have a “solitarizing” influence. Later Gillett (1983)
confirmed these results, but she reported that while extracts of hopper faeces
exerted the appropriate “gregarizing” effects, locustol (presumably a synthe-
tic preparation) did not. Also, Gillett (1983) found that the gregarization
pheromone from the faeces of the hoppers is perceived by the antennae,
whereas Nolte el al. (1970) and Nolte (1974) claimed that locustol is received
and/or perceived through the spiracles. Fuzeau-Braesch et al. (1988) found
phenol, veratrole and guaiacol, but no 5-ethyl-guaiacol ( = Nolte’s “locus-
52 M. P. PENER
tol”), in vapour condensed from the atmosphere of cages of crowded Locusta

and Schistocerca. The mixture of these three compounds and also pure
guaiacol or phenol, tended to increase aggregation behaviour without acting,
however, as attractants. Perhaps these substances only amplify aggregation
behaviour when coupled with other, visual and/or tactile (see above and
Gillett et al., 1976), stimuli. If so, these phenolic compounds may be regarded
as releaser pheromones with a complementary role. Fuzeau-Braesch et al.
(1988) neither investigated the exact source (faeces?) of these substances, nor
their possible primer effect(s) on phase transformation.
In conclusion, a gregarization pheromone does seem to exist in the faeces
of hoppers and to act as a primer, but its identity, importance and mode of
action in phase transformation are not yet fully understood. The “solitariz-
ing” influence of adult faeces (Gillett and Phillips, 1977; Gillett, 1983) may
indicate a further primer pheromonal effect on phase, though the practical
role of this effect in natural phase changes seems to be rather obscure.
Possible relations between phase-affecting primer pheromones and endocrine
factors have not been studied; for example, there is no report in the literature
on possible effects of CA/JH on the production of the relatively well
documented gregarization pheromone (regardless whether it is locustol or
some other substance) which is found in the faeces of hoppers.
6 Concluding remarks
During the previous large-scale locust plague, in the 1950s and early 1960s,
basic research on locusts flourished, especially in the UK and France, with
overt or unexpressed hopes that Old World locust problems would be solved
through a better understanding of fundamental locust biology. It was largely
accepted that the factors affecting, and basic processes underlying, locust
phase transformation may lead to practical control of these insects. This
period coincided with the maturation of insect endocrinology as an estab-
lished branch of biology (cf. Wigglesworth, 1954). Interest in locust research
on the one hand, and in the relatively new promising field of insect
endocrinology on the other, led to the investigation of endocrine effects on
locust phases. The momentum so gained maintained the research in the 1960s
and early 1970s, long after the locust plague had declined in the mid 1960s.
This research produced an extensive literature, especially on the effects of
CA/JH. This is well reflected in the bibliography of the present review but
which is by no way comprehensive for this period.
However, the vast amount of work invested into the subject did not yield
uniformly accepted concepts about the role of the CA and JH in the control
of locust phase changes, except the effect on green colouration. Mostly this
latter effect led to the superficial confirmation of the claim that CA/JH
induce the solitary phase (see Sections 3.2.3 and 4.1). Authors familiar with
the complexity of locust phases usually did not accept this oversimplified
conclusion without serious restrictions (Joly, 1962; Rowell, 1971 ; Pener,
1976b, 1983; Hardie and Lees, 1985), but its repetition in the literature
created a feeling among insect endocrinologists not much specialized in
locusts that the problem of endocrine control of locust phases has been
“solved” and that there is not much room for further research. This attitude
decelerated endocrine research on locust phases.
Applied aspects have played even a more crucial role in this declaration. It
has been long known that density is the primary extrinsic factor which
controls locust phases, and phase change does not precede but follows
changes in density. Consequently for forecasting locust outbreaks, increases
in population density rather than phase characteristics have been surveyed in
the field. Phase was considered as unimportant from the practical standpoint.
Moreover, there were no serious locust outbreaks for over 20 years, from the
mid 1960s until the mid 1980s, leading to the then increasingly accepted
opinion that locusts are pests of the past and research on their phase change
has no applied justification.
The recent locust outbreak which started in 1985-86 and reached a
devastating culmination in 1988, convincingly refuted the concept that
locusts are pests of the past and rekindled interest in locusts and their phase
polymorphism. Locust research is again considered to be important from the
applied standpoint (Anonymous, 1989). The primary role of density in locust
phase changes is not doubted, but the rather mechanistic view that phase is
unimportant and phase change is not a target for applied research is losing its
foothold. Thus, for example, it is realized today that if change from the
solitary to the gregarious phase, especially the marching behaviour of
hoppers and/or the swarming behaviour of adults, can be prevented despite
an increase in densities over critical levels, the locusts may not be able to
emigrate from localized areas. Present and future insect growth regulators
(IGRs), such as hormone analogues and anti-hormonal agents, may serve as
possible candidates for such prevention of major displacements of gregarious
locusts. Locusts which would be unable to make long-distance collective
emigrations from localized areas, would be easy targets to limited conven-
tional or integrated control measures. Most of the locusts may meet death
even without control measures because of starvation imposed by food
limitations in such localized areas.
In the present review I wished to emphasize that the problem of endocrine
effects on locust phase changes is far from being “solved”. Probably, we are
nearer to the beginning than to the end of the road. In the light of the great
54 M .P. PENER
progress made in insect endocrinology and other relevant branches of science

during the last 15 years or so when locust phase-related endocrine research
was rather neglected, we are now able to reframe old questions, pose new
ones and make novel working hypotheses which can be attacked by modern
methods of molecular biology and computer analysis. Thus, for example, are
there AKH-related differences between gregarious and solitary locusts (see
Section 3.7.2)? What is the fuel for the intense marching of gregarious
hoppers (see Section 3.7.1)? Is there an endocrine control of the marching
behaviour and/or of fuel mobilization for marching, and if so, are there
differences in the related endocrine mechanism(s) between marching gregar-
ious and non-marching solitary hoppers? Do the CA/JH (claimed by some
authors to play a primary role in locust phase changes, cf. Nijhout and
Wheeler, 1982), or other hormones, affect aggregation behaviour? It was
demonstrated almost 40 years ago that marching can be induced and
investigated in the laboratory, and almost 30 years ago that aggregation
behaviour can be well studied even in laboratory cages (see Section 3.7. I and
the relevant publications of Ellis and co-workers cited in the same Section).
Today these behavioural patterns can be studied by using time-lapse video
cameras, and the data can be analysed by computerized methods. JH
analogues or anti-juvenile agents (precocenes) can be administered instead of
time-consuming implantations of CA or surgical allatectomy. Phase charac-
teristics at the molecular level can be (cf. Colgan, 1987) and should be
discovered and neuroendocrine effects on these should be investigated. In
spite of the fact that colour-affecting neurohormones have been isolated and
characterized from other insects (see, for example, Matsumoto et al., 1988),
not much is known on the black-patterns/black-colour-promoting neurohor-
monal factor in locusts (see Section 3.2.1). Possible effects of this neurohor-
mone on phase characteristics other than the black patterns, and of other
putative neurohormones on phase changes, are poorly investigated and
practically unknown (see Section 4.3). Possible endocrine or neuroendocrine
effects on production, release and perception of phase-affecting primer
pheromones have not been studied (see Section 5). During the last few years
peptidergic insect neurohormones have become promising candidates for
non-conventional insect control. In contrast to earlier concepts, it is now
agreed that insect neurohormones may be developed to “IGRs” by genetic-
ally engineered microorganisms, especially by baculoviruses (Keeley and
Hayes, 1987; Keeley, 1988; Menn and Bofkovec, 1989). Baculoviruses also
infect locusts, though as a pathogen they kill them very slowly (cf. Bensimon
et a!., 1987). However, an engineered virus with a neuropeptide (neurohor-
mone) gene placed behind a strong non-essential viral promoter could well
produce a devastating neurohormonal deregulation in the insect host. An
oecologically acceptable strategy for the use of a genetically engineered
baculovirus has recently been discovered (Wood et at., 1990). Understanding

the neuroendocrine basis of locust phase changes may well reveal new target
systems for such non-conventional methods.
In conclusion, locust phase change with its extraordinary phenotypic
plasticity is an extremely interesting biological problem and there is enough
evidence to conclude that it is at least influenced, and perhaps completely
regulated, by endocrine and/or neuroendocrine factors. A reassessment of
the subject using modern methods and novel considerations may lead to
interesting and important findings in the fields of both basic and applied
science.
References
Abu-Hakima, R. (1981). Vitellogenin synthesis induced in locust fat body by juvenile

hormone analog in vitro. Experientia 37, 1309-1 3 11.
Albrecht, F. 0. (1955). La densite des populations et la croissance chez Schistocerca
gregaria (Forsk.) et Nomadacris septemfasciata (Serv.); la mue d’ajustement.
J. Agric. trop. Bot. appl. 2, 109-192.
Albrecht, F. 0. (1959). Facteurs internes et fluctuations des effectifs chez Nomadacris
septemjasciata (Serv.). Bull. biol. Fr. Belg. 93, 414461.
Albrecht, F. 0. (1964). Etat hygrometrique, coloration et resistance chez l’imago de
Locusta migratoria migratorioides (R.F.). Experientia 20,97-98.
Albrecht, F. 0. (1965). Influence du groupement, de l’etat hygromktrique et de la
photoperiode sur la resistance au jeQne de Locusta migratoria migratorioides R. et
F.(Orthoptere acridien). Bull. biol. Fr. Belg. 99, 287-339.
Albrecht, F. 0. (1967). “Polymorphisme Phasaire et Biologie des Acridiens Migra-
teurs.” Masson & Cie., Editeurs, Paris.
Albrecht, F. 0. and Blackith, R. E. (1957). Phase and moulting polymorphism in
locusts. Evolution 11, 166177.
Albrecht, F. 0. and Cassier, P. (1964). Modifications de la feconditk et de la
descendance chez Locusta migratoria migratorioides (R. et F.) phase solitaire,
apres implantation de numbreaux corps allates. C.r. hebd. Sianc. Acad. Sci., Paris,
Groupe 12 259, 3375-3377.
Albrecht, F. 0. and Lauga, J. (1978). Influence du photoperiodisme et de la
temperature d’elevage sur la morphologie et la phase de Locusta migratoria
migratorioides (R. et F.) (Orthopteres, Acridiens). C.r. hebd. Sianc. Acad. Sci.,
Paris 286D, 1799-1801.
Albrecht, F. 0. and Lauga, J. (1979). Effets de la photoperiode et de l’humidite sur le
polymorphisme de Locusta migratoria migratorioides (R. et F.) (Orthoptires,
Acridiens) eleve en isolement: etude morphometrique des solitaires verts et bruns.
C.r. hebd. Sianc. Acad. Sci., Paris 289D, 753-755.
Albrecht, F. O., Verdier, M. and Blackith, R. E. (1958). Determination de la fertilite
par l’effet de groupe chez le criquet migrateur (Locusta migratoria migratorioides
R. et F.). Bull. biol. Fr. Belg. 92, 349427.
56 M. P. PENER
Albrecht, F. O., Verdier, M. and Blackith, R. E. (1959). Maternal control of ovariole

number in the progeny of the migratory locust. Nature 184, 103-104.
Ali, Y. (1987). Pheromone-secreting cells in the epidermis of Locusta migratoria
migrutorioides (Orthoptera: Acrididae). Pakistan J . Zool. 19, 127-132.
Amerasinghe, F. P. (1978a). Pheromonal effects on sexual maturation, yellowing, and
the vibration reaction in immature male desert locusts (Schistocerca gregaria).
J. Insect Physiol. 24, 309-314.
Amerasinghe, F. P. (1978b). Effects of J.H.1 and J.H.111 on yellowing, sexual activity
and pheromone production in allatectomized male Schistocerca gregaria. J . Insect
Physiol. 24, 603-6 1 1.
Anonymous (1989). “Desert Locust Research Priorities. Report of the F A 0 Research
Advisory Panel, 2-5 May 1989.” Food and Agricultural Organization of the
United Nations, Rome, Italy.
Baehr, J.-C., Porcheron, P., Papillon, M. and Dray, F. (1979). Haemolymph levels of
juvenile hormone, ecdysteroids and protein during the last two larval instars of
Locusta migratoria. J . Insect Physiol. 25, 41 5421.
Baehr, J. C., Caruelle, J. P. and Poras, M. (1986). The activity of denervated corpora
allata in a diapausing strain of Locusta migratoria: in vivo and in vitro studies.
Int. J . Invertebr. Reprod. Dev. 10, 143-150.
Ballan-DufranGais, C. (1978). Biaccumulation minerale purique et pigmentaire dans
le tegument de Schistocerca gregaria (Forsk.). Dimorphisme sexuel et controle
endocrine. Acrida 7, 85-99.
Beenakkers, A. M. Th., Bloemen, R. E. B., De Vlieger, T. A., Van der Horst, D. J.
and Van Marrewijk, W. J. A. (1985a). Insect adipokinetic hormones. Peptides 6,
Suppl. 3, 437444.
Beenakkers, A. M. Th., Van der Horst, D. J. and Van Marrewijk, W. J. A. (1985b).
Biochemical processes directed to flight muscle metabolism. In “Comprehensive
Insect Physiology Biochemistry and Pharmacology”, Vol. 10, Biochemistry (Eds
G. A. Kerkut and L. I. Gilbert), pp. 451486. Pergamon Press, Oxford.
Benichou-Redouane, K. and Fuzeau-Braesch, S. (1982). Comparaison des taux
d’octopamine chez Locusta migratoria cinerascens grkgaire, solitaire et solitarise
au gaz carbonique, dans different organes nerveux. C.r. hebd. Sianc. Acad. Sci.,
Paris, Sir. III 294, 385-388.
Bensimon, A,, Zinger, S., Gerassi, E., Hauschner, A,, Harpaz, I. and Sela, I. (1987).
“Dark cheeks”, a lethal disease of locusts provoked by a lepidopterous baculo-
virus. J. Invertebr. Path. 50, 254-260.
Bergot, B. J., Schooley, D. A. and De Kort, C . A. D. (1981). Identification of JH I11
as the principal juvenile hormone in Locusta migratoria. Sxperientia 37, 909-910.
Bernays, E. A. (1980). The post-pandrial rest in Locusta migratoria nymphs and its
hormonal regulation. J . Insect Physiol. 26, 119-123.
Blackith, R. E. (1972). Morphornetrics in acridology: a brief survey. Acrida 1, 7-15.
Blackith, R. E. and Albrecht, F. 0. (1959). Morphometric differences between the
eye-stripe polymorphs of the red locust. Sci. J . R. Coll. Sci. 27, 13-27.
Blackith, R. E. and Howden, G. F. (1961). The food reserves of hatchling locusts.
Comp. Biochem. Physiol. 3, 108-124.
Bollenbacher, W. A. and Granger, N. A. (1985). Endocrinology of the prothoracic-
otropic hormone. In “Comprehensive Insect Physiology Biochemistry and Phar-
macology”, Vol. 7, Endocrinology I (Eds G. A. Kerkut and L. I. Gilbert), pp. 109-
151. Pergamon Press, Oxford.
Bouthier, A. (1966). Modifications des pigments (ommochromes et pterines) en

relation avec la mutation albinos chez Locusta migratoria cinerascens Fabr.
(Orthopteres, Acrididae). C.r. hebd. Skanc. Acad. Sci., Paris 262D, 148C-1483.
Bouthier, A. (1976). Action des facteurs hormonaux sur le mktabolisme des ommo-
chromes chez le criquet Locusta migratoria L. (Orthopteres, Acrididae). Ann.
Endocr. 37, 539-540.
Brian, M. V. (1979). Caste differentiation and division of labor. In “Social Insects”
Vol. 1 (Ed. H. R. Hermann), pp. 121-222. Academic Press, New York.
Burnett, G. F. (1951). Observations on the life-history of the red locust, Nomadacris
septemfasciata (Serv.) in the solitary phase. Buil. ent. Res. 42, 473490.
Butler, C. G. and Innes, J. M. (1936). A comparison of the rate of metabolic activity
in the solitary and migratory phases of Locusta migratoria. Proc. R. SOC.B. 119,
296-304.
Carlisle, D. B. and Ellis, P. E. (1959). La persistance des glandes ventrales cephaliques
chez les criquets solitaires. C.r. hebd. Skanc. Acad. Sci., Paris 249, 1059-1060.
Carlisle, D. B. and Ellis, P. E. (1962). Endocrine glands and phase in locusts. Symp.
Genet. Biol. Ital. (Proc. 4th Congr. int. Union Study soc. Insects, Pavia 1961) 10,
2 19-224.
Carlisle, D. B. and Ellis, P. E. (1963). Prothoracic gland and gregarious behaviour in
locusts. Nature 200, 603-604.
Cassier, P. (1963). Action des implantations de corps allates sur la reactivitt
phototropique de Locusta migratoria migratorioides (R. et F.), phase gregaria
(Insecte Orthoptero’ide). C.r. hebd. Skanc. Acad. Sci., Paris, Groupe I 0 257, 4048-
4049.
Cassier, P. (1964a). h u d e et interpretation des effets ti long terme, des implantations
abdominales de corps allates, sur la rCactivitC phototropique de Locusta migratoria
migratorioides (R. et F.), phase gregaire (Insecte Orthopteroide). C.r. hebd. Skanc.
Acad. Sci., Paris, Groupe 12 258, 723-725.
Cassier, P. (1964b). La rtactivite phototropique de Locusta migrutoria migratorioides
(R. et F.), phase gregaire, apres implantation abdominale de corps allates. Insectes
SOC. 11, 131-140.
Cassier, P. (1965a). Determinisme endocrine de quelques caracteristiques phasaires
chez Locusta rnigratoria migratorioides (R. et F.) (Insecte Orthopteroide Acridi-
dae). Znsectes SOC. 12, 71-79.
Cassier, P. (1965b). Le comportement phototropique du criquet migrateur (Locusta
migratoria migratorioides R. et F.): Bases sensorielles et endocrines. Annls Sci. nut.
(Zool.), Skr. 12 7,213-358.
Cassier, P. (1966a). Effets de l’ablation d’un corps allate sur la fecondite et la
descendance des femelles isoltes du criquet migrateur (Locusta migratoria migra-
torioides R. et F.) (Insecte Orthopteroide, Acrididae). Insectes soc. 13, 17-27.
Cassier, P. (1966b). L’activite des corps allates et la reproduction du criquet migrateur
Africain, Locusta migrutoriu migratorioides R. et F. Bull. SOC.zool. Fr. 91, 133-
148.
Cassier, P. (1969). Etat phasaire et destinee post-imaginale des glandes ventrales chez
Locusta migrutoria migratorioides (R. et F.). Proc. 6th Congr. int. Union Study SOC.
Insects (Bern, 1969), 33-38.
Cassier, P. (1970). Influence des conditions d’elevage (isolement et groupement) sur la
fecondite des femelles de Locusta migratoria rnigratorioides (R. et F.) et sur les
caracteristiques de leur descendance: donnees endocrines. Colloq. int. CNRS
58 M. P. PENER
(“L’Influence des Stimuli Externes sur la Gametogenese des Insectes”) No. 189,
87-111.
Cassier, P. (1974). Der Phasenpolymorphismus der Wanderheuschrecken. In “Sozial-
polymorphismus bei Insekten. Problem der Kastenbildung in Tierreich” (Ed. G.
H. Schmidt), pp. 11&151. Wissenschaftliche Verlagsgesellschaft, Stuttgart.
Cassier, P. (1977). Imaginal development of the integument in the desert locust,
Schistocerca gregaria Forsk.: influence of sex and phase. In “Advances in
Invertebrate Reproduction”, Vol. 1 (Eds K. G. Adiyodi and R. G. Adiyodi), pp.
344-355. Peralam-Kenoth, Karrivellur, Kerela, India.
Cassier, P. and Delorme-Joulie, C. (1976). La differenciation imaginale du tegument
chez le criquet pelerin, Schistocerca gregaria Forsk. 111.-Les diffkrences phasaires
et leur determinisme. Insectes soc. 23, 179-198.
Cassier, P. and Fain-Maurel, M.-A. (1968). Influence de la photoperiode sur la
persistance ou la degenerescence des glandes de mue chez les imagos gregaires du
criquet migrateur. Etude experimentale et infrastructurale. C.r. hebd. Sdanc. Acad.
Sci.,Paris 267D, 646648.
Cassier, P. and Fain-Maurel, M.-A. (1969a). Etude infrastructurale des glandes de
mue de Locusta migratoria migratorioides (R. et F.). 111. Sur la persistance ou la
degenerescence des glandes ventrales chez les imagos solitaires. Archs 2001. exp.
g i n . 110, 203-224.
Cassier, P. and Fain-Maurel, M.-A. (1969b). Etude infrastructurale des glandes de
mue de Locusta migratoria migratorioides (R. et F.). IV. Evolution des glandes de
mue au cours de la maturation sexuelle et des cycles ovariens chez les solitaires
verts. Archs Zool. exp. gin. 110, 267-278.
Cassier, P. and Papillon, M. (1968). Effets des implantations de corps allates sur la
reproduction des femelles groupees de Schistocerca gregaria (Forsk.) et sur le
polymorphisme de leur descendance. C.r. hebd. Sdanc. Acad. Sci., Paris 266D,
1048- 1051.
Chamberlain, D. J. (1980). The effects of pod crowding on the viability of eggs of
Locusta migratoria migratorioides (R. & F.) and Schistocerca gregaria (Forsk.)
(Orthoptera: Acrididae). Acrida 9, 5 1-62.
Charlet, M., Roussel, J.-P., Rinternecht, E., Berchtold, J.-P. and Costet, M.-F.
(1988). Developmental and morphogenetic alterations in larvae of Locusta migra-
toria reared on plant diet with a selectively modified sterol profile. J. Insect
Physiol. 34, 787-796.
Chauvin, R. (1941). Contribution a 1’Ctude physiologique du criquet pelerin et du
determinisme des phhomenones gregaires. Annls Soc. ent. Fr. 110, 133-272.
Chen, T. T., Couble, P., De Lucca, F. L. and Wyatt, G. R. (1976). Juvenile hormone
control of vitellogenin synthesis in Locusta migratoria. In “The Juvenile
Hormones” (Ed. L. I. Gilbert), pp. 505-529. Plenum Press, New York and
London.
Chen, T. T., Couble, P., Abu-Hakima, R. and Wyatt, G. R. (1979). Juvenile
hormone-controlled vitellogenin synthesis in Locusta migratoria fat body. Hor-
monal induction in vivo. Dev. Biol. 69, 59-72.
Chopard, L. (1949). L’ktat actuel de la question des phases chez les insectes. Ann&
Biol. 25, 105-109.
Colgan, D. J. (1987). Developmental changes of isoenzymes catalysing glycolytic and
associated reactions in Locusta migratoria in relation to the rearing density of
hatchlings. Insect Biochem. 17, 303-308.
Couillaud, F., Girardie, J., Tobe, S. S. and Girardie, A. (1984). Activity of

disconnected corpora allata in Locusta migratoria: juvenile hormone biosynthesis
in vitro and physiological effects in vivo. J . Insect Physiol. 30, 551-556.
Couillaud, F., Mauchamp, B. and Girardie, A. (1985). Regulation of juvenile
hormone titer in African locust. Experientiu 41, 1165-1 167.
Couillaud, F., Mauchamp, B. and Girardie, A. (1987). Biological, radiochemical and
physicochemical evidence for the low activity of disconnected corpora allata in
locust. J. Insect Physiol. 33, 223-228.
Dadd, R. H. (1961). Observations on the effects of carotene on the growth and
pigmentation of locusts. Bull. ent. Res. 52, 63-81.
Dale, J. F. and Tobe, S. S. (1986). Biosynthesis and titre ofjuvenile hormone during
the first gonotrophic cycle in isolated and crowded Locusta migratoria females.
J . Insect Physiol. 32, 763-769.
Dale, J. F. and Tobe, S. S. (1988). Differences in the stimulation by calcium
ionophore of juvenile hormone I11 release from corpora allata of solitarious and
gregarious Locusta migratoria. Experientia 44,24&242.
David, J.-C. and Fuzeau-Braesch, S. (1979). Amines bioghes et AMP cyclique chez
Locusta migratoria: recherche de rtcepteurs i octopamine. C.r. hebd. Skanc. Acad.
Sci., Paris 288D, 1207-1210.
Dearn, J. M. (1974a). Phase transformation and chiasma frequency variations in
locusts. I. Schistocerca gregaria. Chromosoma 45, 321-338.
Dearn, J. M. (1974b). Phase transformation and chiasma frequency variations in
locusts. 11. Locusta migratoria. Chromosoma 45, 339-352.
Dearn, J. M. (1977). Pleiotropic effects associated with albino mutation in the desert
locust, Schistocerca gregaria (Forsk.), and their relationship to phase variation.
Acrida 6, 43-53.
De Wilde, J. (1975). An endocrine view of metamorphosis, polymorphism and
diapause in insects. Am. Zool. 15, Suppl. 1, 13-27.
De Wilde, J. and Beetsma, J. (1982). The physiology of caste development in social
insects. Adv. Insect Physiol. 16, 167-246.
Diederen, J. H. B., Van Etten, E. W. M., Biegstraaten, A. I. M., Terlou, M., Vullings,
H. G. B. and Jansen, W. F. (1988). Flight-induced inhibition of the cerebral
median peptidergic neurosecretory system in Locusta migratoria. Gen. comp.
Endocr. 71, 257-264.
Dingle, H. and Haskell, J. B. (1967). Phase polymorphism in the grasshopper
Melanoplus diflerentialis. Science 155, 590-592.
Dirsh, V. M. (1951). A new biometrical phase character in locusts. Nature 167, 281-
282.
Dirsh, V. M. (1953). Morphometrical studies on phases of the desert locust. Anti-
Locust Bull. 16, 1-34.
Dudley, B. (1964). The effects of temperature and humidity upon certain morpho-
metric and colour characters of the desert locust (Schistocerca gregaria Forskbl)
reared under controlled conditions. Trans. R. ent. Soc. Lond. 116, 115-126.
Ellis, P. E. (1950). Marching in locust hoppers of the solitary phase. Nature 166, 151.
Ellis, P. E. (1951). The marching behaviour of hoppers of the African migratory
locust (Locusta migratoria migratorioides R. & F.) in the laboratory. Anti-Locust
Bull. 7,1-46.
Ellis, P. E. (1959). Learning and social aggregation in locust hoppers. Anim. Behav. 7,
91-106.
60 M. P. PENER
Ellis, P. E. (1962a). Behavioural mechanisms in locust gregariousness. Symp. Genet.

Biol. Ital. (Proc. 4th Congr. int. Union Study SOC.Insects, Pavia, 1961) 10,225-234.
Ellis, P. E. (1962b). The behaviour of locusts in relation to phases and species. Colloq.
int. C N R S (“Physiologie, Comportement et Ecologie des Acridiens en Rapport
avec la Phase”) No. 114, 123-143.
Ellis, P. E. (1963a). The influence of some environmental factors on learning and
aggregation in locust hoppers. Anim. Behav. 11, 142-151.
Ellis, P. E. (1963b). Changes in the social aggregation of locust hoppers with changes
in rearing conditions. Anim. Behav. 11, 152-160.
Ellis, P. E. (1964). Changes in marching of locusts with rearing conditions. Behaviour
23, 193-202.
Ellis, P. E. and Ashall, C. (1957). Field studies on diurnal behaviour, movement and
aggregation in the desert locust (Schistocerca gregaria Forskil). Anti-Locust Bull.
25, 1-94.
Ellis, P. E. and Carlisle, D. B. (1961). The prothoracic gland and colour change in
locusts. Nature 190, 368-369.
Ellis, P. E. and Gillett, S. (1968). Social aggregation and an airborne gregarising
factor in locusts. Colloq. int. CNRS. (“L’Effet de Groupe chez les Animaux”)
NO. 173, 173-183.
Ellis, P. E. and NovLk, V. J. A. (1971). Metamorphosis hormones and phase
dimorphism in Schistocerca gregaria. I. Implantation of endocrine glands into
hoppers reared in isolation; the effects on coloration. Endocr. exp. 5, 13-18.
Ellis, P. E. and Pearce, A. (1962). Innate and learned behaviour patterns that lead to
group formation in locust hoppers. Anim. Behav. 10, 305-318.
Engelmann, F. (1983). Vitellogenesis controlled by juvenile hormone. In “Inverte-
brate Endocrinology, Vol. 1, Endocrinology of Insects” (Eds R. G. H. Downer
and H. Laufer), pp. 259-270. Alan R. Liss Inc., New York.
Evans, P. D. (1982). Properties of modulatory octopamine receptors in locusts. In
“Neuropharmacology of Insects” Ciba Foundation Symposium, No. 88 (Eds D.
Evered, M. O’Connor and J. Whelan), pp. 48-69. Pitman, London.
Fain, M. J. and Riddiford, L. M. (1975). Juvenile hormone titers in the hemolymph
during late larval development of the tobacco hornworm, Manduca sexta (L.).
Biol. Bull., Woods Hole 149, 506521.
Fain-Maurel, M. A. and Cassier, P. (1969). Etude infrastructurale des glandes de mue
de Locusta migratoria migratorioides (R. et F.). 11.-Analyse morphologique des
etapes de la degenerescence chez les irnagos gregaires. A r c h Zool. exp. gdn. 110,
91-126.
Farrow, R. A. and Colles, D. H. (1980). Analysis of the interrelationships of
geographical races of Locusta migratoria (Linneus) (Orthoptera: Acrididae) by
numerical taxonomy, with special reference to sub-speciation in the tropics and
affinities of the Australian race. Acrida 9, 77-99.
Faure, J. C. (1932). The phases of locusts in South Africa. Bull. ent. Res. 23,293424.
Faure, J. C. (1943a). The phases of the lesser army worm [Laphygmaexiqua (Hiibn.)].
Farming S . Afr. 18, 69-78.
Faure, J. C. (1943b). Phase variation in the army worm, Laphygma exempta (Walk.).
Sci. Bull. Dept. Agric. S. Afr. 234, 1-17.
Ferenz, H.-J., Lubzens (Wajc), E. and Glass, H. (1981). Vitellin and vitellogenin
incorporation by isolated oocytes of Locusta migratoria migratorioides (R. F.).
J . Insect Physiol. 27, 869-875.
Fescemyer, H. W. and Hammond, A. M. (1986). Effect of density and plant age on

color phase variation and development of larval velvetbean caterpillar, Anticarsia
gemmatalis Hiibner (Lepidoptera: Noctuidae). Env. Ent. 15, 784-789.
Fescemyer, H. W. and Hammond, A. M. (1988). The relationship between popula-
tion density, juvenile hormone, juvenile hormone esterase and phase variation in
larvae of the migrant insect. Anticarsia gemmatalis Hiibner. J . Insect Physiol. 34,
29-3 5.
Fescemyer, H. W., Rose, R. L., Sparks, T. C. and Hammond, A. M. (1986). Juvenile
hormone esterase activity in developmentally synchronous ultimate stadium
larvae of the migrant insect, Anticarsia gemmatalis. J. Insect Physiol, 32, 1055-
1063.
Feyereisen, R. (1985). Regulation of juvenile hormone titer: synthesis. In “Com-
prehensive Insect Physiology Biochemistry and Pharmacology”, Vol. 7, Endo-
crinology I (Eds G. A. Kerkut and L. I. Gilbert), pp. 391429. Pergamon Press,
Oxford.
Ford, E. B. (1961). The theory of genetic polymorphism. Symp. R. ent. Soc. Lond. 1,
11-19.
Fuzeau-Braesch, S. (1960). Etude biologique et biochimique de la pigmentation d’un
insecte: Gryllus bimaculatus De Geer (Gryllide, Orthopt2re). Bull. biol. Fr. Belg.
94, 525-627.
Fuzeau-Braesch, S . (1965). Etude du pigment cuticulaire du mutant albinos de
Locusta migratoria (Orthop.). Bull. SOC.zool. Fr. 90, 477486.
Fuzeau-Braesch, S. (1966). Etude du noircissement cuticuhire non-exuvial chez
Locusta migratoria L. J. Insect Physiol. 12, 1363-1368.
Fuzeau-Braesch, S. (1971). Contribution a l’ktude du r6le de l’hormone juvenile dans
la pigmentation. A r c h Zool. exp. gin. 112, 625-633.
Fuzeau-Braesch, S. (1972). Pigments and color changes. Annu. Rev. Ent. 17,403424.
Fuzeau-Braesch, S. (1977a). Comportement et taux de catecholamines: etude com-
parative des insectes gregaires, solitaires et trait& au gaz carbonique chez Locusta
migratoria (Insectes, Orthoptkres). C.r. hebd. Sianc. Acad. Sci., Paris 284D, 1361-
1363.
Fuzeau-Braesch, S. (1977b). Aspect neurophysiologique de la differenciation phasaire
chez le criquet migrateur: amines biogknes et permeabilitk membranaire. Bull. Soc.
zool. Fr. 102, 327-328.
Fuzeau-Braesch, S. (1985). Colour changes. In “Comprehensive Insect Physiology
Biochemistry and Pharmacology”, Vol. 9, Behaviour (Eds G. A. Kerkut and L. I.
Gilbert), pp. 549-589. Pergamon Press, Oxford.
Fuzeau-Braesch, S. and David, J.-C. (1978). Etude du taux d’octopamine chez
Locusta migratoria (Insecte, Orthopthre): comparaison entre insectes grkgaires,
solitaires et traites au gaz carbonique. C.r. hebd. Sianc. Acad. Sci., Paris 286D,
697-699.
Fuzeau-Braesch, S. and Nicolas, G. (1981). Effect of carbon dioxide on subsocial
insects. Comp. Biochem. Physiol. 68A, 289-297.
Fuzeau-Braesch, S., Nicolas, G. and Sellier, R. (1973). Etude de la pars stridens de
Locusta migratoria cinerascens (Fab.) sous differentes conditions experimentales.
Fuzeau-Braesch, S., Coulon, J. F. and David, J. C. (1 979). Octopamine levels during
the moult cycle and adult development in the migratory locust, Locusla migra-
toria. Experientia 35, 1349-1350.
62 M .P. PENER
Fuzeau-Braesch, S., Nicolas, G., Baehr, J.-C. and Porcheron, P. (1982). A study of
hormonal levels of the locust Locusta migratoria cinerascens artificially changed to
the solitary state by a chronic CO, treatment of one minute per day. Comp.
Biochem. Physiol. 71A, 53-58.
Fuzeau-Braesch, S., Genin, E., Jullien, R., Knowles, E. and Papin, C. (1988).
Composition and role of volatile substances in atmosphere surrounding two
gregarious locusts, Locusta migratoria and Schistocerca gregaria. J . chem. Ecol. 14,
1023-1033.
Gadot, M. and Applebaum, S. W. (1986). Farnesoic acid and allatotropin in relation
to locust allatal maturation. Mol. cell. Endocr. 48, 69-76.
Gadot, M., Faktor, 0. and Applebaum, S. W. (1987a). Maturation of locust corpora
allata during the reproductive cycle: effect of reserpine on allatotropic activity,
juvenile hormone-111biosynthesis and oocyte development. Archs Insect Biochem.
Physiol. 4, 17-27.
Gadot, M., Rafaeli, A. and Applebaum, S. W. (1987b). Partial purification and
characterization of locust allatotropin I. Archs Insect Biochem. Physiol. 4, 213-
223.
Gande, A. R., Morgan, E. D. and Wilson, I. D. (1979). Ecdysteroid levels throughout
the life cycle of the desert locust, Schistocerca gregaria. J . Insect Physiol. 25, 669-
675.
Gardiner, B. G. (1958). Some observations on the respiration of young nymphs of
Schistocerca gregaria (Forskkl) in relation to phase and rearing density. Proc. R .
ent. SOC. Lond. A 33, 159-166.
C h i n , E., Jullien, R., Perez, F. and Fuzeau-Braesch, S. (1986). Cuticular hydro-
carbons of gregarious and solitary locusts Locusta migratoria cinerascens.
J . chem. Ecol. 12, 1213-1238.
Gtnin, E., Jullien, R. and Fuzeau-Braesch, S. (1987). New natural aliphatic ethers in
cuticular waxes of gregarious and solitary locusts Locusta migratoria cinerascens
(11). J . chem. Ecol. 13, 265-282.
Gillett, S. (1968). Airborne factor affecting the grouping behaviour of locusts. Nature
218, 782-783.
Gillett, S. D. (1972). Social aggregation of adult Schistocerca gregaria and Locusta
migratoria migratorioides in relation to the final m,oult and ageing. Anim. Behav.
20, 52&533.
Gillett, S. D. (1973). Social determinants of aggregation behaviour in adults of the
desert locust. Anim. Behav. 21, 599-606.
Gillett, S. D. (1975a). The action of the gregarisation pheromone on five non-
behavioural characters of phase polymorphism of the desert locust, Schistocerca
gregaria (Forskbl). Acrida 4, 137-149.
Gillett, S. D. (1975b). Changes in the social behaviour of the desert locust,
Schistocerca gregaria, in response to the gregarizing pheromone. Anim. Behav. 23,
494503.
Gillett, S. D. (1983). Primer pheromones and polymorphism in the desert locust.
Anim. Behav. 31, 221-230.
Gillett, S. D. and Phillips, M. L. (1977). Faeces as a source of a locust gregarisation
stimulus. Effects on social aggregation and on cuticular colour of nymphs of the
desert locust, Schistocerca gregaria (Forsk.). Acrida 6,279-286.
Gillett, S. D., Packham, J. M. and Papworth, S. J. (1976). Possible pheromonal effects
on aggregation and dispersion in the desert locust, Schistocerca gregaria (Forsk.).
Acrida 5, 287-297.
Girardie, A. (1966). Controle de I’activite genitale chez Locusta migratoria. Mise en

ividence d’un facteur gonadotrope et d’un facteur allatotrope dans la pars
intercerebralis. Bull. Soc. zool. Fr. 91, 423439.
Girardie, A. (1 974). Recherches sur le r81e physiologique des cellules neuroskcretrices
laterales du protocerebron de Locusta migratoria migratorioides (Insecte Orthop-
tere). Zool. Jb. (Physiol.) 78, 31G-326.
Girardie, A. and Cazal, M. (1965). R81e de la pars intercerebralis et des corpora
cardiaca sur la melanisation chez Locusta migratoria (L.). C.r. hebd. SCanc. Acad.
Sci.,Paris, Groupe 12 261, 4525-4527.
Girardie, A. and Joly, P. (1968). Micanisme physiologique de I’effet de groupe chez
les acridiens. Collog. int. C N R S (“L‘Effet de Groupe chez les Animaux”) No. 173,
127-145.
Girardie, A. and Vogel, A. (1966). Etude du contr6le neuro-humoral de I’activite
sexuelle mlle de Locusta migratoria (L.). C.r. hebd. Sianc. Acad. Sci., Paris 263D,
543-546.
Goldsworthy, G. J. (1983). The endocrine control of flight metabolism in locusts.
Adv. Insect Physiol. 17, 149-204.
Goldsworthy, G. J., Johnson, R. A. and Mordue, W. (1972). In vivo studies on the
release of hormones from the corpora cardiaca of locusts. J . comp. Physiol. 79,85-
96.
Goldsworthy, G. J., Coupland, A. J. and Mordue, W. (1973). The effects of corpora
cardiaca on tethered flight in the locust. J. comp. Physiol. 82, 339-346.
Goldsworthy, G. J., Lee, S. S. and Jutsum, A. R. (1977). Cerebral neurosecretory cells
and flight in the locust. J. Insect Physiol. 23, 717-721.
Goodwin, T. W. (1952). The biochemistry of locust pigmentation. Biol. Rev. 27,439-
460.
Goodwin, T. W. and Srisukh, S. (1951). Biochemistry of locusts. 5. The green pigment
of the haemolymph and integument of solitary locusts (Locusta migratoria
migratorioides, R. & F., and Schistocerca gregaria, Forsk.). Biochem. J. 48, 199-
203.
Goosey, M. W. and Candy, D. J. (1980). The o-octopamine content of the
haemolymph of the locust, Schistocerca americana gregaria and its elevation
during flight. Insect Biochem. 10, 393-397.
Granger, N. A. and Goodman, W. G. (1983). Juvenile hormone radioimmuno-
assays-theory and practice. Insect Biochem. 13, 333-340.
Greenwood, M. and Chapman, R. F. (1984). Differences in numbers of sensilla on the
antennae of solitarious and gregarious Locusta migratoria L. (Orthoptera: Acridi-
dae). Int. J . Insect Morphol. Embryol. 13, 295-301.
Gunn, D. L. (1960). The biological background of locust control. Annu. Rev. Ent. 5,
279-300.
Gunn, D. L. and Hunter-Jones, P. (1952). Laboratory experiments on phase
differences in locusts. Anti-Locust Bull. 12, 1-29.
Halbwachs, M. C., Joly, L. and Joly, P. (1957). Resultats d’implantations de “glandes
ventrales” a Locusta migratoria L. J . Insect Physiol. 1, 143-149.
Hardie, J. and Lees, A. D. (1985). Endocrine control of polymorphism and
polyphenism. In “Comprehensive Insect Physiology Biochemistry and Pharma-
cology”, Vol. 8, Endocrinology I1 (Eds G. A. Kerkut and L. I. Gilbert), pp. 441-
490. Pergamon Press, Oxford.
Harvey, A. W. (198 1). A reclassification of the Schistocerca americana complex
(Orthoptera: Acrididae). Acrida 10, 61-77.
64 M. P. PENER
Haskell, P. T. and Moorhouse, J. E. (1963). A blood-borne factor influencing the

activity of the central nervous system of the desert locust. Nature 197, 5658.
Hertz, M. and Imms, A. D. (1937). On the responses of the African migratory locust
to different types of background. Proc. R. SOC.B 122, 281-297.
Highnam, K. C. and Haskell, P. T. (1964). The endocrine systems of isolated and
crowded Locusta and Schistocerca in relation to oocyte growth, and the effects of
flying upon maturation. J . Insect Physiol. 10, 849-864.
Highnam, K. C., Lusis, 0. and Hill, L. (1963). The role of the corpora allata during
oocyte growth in the desert locust, Schistocerca gregaria Forsk. J. Insect Physiol.
9, 587-596.
Hirn, M., Hetru, C . , Lagueux, M. and Hoffmann, J. A. (1979). Prothoracic gland
activity and blood titres of ecdysone and ecdysterone during the last larval instar
of Locusta migratoria L. J . Insect Physiol. 25, 255-261.
Hoffmann, J. A. and Koolman, J. (1974). Prothoracic glands in the regulation of
ecdysone titres and metabolic fate of injected labelled ecdysone in Locusta
migratoria. J . Insect Physiol. 20, 1593-1 601.
Hoffmann, J. A. and Weins, M.-J. (1974). Activitt proteosynthetique des glandes
prothoraciques en titre d’ecdysone chez des larves permanentes de Locusta
migratoria obtenues par irradiation stlective du tissu hCmatopoYetique. Experien-
tia 30, 821-822.
Huibregtse-Minderhoud, L., Van den Hondel-Franken, M. A. M., Van der Kerk-Van
Hoof, A. C., Biessels, H. W. A., Salemink, C. A,, Van der Horst, D. J. and
Beenakkers, A. M. Th. (1980). Quantitative determination of the juvenile
hormones in the haemolymph of Locusta migratoria during normal development
and after implantation of corpora allata. J. Insect Physiol. 26, 627-63 1.
Hunter-Jones, P. (1958). Laboratory studies on the inheritance of phase characters in
locusts. Anti-Locust Bull. 29, 1-32.
Hunter-Jones, P. (1962). Coloration of the desert locust (Schistocerca gregaria
Forskil) reared in isolation. Entomologist’s mon. Mag. 98, 89-92.
Injeyan, H. S. and Tobe, S. S. (1981a). Phase polymorphism in Schistocerca gregaria:
reproductive parameters. J. Insect Physiol. 27, 97-102.
Injeyan, H. S. and Tobe, S. S. (1981b). Phase polymorphism in Schistocerca gregaria:
assessment of juvenile hormone synthesis in relation to vitellogenesis. J. Insect
Physiol. 27, 203-210.
Injeyan, H. S., Tobe, S. S. and Rapport, E. (1979). The effects of exogenous juvenile
hormone treatment on embryogenesis in Schistocerca gregaria. Can. J. Zool. 57,
838-845.
Injeyan, H. S., Dale, J. F. and Tobe, S. S. (1981). Increased juvenile hormone
synthesis and decreased fertility in aging Schistocerca gregaria. Can. J . Zool. 59,
1744-1748.
Ismail, S., Porcheron, P. and Fuzeau-Braesch, S. (1979). Taux des ecdysteroides chez
des adultes de Locusta migratoria cinerascens solitaires, gregaires et trait& par le
gaz carbonique. C.r. Sianc. SOC.Biol. 173, 553-557.
Iwao, S. (1962). Studies on the phase variation and related phenomena in some
lepidopterous insects. Mem. Coll. Agric. Kyoto Univ. 84, 1-80.
Jago, N. D. (1985). The evolutionary interrelationships of phase attributes and
mobility in the acridoidea. In “Proceedings, 3rd Triennial Meeting, Pan American
Acridological Society” (Ed. D. A. Nickle), pp. 65-9 1. Pan American Acridological
Society, Detroit, Michigan.
Jago, N. D., Antoniou, A. and Scott, P. (1979). Laboratory evidence showing the
separate species status of Schistocerca gregaria, americana and cancellata (Acri-
didae: Cyrtacanthacridinae). Syst. Ent. 4, 133-142.
Joly, L. (1954). Resultats d’implantations systematiques de corpora allata a de jeunes
larves de Locusta migratoria L. C.r. Sianc. SOC.Biol. 148, 579-583.
Joly, L. (1960). “Fonctions des Corpora Allata chez Locusta migratoria (L.).” These,
Strasbourg.
Joly, L. and Joly, P. (1974). Comparaison de la phase gregaire et de la phase solitaire
de Locusta migratoria migratorioides (Orthoptere) du point de vue de la teneur de
leur hemolymphe en hormone juvenile. C.r. hebd. Sianc. Acad. Sci., Paris 279D,
1007-1009.
Joly, L. and Schneider, M. (1976). Une propritte physiologique des glandes prothora-
ciques des insectes non liee a la production d’ecdysone. C.r. hebd. Sianc. Acad.
Sci., Paris 282D, 1437-1439.
Joly, L., Joly, P. and Porte, A. (1969). Remarques sur I’ultrastructure de la glande
ventrale de Locusta migratoria L. (Orthoptere) en population dense. C.r. hebd.
Stanc. Acad. Sci., Paris 269D, 917-918.
Joly, L., Hoffmann, J. and Joly, P. (1977). Controle humoral de la differenciation
phasaire chez Locusta migratoria migratorioides (R. & F.) (Orthopteres). Acrida 6,
3342.
Joly, P. (1 949). Le systbme endocrine retrockrkbral chez les acridiens migrateurs.
Annls Sci. nat. (Zool.) Sir. I 1 11, 255-262.
Joly, P. (1951). Determinisme endocrine de la pigmentation chez Locusta migratoria
L. C.r. Sianc. SOC.Biol. 145, 1362-1364.
Joly, P. (1952). Determinisme de la pigmentation chez Acrida turrita L. (Insecte
Orthopteroide). C.r. hebd. Seanc. Acad. Sci., Paris 235, 1054-1056.
Joly, P. (1956). Croissance et indices de grkgarisation chez Locusta migratoria (L.).
Insectes SOC. 3, 17-24.
Joly, P. (1962). R61e jouk par les corpora allata dam la realisation du polymorphisme
de phase chez Locusta migratoria L. Colloq. int. C N R S (“Physiologie, Comporte-
ment et Ecologie des Acridiens en Rapport avec la Phase”) No. 114, 77-88.
Joly, P. (1968). “Endocrinologie des Insectes.” Masson & Cie., Editeurs, Paris.
Joly, P. and Joly, L. (1954). RCsultats de greffes de corpora allata chez Locusta
migratoria L. Annls Sci. nut. (Zool.) Sir. I 1 15 (1953), 331-345.
Joly, P. and Meyer, A. S. (1970). Action de I’hormone juvenile sur Locusta migratoria
(Orthoptere) en phase gregaire. Archs Zool. exp. gin. 111, 51-63.
Joly, P., Joly, L. and Halbwachs, M. (1956). Controle humoral de developpement
chez Locusta migratoria. Annls Sci. nut. (Zool.) Sir. I 1 18, 257-261.
Jutsum, A. R. and Goldsworthy, G. J. (1977). The role of the glandular lobes of the
corpora cardiaca during flight in Locusta. Physiol. Ent. 2, 125-132.
Keeley, L. L. (1988). Potential application of neuroendocrine research to insect
control. In “Biotechnology for Crop Protection”, American Chemical Society
Series, No. 379 (Eds P. A. Hedin, J. J. Menn and R. M. Hollingworth), pp. 147-
159. American Chemical Society, Washington, DC.
Keeley, L. L. and Hayes, T. K. (1987). Speculations on biotechnology appEcations
for insect neuroendocrine research. Insect Biochem. 17, 639-65 1.
Kennedy, J. S. (1956). Phase transformation in locust biology. Bioi. Rev. 31, 349-
370.
Kennedy, J. S. (1961). Continuous polymorphism in locusts. Symp. R . ent. SOC.Lond.
1, 8C90.
66 M .P. PENER
Kennedy, J. S. (1962). La division du travail entre les phases acridiennes. Colloq. int.
C N R S (“Physiologie, Comportement et Ecologie des Acridiens en Rapport avec la
Phase”) No. 114, 269-297.
Key, K. H. L. (1950). A critique on the phase theory of locusts. Q. Rev. Biol. 25, 363-
407.
Key, K. H. L. (1957). Kentromorphic phases in three species of Phasmatodea. Aust.
J . Zool. 5, 247-284.
Kramer, S. J. and Kalish, F. (1984). Regulation of the corpora allata in the black
mutant of Manduca sexta. J. Insect Physiol. 30, 31 1-316.
Kuqukekgi, S. (1969). Some observations on the endocrine systems in the embryos of
the gregarious and solitary phases of Schistocerca gregaria (Forsk.) (Orthoptera:
Acrididae). I-The ventral head glands. Cornmuns Fac. Sci. Univ. Ankara, Sir. C,
Sci. nut. 14C, 1-21.
Kutsch, W. (1983). Aspects of the ontogeny of locust flight. In “Biona Report No. 2,
Physiology and Biophysics of Insect Flight, Special Aspects 11” (Ed. W. Nachti-
gall), pp. 71-79. Gustav Fischer, Stuttgart.
Lauga, J. (1974). Analyse biomktrique du polymorphisme des nouveaux-nes chez
Locusta migratoria. Acrida 3, 277-284.
Lauga, J. (1976a). Analyse morphometrique de la differenciation phasaire durant la
croissance de Locusta migratoria L. (Orthoptere, Acrididae). Bull. Soc. Hist. nut.
Toulouse 112, 327-333.
Lauga, J. (1976b). “Recherches Quantitatives sur le Polymorphisme Phasaire du
Criquet Migrateur Locusta migratoria L (Insecte, Orthoptere).” These, Universite
Paul Sabatier, Toulouse.
Lauga, J. (1977a). Le probleme de la mesure de la phase chez les acridiens migrateurs:
historique et definition d’echelles phasaires chez Locusta migratoria L. (Insecte,
Orthoptere). Archs Zool. exp. gPn. 118, 247-272.
Lauga, J. (1977b). Nature et determination du polymorphisme phasaire morphologi-
que des larves nouveau-nees de Locusta migratoria migratorioides (R.& F.).
Acrida 6 , 239-247.
Lazarovisi, P. and Pener, M. P. (1977). Juvenile hormones (JHs) and completion of
oocyte development in the African migratory locust: A comparative and quantita-
tive study. Gen. comp. Endocr. 33, 434452.
Lea, A. and Webb, D. van V. (1939). Field observations on the red locust at Lake
Rukwa in 1936 and 1937. Sci. Bull. Dept. Agric. Un. S. Afr. 189, 1-81.
Lee, S. S. and Goldsworthy, G. J. (1975). Alletectomy and flight performance in male
Locusta migratoria. J. comp. Physiol. 100, 351-359.
Lee, S. S. and Goldsworthy, G. J. (1976). The effect of allatectomy and ovariectomy
on flight performance in female Locusta migratoria migratorioides (R. & F.).
Acrida 5, 169-1 80.
Lees, A. D. (1961). Clonal polymorphism in aphids. Symp. R. ent. SOC.Lond. 1, 68-
79.
Lees, A. D. (1983). The endocrine control of polymorphism in aphids. In “Inverte-
brate Endocrinology”, Vol. 1, Endocrinology of Insects (Eds R. G. H. Downer
and H. Laufer), pp. 369-377. Alan R. Liss, Inc., New York.
Lespinasse, R. (1973). Comportement des chromosomes surnumkraries et relation
avec le taux de mortalite dans une population africaine de Locusta migratoria
migratorioides. Chromosoma 44, 107-122.
Lespinasse, R. (1977). Analyse de la transmission des chromosomes surnumeraires

chez Locusta migratoria migratorioides R. et F. (Orthoptera, Acrididae). Chromo-
soma 59, 307-322.
Lespinasse, R. and Nicolas, G. (1975). Presence de chromosomes surnumeraires et
aptitude a la realisation du phenotype solitaire chez le criquet migrateur Locusta
migratoria migratorioides R. et F. Reactivite pigmentaire sous les effets du CO,.
Lespinasse, R. and Nicolas, G. (1 98 1). Correlation between B chromosome frequency
and solitary phenotype production in crowded populations treated with CO, in
different strains of Locusta migratoria L. In “Biosystematics of Social Insects”
(Eds P. E. Howse and J.-L. Clement), pp. 95-106. Academic Press, New York.
Loher, W. (1961). The chemical acceleration of the maturation process and its
hormonal control in the male of the desert locust. Proc. R . SOC.B 153 (1960), 380-
397.
Loher, W., Ruzo, L., Baker, F. C., Miller, C. A. and Schooley, D. A. (1983).
Identification of the juvenile hormone from the cricket, Teleogryllus commodus,
and juvenile hormone changes. J . Insect Physiol. 29, 585-589.
Long, D. 8. (1953). Effects of population density on larvae of Lepidoptera. Trans. R.
ent. SOC.Lond. 104, 543-585.
Lukoschus, F. (1955). Stoffwechselvorgange wahrend der Entwicklung von Konigin
und Arbeiterin und ihre mogliche Bedeutung fur die kiinstliche Aufzucht von
Koniginnen. Z . Bienenforsch. 3, 40-45.
Luscher, M. (1961). Social control of polymorphism in termites. Symp. R. ent. SOC.
Lond. 1, 57-67.
Liischer, M. (Ed.) (1976a). “Phase and Caste Determination in Insects-Endocrine
Aspects.” Pergamon Press, Oxford.
Liischer, M. (1976b). Introduction. In “Phase and Caste Determination in Insects-
Endocrine Aspects” (Ed. M. Liischer), pp. 1 4 . Pergamon Press, Oxford.
Marty, R., Fuzeau-Braesch, S. and Zalta, J.-P. (1972). Influence de la “gregarisation”
et de la “solitarisation” sur la composition qualitative et quantitative de I’hemo-
lymphe de Locusta migratoria (L.) cinerascens mutant albinos. C.r. hebd. Skanc.
Acad. Sci., Paris 274D, 556-559.
Matsumoto, S., Isogai, A. and Suzuki, A. (1988). Purification and characterization of
melanization and reddish coloration hormone (MRCH) in lepidopteran insects. In
“Advances in Pigment Cell Research”, pp. 437-451. Alan R. Liss Inc., New York.
Matthee, J. J. (1945). Biochemical differences between the solitary and gregarious
phases of locusts and noctuids. Bull. ent. Res. 36, 343-371.
Matthee, J. J. (1946). A study of the phases of the army worm (Laphygma exempta
Walk.). J. ent. SOC.S . Afr. 9, 6&77.
Matthee, J. J. (1947). Phase variation in the lawn caterpillar (Spodoptera abyssinia
Guen.). J. ent. SOC.S. Afr. 10, 16-23.
May, I. R. (1971). Phase polymorphism in locusta species. J. S . Afr. biol. Sci. 12, 23-
57.
Menn, J. J. and Bofkovec, A. B. (1989). Insect neuropeptides: potential new insect
control agents. J.,agric. Food Chem. 37, 271-278.
Michel, R. (1970a). Etude experimentale des variations de la tendance au vol chez le
criquet pelerin Schistocerca gregaria (Forsk.), eleve. isolement pendant plusieurs
generations. Insectes S O C . 17, 21-38.
68 M. P. PENER
Michel, R. (1970b). Etude experimentale de l’activitk maximum de vol journaliere du

criquet pelerin (Schistocerca gregaria Forsk) elevtt en groupe ou en isolement.
Behaviour 36, 28C-299.
Michel, R. (1972a). Etude experimentale de l’influence des glandes prothoraciques sur
I’activite de vol du criquet pklerin Schistocerca gregaria. Gen. comp. Endocr. 19,
96-101.
Michel, R. (1972b). Influence des corpora cardiaca sur les possibilitks de vol soutenu
du criquet pelerin Schistocerca gregaria. J. Insect Physiol. 18, 1811-1827.
Michel, R. (1973a). Influence des corpora allata et de mimetique d’hormone juvenile
sur la tendance au vol soutenu du criquet pelerin Schistocerca gregaria (Forsk.)
eleve en groupe dense o u en isolement. Archs 2001. exp. gen. 114, 187-21 1.
Michel, R. (1973b). Variations de la tendance au vol soutenu du criquet pelerin
Schistocerca gregaria apres implantations de corpora cardiaca. J. Insect Physiol.
19, 1317-1325.
Michel, R. (1980a). Etude au laboratoire du dtveloppement possible de l’activitk
migratrice chez le criquet pelerin, Schistocerca gregaria, lors des invasions et des
rkessions. Behaviour 75, 251-261.
Michel, R. (1980b). Development of flight behaviour of successive generations of
desert locust (Schistocerca gregaria) raised in isolation then in groups. Anim.
Behav. 28, 1288-1289.
Michel, R. and Bernard, A. (1973). Influence de la pars intercerebralis sur l’induction
au vol soutenu chez le criquet pelerin Schistocerca gregaria. Acrida 2, 139-149.
Michelmore, A. P. G. and Allan, W. (1934). Observations on phases of the red-
winged locust in Northern Rhodesia. Bull. ent. Res. 25, 101-128.
Michener, C. D. (1961). Social polymorphism in Hymenoptera. Symp. R . en?. Soc.
Lond. 1, 43-56.
Mordue, W. and Goldsworthy, G. J. (1974). Some recent progress in acridid
endocrinology. Acrida 3, IX-XXXVIII.
Mordue (Luntz), A. J. (1977). Some effects of amputation of the antennae on
pigmentation, growth and development in the locust, Schistocerca gregaria.
Physiol. Ent. 2, 293-300.
Moreteau, 3. (1 975). Fonction chromatotrope de la pars intercerebralis chez l’acri-
dien Oedipoda coerulescens. J. Insect Physiol. 21, 1407-1413.
Moreteau-Levita, B. (1972a). R81e de la pars intercerebralis dans la realisation de
l’homochromie d’Oedipoda coerulescens L. (Acridien, Orthoptere). C.r. hebd.
Sianc. Acad. Sci., Paris 274D, 3277-3279.
Moreteau-Levita, B. (1972b). R6le des corpora cardiaca dans la pigmentation
d’oedipoda coerulescens L. (Acridien, Orthoptere). C.r. hebd. Sianc. Acad. Sci.,
Paris 275D, 2699-2701.
Morton, D. B. and Evans, P. D. (1983). Octopamine distribution in solitarious and
gregarious forms of the locust, Schistocerca americana gregaria. Insect Biochem.
13. 177-183.
Needham, A. E. (1978). Insect biochromes: their chemistry and role. In “Bio-
chemistry of Insects” (Ed. M. Rockstein), pp. 233-305. Academic Press, New
York.
Ngmec, V. (1971). Effets de certains analogues de l’hormone juvCnile sur deux especes
de criquets: Locusta migratoria migratorioides (R. et F.) et Schistocerca gregaria
(Forsk). Archs Zool. exp. gin. 112, 511-517.
NEmec, V., Jarolim, V., Hejno, K. and Sorm, F. (1970). Natural and synthetic
materials with insect hormone activity. 7. Juvenile activity of the farnesane-type
compounds on Locusta migratoria L. and Schistocerca gregaria (Forsk.). Life Sci.

(Part iZ,J 9, 821-831.
Nickerson, B. (1954). A possible endocrine mechanism controlling locust pigmen-
tation. Nature 174, 357-358.
Nickerson, B. (1956). Pigmentation of hoppers of the desert locust (Schistocerca
gregaria Forskil) in relation to phase coloration. Anti-Locust Bull. 24, 1-34.
Nicolas, G. (1977). Recherche du r61e de I’hormone juvenile dans la realisation de
I’homochromie chez le criquet migrateur, Locusta migratoria L. Utilisation d’une
hormone juvenile synthetique. C.r. Seanc. SOC.Biol. 171, 503-507.
Nicolas, G. and Isma’il, S. (1978). Realisation expkrimentale de l’assombrissement
tkgumentaire chez le criquet migrateur Locusta migratoria L. Influence des
neurosecrttions cerkbrales: comparaison avec les effets du CO,. C.r. Seanc. SOC.
Biol. 172, 1075-1078.
Nijhout, H. F. and Wheeler, D. E. (1982). Juvenile hormone and the physiological
basis of insect polymorphism. Q. Rev. Biol. 57, 109-133.
Nolte, D. J. (1963). A pheromone for melanization of locusts. Nature 200, 66G661.
Nolte, D. J. (1964a). Chiasma frequency and gregarization in locusts. Nature 204,
11 10-1 11 1.
Nolte, D. J. (1964b). The nuclear phenotype of locusts. Chromosoma 15, 367-388.
Nolte, D. J. (1965). The pigmentation of locusts. S. Afr. J . Sci. 61, 173-178.
Nolte, D. J. (1967). Phase transformation and chiasma formation in locusts.
Chromosoma 21, 123-139.
Nolte, D. J. (1968). The chiasma-inducing pheromone of locusts. Chromosoma 23,
346-358.
Nolte, D. J. (1974). The gregarization of locusts. Biol. Rev. 49, 1-14.
Nolte, D. J. (1976). Locustol and its analogues. J. insect Physiol. 22, 833-838.
Nolte, D. J. (1977). The action of locustol. J. insect Physiol. 23, 899-903.
Nolte, D. J., May, I. R. and Thomas, B. M. (1970). The gregarisation pheromone of
locusts. Chromosoma 29, 462473.
Nolte, D. J., Eggers, S. H. and May, I. R. (1973). A locust pheromone: locustol.
J . insect Physiol. 19, 1547-1554.
Norris, M. J. (1950). Reproduction in the African migratory locust (Locusta
migratoria migratorioides R. & F.) in relation to density and phase. Anti-Locust
Bull. 6, 1-48.
Norris, M. J. (1952). Reproduction in the desert locust (Schistocerca gregaria Forsk.)
in relation to density and phase. Anti-Locust Bull. 13, 1 4 9 .
Norris, M. J. (1954). Sexual maturation in the desert locust (Schistocerca gregaria
Forskil) with special reference to the effects of grouping. Anti-Locust Bull. 18,
144.
Norris, M. J. (1959). Reproduction in the red locust (Nomadacris septemfasciata
Serville) in the laboratory. Anti-Locust Bull. 36, 1 4 6 .
Norris, M. J. (1963). Laboratory experiments on gregarious behaviour in ovipositing
females of the desert locust, Schistocerca gregaria. Entomologia exp. appl. 6, 279-
303.
Norris, M. J. (1964). Accelerating and inhibiting effects of crowding on sexual
maturation in two species of locusts. Nature 203, 784-785.
Norris, M. J. (1970). Aggregation response in ovipositing females of the desert locust
with special reference to the chemical factor. J . insect Physiol. 16, 1493-1515.
70 M. P. PENER
Norris, M. J. and Pener, M. P. (1965). An inhibitory effect of allatectomized males

and females on the sexual maturation of young male adults of Schistocerca
gregaria (Forsk.) (Orthoptera: Acrididae). Nature 208, 1 122.
Novak, V. J. A. and Ellis, P. E. (1967). The metamorphosis hormones and the phase
dimorphism in Schistocerca gregaria. 11. Implantation of the glands into hoppers
reared in crowded conditions. Gen. comp. Endocr. 9, 477478.
Odhiambo, T. R. (1965). Metabolic effects of the corpus allatum hormone in the
desert locust, Schistocerca gregaria. Nature 207, 1314-13 15.
Odhiambo, T. R. (1966a). Growth and the hormonal control of sexual maturation in
the male desert locust, Schistocerca gregaria (Forskil). Trans. R . ent. SOC.Lond.
118, 393412.
Odhiambo, T. R. (1966b). The metabolic effects of the corpus allatum hormone in the
male desert locust. I. Lipid metabolism. J. exp. Biol. 45, 45-50.
Odhiambo, T. R. (1966~).The metabolic effects of the corpus allatum hormone in the
male desert locust. 11. Spontaneous locomotor activity. J . exp. Biol. 45, 5143.
Orchard, I. (1982). Octopamine in insects: neurotransmitter, neurohormone, and
neuromodulator. Can. J. Zool. 60, 659-669.
Orchard, I. (1987). Adipokinetic hormones-an update. J. Insect Physiol. 33, 451-
463.
Orchard, I. and Lange, A. B. (1983). The hormonal control of haemolymph lipid
during flight in Locusta migratoria. J . Insect Physiol. 29, 639-642.
Orchard, I. and Lange, A. B. (1984). Cyclic AMP in locust fat body: correlation with
octopamine and adipokinetic hormones during flight. J . Insect Physiol. 30, 901-
904.
Orchard, I., Loughton, B. G . and Webb, R. A. (1981). Octopamine and short-term
hyperlipaemia in the locust. Gen. comp. Endocr. 45, 175-180.
Orchard, I., Carlisle, J. A., Loughton, B. G., Gole, J. W. D. and Downer, R. G. H.
(1982). In vitro studies on the effects of octopamine on locust fat body. Gen. comp.
Endocr. 48, 7-13.
Padgham, D. E. (1976a). Control of melanization in first instar larvae of Schistocerca
gregaria. J. Insect Physiol. 22, 1409-1419.
Padgham, D. E. (1976b). Bursicon-mediated control of tanning in melanizing and
non-melanizing first instar larvae of Schistocerca gregaria. J. Insect Physiol. 22,
1447-1 452.
Papillon, M. (1960). Etude preliminaire de la rtpercussion du groupement de parents
sur les larves nouveau-nCes de Schistocerca gregaria Forsk. Bull. biol. Fr. Belg. 94,
203-263.
Papillon, M. (1968). Facteurs ecologiques et phases chez le criquet piilerin, Schisto-
cerca gregaria (Forsk.) 11-Influence de la densite des populations. Bull. biol. 102,
271-307.
Papillon, M. (1970). Influence du groupement des adultes sur leur fecondite et sur le
polymorphisme de leur descendance chez le criquet pelerin Schistocerca gregaria
Forsk. Colloq. int. CNRS (“L’lnfluence des Stimuli Externes sur la GamCtogenbe
des Insectes”) No. 189, 71-86.
Passama-Vuillaume, M. (1965). Etude du pigment vert chez Locusta migratoria L.
normal et albinos. Bull. SOC.zool. Fr. 90, 485492.
Pener, M. P. (1965a). Comparative studies on oxygen consumption in the albino and
normal strains of Schistocerca gregaria bred under crowded and isolated con-
ditions. Proc. 12th int. Congr. Ent. (London, 1964), 222-223.
Pener, M. P. (1965b). On the influence of corpora allata on maturation and sexual

behaviour of Schistocerca gregariu. J . Zool. 147, 119-1 36.
Pener, M. P. (1967a). Effects of allatectomy and sectioning of the nerves of the
corpora allata on oocyte growth, male sexual behaviour, and colour change in
adults of Schistocerca gregariu. J. Insect Physiol. 13, 665-684.
Pener, M. P. (1967b). Comparative studies on reciprocal interchange of the corpora
allata between males and females of adult Schistocerca gregaria (ForskB1) (Orth-
optera: Acrididae). Proc. R. ent. Soc. Lond. A 42, 139-148.
Pener, M. P. (1968). The effect of corpora allata on sexual behaviour and “adult
diapause” in males of the red locust. Entomologiu exp. uppl. 11, 94-100.
Pener, M. P. (1972). The corpus allatum in adult acridids: the inter-relation of its
functions and possible correlations with the life cycle. In “Proceedings of the
International Study Conference on the Current and Future Problems of Acrido-
logy” (London, 1970) (Eds C. F. Hemming and T. H. C. Taylor), pp. 135-147.
Centre for Overseas Pest Research, London.
Pener, M. P. (1976a). The differential effect of the corpora allata on male sexual
behaviour in crowded and isolated adults of Locustu migratoria migratorioides
(R.& F.). Acrida 5, 189-206.
Pener, M. P. (1976b). The differential effect of the corpora allata on yellow coloration
in crowded and isolated Locustu migrutoriu rnigrutorioides (R. & F.) males. Acridu
5, 269-285.
Pener, M. P. (1983). Endocrine aspects of phase polymorphism in locusts. In
“Invertebrate Endocrinology”, Vol. 1, Endocrinology of Insects (Eds R. G. H.
Downer and H. Laufer), pp. 379-394. Alan R. Liss Inc., New York.
Pener, M. P. (1985). Hormonal effects on flight and migration. In “Comprehensive
Insect Physiology Biochemistry and Pharmacology”, Vol. 8, Endocrinology I1
(Eds G. A. Kerkut and L. I. Gilbert), pp. 491-550. Pergamon Press, Oxford.
Pener, M. P. (1986). Endocrine aspects of mating behavior in acridids. In “Proceed-
ings, 4th Triennial Meeting, Pan American Acridological Society” (Ed. D. A.
Nickle), pp. 9-26. Pan American Acridological Society, Detroit, Michigan.
Pener, M. P. and Lazarovigi, P. (1979). Effect of exogenous juvenile hormones on
mating behaviour and yellow colour in allatectomized adult male desert locusts.
Physiol. Ent. 4, 251-261.
Pener, M. P., Girardie, A. and Joly, P. (1972). Neurosecretory and corpus allatum
controlled effects on mating behavior and color change in adult Locusta migrutoria
migratorioides males. Gen. comp. Endocr. 19, 494-508.
Pener, M. P., Orshan, L. and De Wilde, J. (1978). Precocene I1 causes atrophy of
corpora allata in Locusta migrutoriu. Nature 272, 350-353.
Pener, M. P., Dessberg, D., Lazarovisi, P., Reuter, C. C., Tsai, L. W. and Baker, F. c.
(1986). The effect of a synthetic precocene on juvenile hormone I11 titre in late
Locusta eggs. J. Insect Physiol. 32, 853-857.
Queinnec, Y. (1973). Analyse de la rtactivitt cardiaque de Locustu migratoria
rnigrutorioides(R. et F.) a la lumiere et a d’autres stimulations externes. Comparai-
son entre les phases. Insectes SOC.20, 157-188.
Raabe, M. (1982). “Insect Neurohormones.” Plenum Press, New York and London.
Raabe, M. (1983). Pigment metabolism. In “Invertebrate Endocrinology”, Vol 1,
Endocrinology of Insects (Eds R. G. H. Downer and H. Laufer), pp. 493-500.
Alan R. Liss Inc., New York.
Rainey, R. C. (1963). Meteorology and the migration of desert locusts. World
Meteorol, Org., Tech. Note No. 54 (also as Anti-Locust Mem. No. 7), 1-1 15.
72 M. P. PENER
Rainey, R. C. (1976). Flight behaviour and features of the atmospheric environment.

In “Insect Flight”, Symposium of the Royal Entomological Society, London,
No. 7 (Ed. R. C. Rainey), pp. 75-1 12. Blackwell, Oxford.
Reichhart, J. M. and Charlet, M. (1986). Ecdysiotropic activity in brains and corpora
cardiaca of larvae and adults of Locusta migratoria: in vitro assays. Int. J.
Invertebr. Reprod. Dev. 10, 17-25.
Richards, 0. W. (1961). An introduction to the study of polymorphism in insects.
Symp. R. ent. SOC.Lond. 1, 1-10,
Robinson, D. J. and Hartley, J. C. (1978). Laboratory studies of a tettigoniid (Insecta:
Orthoptera) Ruspolia dzzerens (Serville): colour polymorphism. J. nat. Hist. 12,
81-86.
Rothschild, M., Gardiner, B., Mummery, R. and Valadon, G. (1977). Carotenoids in
solitaria and gregaria phases of the locust, Schistocerca gregaria fed on artificial
and natural diets. J . Zool. 181, 475494.
Roussel, J.-P. (1963a). Etude de la consommation d’oxygene chez Locusta migratoria
L. J . Insect Physiol. 9, 349-361.
Roussel, J.-P. (1963b). Consommation d’oxygene apres ablation des corpora allata
chez des femelles adultes de Locusta migratoria L. J. Insect Physiol. 9, 721-725.
Roussel, J.-P. (1972a). Difference phasaire de rythme cardiaque chez Locusta
migratoria L. C.r. hebd. Seanc. Acad. Sci., Paris 274D, 2071-2073.
Roussel, J.-P. (1972b). Le rythme cardiaque de la phase solitaire de Locusta
migratoria L. Bull. SOC.zool. Fr. 97, 171-179.
Roussel, J.-P. (1973). Realisation de la difference phasaire du rythme cardiaque chez
Locusta migratoria L. I. Vie larvaire. Experientia 29, 433435.
Roussel, J.-P. (1975a). Realisation de la difference phasaire du rythme cardiaque chez
Locusta migratoria L. 11. Vie imaginale. Bull. Soc. zool. Fr. 100, 323-326.
Roussel, J.-P. (1975b). Rythme cardiaque aprks ablation des corpora allata dans la
phase solitaire de Locusta rnigratoria L. C.r. hebd. Seanc. Acad. Sci., Paris 280D,
85-88.
Roussel, J.-P. (1975~).Le rhythme cardiaque des adultes solitaires de premiire
generation chez I’insecte Orthoptkre Locusta migratoria L., prive de ses corpora
allata. C.r. Congr. natn. SOC.Savantes 99 (BesanGon, 1974) Sci. F a x . 3, 11-15.
Roussel, J.-P. (1975d). Action juvenilisante, chromatotrope, gonadotrope, et cardio-
trope de-JH-I11 sur Locusta migratoria. J . Insect Physiol. 21, 1007-1015.
Roussel, J.-P. (1976a). Activite comparee des hormones juveniles en C-18 (JH-I) et en
(2-16 (JH-111) chez Locusta migratoria. J. Insect Physiol. 22, 83-88.
Roussel, J.-P. (1976b). Activite de I’hormone juvenile en C,, (JH-11) chez Locusta
migratoria. J . Insect Physiol. 22, 729-733.
Roussel, J.-P. and Perron, J.-M. (1974). Action de substances mimttiques de
l’hormone juvenile sur Schistocerca gregaria Forsk. Archs Zool. exp. gin. 115,
251-262.
Rowell, C. H. F. (1967). Corpus allatum implantation and green/brown polymor-
phism in three African grasshoppers. J . Insect Physiol. 13, 1401-1412.
Rowell, C. H. F. (1971). The variable coloration of the acridoid grasshoppers. Adv.
Insect Physiol. 8, 145-198.
Safranek, L. and Riddiford, L. M. (1975). The biology of the black larval mutant of
the tobacco hornworm, Manduca sexta. J . Insect Physiol. 21, 1931-1938.
Schooley, D. A., Baker, F. C., Tsai, L. W., Miller, C. A. and Jamieson, G. C. (1984).
Juvenile hormones 0, I, and I1 exist only in Lepidoptera. Zn “Eiosynthesis,
Metabolism and Mode of Action of Invertebrate Hormones” (Eds J. Hoffmann

and M. Porchet), pp. 373-383. Springer-Verlag, Berlin.
Sellier, R. (1955). Recherches sur la morphogknese et le polymorphisme alaires chez
les Orthoptkres Gryllides. Annls Sci. nat. (Zool.) Sir. I 1 16 (1954), 595-739.
Siegert, K., Morgan, P. and Mordue, W. (1985). Primary structures of locust
adipokinetic hormones 11. Biol. Chem. Hoppe-Seyler 366, 723-727.
Simmonds, M. S. J. and Blaney, W. M. (1986). Effects of rearing density on
development and feeding behaviour in larvae of Spodoptera exempta. J. Insect
Physiol. 32, 1043-1045.
Staal, G. B. (1961). “Studies on the Physiology of Phase Induction in Locusta
migratoria migratorioides R. & F.” H. Veenman & Zonen N.V., Wageningen, The
Netherlands. (Also as Meded. Landbouwhugesch. Wageningen No. 72 and Publika-
tie Fonds Landbouw Export Bureau 1916-1918 No. 40, 1-125.)
Staal, G. B. and De Wilde, J. (1962). Endocrine influences on the development of
phase characters in Locusta. Colloq. int. CNRS (“Physiologie, Comportement et
Ecologie des Acridiens en Rapport avec la Phase”), No. 114, 89-105.
Stone, J. V. and Mordue, W. (1980). Adipokinetic hormone. Zn “Neurohormonal
Techniques in Insects” (Ed. T. A. Miller), pp. 31-80. Springer, New York.
Stower, W. J. (1959). The colour patterns of hoppers of the desert locust (Schistocerca
gregaria Forskbl). Anti-Locust Bull. 32, 1-75.
Stower, W. J. (1963). Photographic techniques for the analysis of locust “hopper”
behaviour. Anim. Behav. 11, 198-205.
Stower, W. J., Davies, D. E. and Jones, I. B. (1960). Morphometric studies of the
desert locust, Schistocerca gregaria. J. Anim. Ecol. 29, 309-339.
Strich, M. C. (1955). Etude de la glande ventrale chez Locusta migratoria migrator-
ioides L. (Orth. Acridoidea). Annls Sci. nat. (Zool.) Sir. I I 16 (1954), 399-411.
Strich-Halbwachs, M. C. (1954). R81e de la glande ventrale chez Locusta migratoria
(L.). C.r. Sianc. SOC.Biol. 148, 2087-2091.
Strich-Halbwachs, M. C. (1958). Action de la glande ventrale sur le developpement
ovarien de Locusta migratoria L. (Orthoptera). J. Insect Physiol. 1, 34G351.
Strich-Halbwachs, M. C. (1959). Controle de la mue chez Locusta migratoria. Annls
Sci. nat. (Zool.) Sir. 12 1, 483-570.
Strong, L. (1965). The relationships between the brain, corpora allata, and oocyte
growth in the Central American locust, Schistocerca sp.-I. The cerebral neuro-
secretory system, the corpora allata, and oocyte growth. J. Insect Physiol. 11, 135-
146.
Strong, L. (1968). The effect of enforced locomotor activity on lipid content in
allatectomized males of Locusta migratoria migratorioides. J . exp. Biol.48, 625-
630.
Symmons, P. M. (1969). A morphometric measure of phase in the desert locust,
Schistocerca gregaria (Forsk.). Bull. ent. Res. 58, 803-809.
Tobe, S. S. and Stay, B. (1985). Structure and regulation of the corpus allatum. Adv.
Insect Physiol. 18, 305432.
Tojo, S., Morita, M. and Hiruma, K. (1985a). Effects ofjuvenile hormone on some
phase characteristics in the common cutworm, Spodoptera litura. J. Insect Physiol.
31,243-249.
Tojo, S., Morita, M., Agui, N. and Hiruma, K. (1985b). Hormonal regulation of
phase polymorphism and storage-protein fluctuation in the common cutworm,
Spodoptera litura. J. Insect Physiol. 31, 283-292.
74 M. P. PENER
Truman, J. W., Riddiford, L. M. and Safranek, L. (1973). Hormonal control of

cuticle coloration in the tobacco hornworm, Manduca sexta: basis of an ultra-
sensitive bioassay for juvenile hormone. J. Insect Physiol. 19, 195-203.
Uvarov, B. P. (1921). A revision of the genus Locusta, L. (= Pachytylus, Fieb.), with a
new theory as to periodicity and migrations of locusts. Bull. ent. Res. 12, 135-163.
Uvarov, B. P. (1966). “Grasshoppers and Locusts”, Vol. 1. Cambridge University
Press, Cambridge.
Uvarov, B. P. (1977). “Grasshoppers and Locusts”, Vol. 2. Centre for Overseas Pest
Research, London.
Verdier, M. (1958). Modifications pigmentaires lie& a la densite chez les Tettigonides.
Bull. SOC.zool. Fr. 83, 252-253.
Vincent, J. F. V. (1972). The dynamics of release and the possible identity of bursicon
in Locusta migratoria migratorioides. J. Insect Physiol. 18, 757-780.
Wajc, E. (1973). “The Effect of the Corpora Allata on Flight Activity of Locusta
migratoria migratorioides (R. & F.).” PhD Thesis, London.
Wajc, E. and Pener, M. P. (1969). The effect of the corpora allata on the mating
behavior of the male migratory locust, Locusta migratoria migratorioides [R. & F.].
Israel J. Zool. 18, 179-192.
Wajc, E. and Pener, M. P. (1971). The effect of the corpora allata on the flight activity
of the male African migratory locust, Locusta migratoria migratorioides (R. & F.).
Gen. comp. Endocr. 17, 327-333.
Walloff, Z. (1972). Orientation of flying locusts, Schistocerca gregaria (Forsk.) in
migrating swarms. Bull. ent. Res. 62, 1-72.
Warren, J. T., Sakurai, S., Rountree, D. B., Gilbert, L. I., Lee, S.-S. and Nakanishi,
K. (1988). Regulation of the ecdysteroid titer of Manduca sexta: reappraisal of the
role of the prothoracic glands. Proc. nntl. Acad. Sci. USA 85, 958-962.
Weaver, P. (1983). Pheromones and behavior. In “Invertebrate Endocrinology”,
Vol. 1, Endocrinology of Insects (Eds R. G. H. Downer and H. Laufer), pp. 543-
555. Alan R. Liss Inc., New York.
Wigglesworth, V. B. (1954). “The Physiology of Insect Metamorphosis.” Cambridge
University Press, Cambridge.
Wilson, E. 0. and Bossert, W. H. (1963). Chemical communication among animals.
Recent Progr. Horm. Res. 19, 673-716.
Wilson, I. D. and Morgan, E. D. (1978). Variations in ecdysteroid levels in 5th instar
larvae of Schistocerca gregaria in gregarious and solitary phases. J . Insect Physiol.
24, 751-756.
Wood, H. A., Hughes, P. R., Van Beek, N. and Hamblin, M. (1990). An ecologically
acceptable strategy for the use of genetically engineered baculovirus pesticides.
In “Insect Neurochemistry and Neurophysiology, 1989” (Eds A. B. Borkovec and
E. P. Masler) pp. 285-288. Humana Press, Clifton, New Jersey.
Wyatt, G. R., Cook, K. E., Firko, H. and Dhadialla, T. S. (1987). Juvenile hormone
action on locust fat body. Insect Biochem. 17, 1071-1073.
Yagi, S. (1976). The role of juvenile hormone in diapause and phase variation in some
lepidopterous insects. In “The Juvenile Hormones” (Ed. L. I. Gilbert), pp. 288-
300. Plenum Press, New York.
Yagi, S. and Kuramochi, K. (1976). The role ofjuvenile hormone in larval duration
and spermiogenesis in relation to phase variation in the tobacco cutworm,
Spodoptera litura. Appl. Ent. Zool. 11, 133-138.
Addenda
Some unforeseen delays occurred in the publication of the present review.

Meanwhile many relevant new articles have been published. This situa-
tion led to the following addenda, completed before the proofs became
available.
The development of the recent plague of the desert locust, Schistocerca
greguriu (see Section 6), was summarized by Skaf (1990). In 1989 this plague
declined, presumably partly because of the massive pesticide spraying in
Africa and adjacent semi-arid zones (Arabian Peninsula, etc.) and partly
because of the dry weather in 1989 in these areas. There is now much
argument about whether the massive employment of pesticides was a suitable
and economic strategy (cf. Gibbons, 1990). An interesting event in the recent
plague is that in autumn 1988 gregarious swarms of the desert locust escaping
from West Africa crossed the Atlantic and reached the Caribbean region,
implying an uninterrupted flight of some 5000 km (Kevan, 1989; Ritchie and
Pedgley, 1989). Although displacement of locust swarms depends mostly on
atmospheric air currents (see Rainey, 1989), crossing of the Atlantic means
that physiological factors, including the endocrine control of flight fuel
mobilization, transport and utilization by adipokinetic hormones (see Sec-
tions 3.7.2,4.3 and 6), must ensure the ability of the gregarious adults to fly,
at least in order to remain airborne, for much longer periods than was
previously suspected.
The recent locust plague probably played a major role in the resumption of
locust research, perhaps best reflected by the currently increasing number of
reviews devoted to various subjects on locusts. The article of Waloff and
Popov (1990), dealing with the vast contributions of Uvarov to acridology,
presents excellent historical perspectives and a summary of concepts in
relation to locust phases (see Section 2.1). Two recent reviews (Ferenz, 1990;
Loher, 1990) are devoted to locust pheromones. They detail this subject
much more widely than the relevant section of the present review (see Section
5) and emphasize the pheromonal aspects of locust phase changes. The major
conclusions, however, are rather similar; more basic research is urgently
needed for understanding the roles of pheromones in locust phase transfor-
mation and for evaluating the applied potential of pheromone-related
manipulations in locust control. Pheromonal-hormonal interrelations should
also be studied.
Endocrine effects on locust phase changes were summarized in a small-
scale review (Pener, 1990) with a section on applied aspects. A major review
was published by Dale and Tobe (1990) on the endocrine basis of locust
phase polymorphism. Like the present article (see Section 4. l), these authors
also conclude that knowledge regarding the importance of JH titre and
76 M. P. PENER
biosynthesis in phase differentiation in locusts is unsatisfactory. They outline

three major reasons for this situation: (1) the complexity of the relationship
between JH biosynthesis and JH titre is not fully understood even in
gregarious locusts; (2) the effects of factors other than the rate of JH
biosynthesis (e.g. haemolymph JH esterases, JH binding proteins, etc.) on JH
titre have not been investigated sufficiently in locusts and no data comparing
crowded and isolated locusts are available in this respect; (3) phase differen-
tiation involves causative factors which are independent of JH titre. Accord-
ing to Dale and Tobe (1990, p. 409), “. . . no very startling evidence has yet
been yielded by the comparative study of the action of endocrine agents in
locusts of different phases” and consequently, “this leaves an understanding
of the fundamental nature of phase polymorphism still to be sought”.
Adipokinetic hormones and their mode of action in relation to mobiliza-
tion, transport and utilization of lipids as flight fuel were again reviewed
recently (Goldsworthy and Mordue, 1989; Wheeler, 1989; Gade, 1990).
Although these reviews extend the subject to insects other than locusts and to
metabolic hormones other than AKHs (for example, hypertrehalosaemic
hormones), AKHs in locusts still constitute the basic and best investigated
case. Within the last few years considerable advancement has been made in
research on insect neurohormones (review by Holman et al., 1990; see also
several articles in the book edited by Borkovec and Masler, 1990), but no
studies have been reported on the role of neurohormones in locust phase
changes, or on phase-dependent differences in neurohormones and/or in
their mode of action. The only notable exception comes from our laboratory.
We injected graded doses of synthetic AKHI, or of CC extracts, to 10-19-
and 24-30-day-old isolated and crowded adult males of Locusta migratoria
migratorioides and assessed haemolymph lipid levels (Ayali and Pener, 1991
and submitted). We found that: (1) the resting lipid level (before injection)
was considerably higher in crowded than in isolated locusts, and (2) the
increase of haemolymph lipids 90-100 min after injection of either AKHI or
CC extracts was again markedly higher in crowded locusts. Appropriate
calculations have shown that the adipokinetic response of the isolated
locusts, as reflected by elevation of haemolymph lipid level, is only 3040%
of that of the crowded locusts. These findings correlate well with the more
active flight behaviour of the gregarious locusts in comparison to that of the
less active solitary ones (see Section 3.7.2).
The recent locust plague led to the establishment of the “Emergency
Centre for Locust Operation” within the Plant Production and Protection
Division of the Food and Agricultural Organization (FAO) of the United
Nations. This Centre now produces a register (Food and Agricultural
Organization, 1989, 1990) comprising information on currently con-
ducted locust research projects, including projects on locust physiology and

endocrinology, all around the world.
Density-dependent phase polymorphism in lepidopteran larvae (see Sec-
tion 2.2) has received some further attention. Most important is the review by
Hammond and Fescemyer (1987) which, although focused on one species,
Anticarsia gemmatalis, presents a reasonable account of phase polymor-
phism in noctuids. A further r,elevant publication is that of Fescemyer and
Hammond (1988). Recently, Morita et al. (1988) have shown that cuticular
melanization in crowded larvae of Spodoptera litura is caused by a melaniza-
tion-and-reddish-colouration hormone (MRCH) in the absence (or in the
presence of low levels) of JH. Primary structure analysis of this MRCH
isolated and purified from head extracts of adult Bombyx mori (Matsumoto
et al., 1990) revealed that it is the same molecule as the pheromone
biosynthesis activating neuropeptide (PBAN), previously purified by the
same group, from the same source, through monitoring its pheromonotropic
activity in B. mori (Kitamura et al., 1989). Interestingly, extracts of brain,
CC, CA, suboesophageal ganglion and thoracic ganglia from adult Locusta
migratoria induced pheromonotropic responses in the European corn borer
moth, Ostrinia nubialis (Sreng et al., 1990). M. Altstein, Y. Gazit, A. Ayah
and M. P. Pener (in preparation) also found by a pheromonotropic bioassay
employing the noctuid Heliothis peltigera and quantification of the phero-
mone produced (for the method see Gazit et al., 1990), as well as by an
immunochemical analysis using a PBAN antiserum and ELISA, that the
brain, CC, CA and suboesophageal ganglion of young fifth-instar male
nymphs of Locusta comprise a PBAN-like peptide. Considering the identity
of the MRCH and the PBAN (see above), it is tempting to speculate that the
PBAN-like neuropeptide found in Locusta may induce melanization in
locusts and may be identical to the NSC-CC neuroendocrine factor which
promotes the black patterns characteristic to gregarious hoppers (see Sec-
tions 3.2.1, 3.2.3 and 4.3). However, the situation may not be so simple. Like
Sreng et al. (1990), we found this PBAN-like neuropeptide also in the CA of
Locusta, but CA implantations to gregarious hoppers lead to green colour
which is accompanied by reduction or disappearance of the black patterns
(see Section 3.2.1). Although the effects of the implanted CA are undoub-
tedly caused by the JH because they are induced also by JH-analogues, it is
difficult to reconcile the reduction of the black patterns with the assumption
that the PBAN-like neuropeptide (which is present and perhaps even
originates in the CA-cf. Sreng et al., 1990) promotes melanization and
black pattern formation in locusts.
78 M. P. PENER
References t o the addenda
Ayah, A. and Pener, M. P. (1991). Differences in response to adipokinetic hormone

between the solitary and gregarious phases of Locusta migratoria. Gen comp.
Endocr. 82, 254 (Abstracts of papers presented at the Fifteenth Conference of
European Comparative Endocrinologists, abstract no. 123.
Borkovec, A. B. and Masler, E. P. (Eds) (1990). “Insect Neurochemistry and
Neurophysiology, 1989”. Humana Press, Clifton, New Jersey.
Dale, J. F. and Tobe, S. S. (1990). The endocrine basis of locust phase polymorphism.
In “Biology of Grasshoppers” (Eds R. F. Chapman and A. Joern), pp. 393414.
John Wiley & Sons, New York.
Ferenz, H. J. (1990). Locust pheromones-basic and applied aspects. Bol. Sanidad
Veg., Fuera de Serie, No. 20 (also as “Proceedings of the 5th International Meeting
of the Orthopterists’ Society, 17-20 July 1989, Valsain (Segovia), Spain”), 29-37.
Fescemyer, H. W. and Hammond, A. M. (1988). Effect of larval density and plant age
on size and biochemical composition of adult migrant moths, Anticarsia gemmata-
lis Hubner (Lepidoptera: Noctuidae). Env. Ent. 17, 213-219.
Food and Agricultural Organization (1989). “The Desert Locust Research and
Development Register, No. 1, July 1989”. Emergency Centre for Locust Opera-
tions, Food and Agricultural Organization of the United Nations, Rome, Italy.
Food and Agricultural Organization (1990). “The Desert Locust Research and
Development Register, No. 2, March 1990”. Emergency Centre for Locust
Operations, Food and Agricultural Organization of the United Nations, Rome,
Italy.
Gade, G. (1990). The adipokinetic hormone/red pigment-concentrating hormone
peptide family: structures, interrelationships and functions. J. Insect Physiol. 36,
1-12.
Gazit, Y., Dunkelblum, E., Benichis, M. and Altstein, M. (1990). Effect of synthetic
PBAN and derived peptides on sex pheromone biosynthesis in Heliothis peltigera
(Lepidoptera: Noctuidae). Insect Biochem. 20, 853-858.
Gibbons, A. (1990). Overkilling the insect enemy. Science 249, 621.
Goldsworthy, G. and Mordue, W. (1989). Adipokinetic hormones: functions and
structures. Biol. Bull. 177, 218-224.
Hamrnond, A. M. and Fescemyer, H. W. (1987). Physiological correlates in migra-
tory noctuids: the velvetbean caterpillar as a model. Insect Sci.Appl. 8, 581-589.
Holman, G.M., Nachman, R.J. and Wright, M. S. (1990). Insect neuropeptides.
Annu. Rev. Ent. 35,201-217.
Kevan, D. K. McE. (1989). Transatlantic travellers. Antenna 13, 12-15.
Kitamura, A., Nagasawa, H., Kataoka, H., Inoue, T., Matsumoto, S., Ando, T. and
Suzuki, A. (1989). Amino acid sequence of pheromone-biosynthesis-activating
neuropeptide (PBAN) of the silkworm, Bombyx mori. Biochem. biophys. Res.
Commun. 163, 520-526.
Loher, W. (1990). Pheromones and phase transformation in locusts. In “Biology of
Grasshoppers” (Eds R. F. Chapman and A. Joern), pp. 337-355. John Wiley &
Sons, New York.
Matsumoto, S., Kitamura, A., Nagasawa, H., Kataoka, H., Orikasa, C., Mitsui, T.
and Suzuki, A. (1990). Functional diversity of a neurohormone produced by
the suboesophageal ganglion: molecular identity of melanization and reddish
colouration hormone and pheromone biosynthesis activating neuropeptide.

f. Insect Physiol. 36, 427432.
Morita, M., Hatakoshi, M. and Tojo, S. (1988). Hormonal control of cuticular
melanization in the common cutworm, Spodoptera litura. f. Insect Physiol. 34,
751-758.
Pener, M. P. (1990). Endocrine effects on locust phase changes; basic and applied
aspects. Bol. Sanidad Veg., Fuera de Serie, No. 20 (also as “Proceedings of the 5th
International Meeting of the Orthopterists’ Society, 17-20 July 1989, Valsain
(Segovia), Spain”), 39-55.
Rainey, R. C. (1989). “Migration and Meteorology. Flight Behaviour and the
Atmospheric Environment of Locusts and other Migrant Pests.” Clarendon Press,
Oxford.
Ritchie, M. and Pedgley, D. (1989). Desert locusts cross the Atlantic. Antenna 13,
10-1 2.
Skaf, R. (1990). The development of a new plague of the desert locust Schistocerca
gregariu (Forskgl) (Orthoptera; Acrididae) 1985-1989. Bol. Sanidad Veg.,Fuere de
Serie, No. 20 (also as “Proceedings of the 5th International Meeting of the
Orthopterists’ Society, 17-20 July 1989, Valsain (Segovia), Spain”), 59-66.
Sreng, L., Moreau, R. and Girardie, A. (1990). Locust neuropeptides stimulating sex
pheromone production in female European corn borer moth, Ostrinia nubialis.
f. Insect Physiol. 36, 719-726.
Waloff, N. and Popov, G. B. (1990). Sir Boris Uvarov (1889-1970): The father of
acridology. Annu. Rev. Ent. 35, 1-24.
Wheeler, C. H. (1989). Mobilization and transport of fuels to the flight muscles. In
“Insect Flight” (Eds G. J. Goldsworthy and C. H. Wheeler), pp. 273-303. CRC
Press, Boca Raton, Florida.

Pener1991, Locust Phase Polymorphism and Its Endocrine

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Locust Phase Polymorphism and its Endocrine

1 Insect polymorphism and its endocrine aspects 1

1 insect polymorphism and its endocrine aspects

The term polymorphism roughly means that distinct morphological dif-

ADVANCES IN INSECT PHYSIOLOGY VOL 23 Copyrrghr 0 1991 Academic Press Limited

dimorphism, that is to morphological difference(s) other than in the genitalia

wide a range of intermediates are needed for unequivocal distinction? It does

1.2 POLYMORPHISM AND ENDOCRINE FACTORS

In environmentally controlled insect polymorphism (including physiological

The theory of locust phases was formed by Uvarov (1921) in a taxonomic

also in the next generation; a full-scale phase transformation may take

locust, Locusta migratoria (Oedipodinae), with its various subspecies, most

2.2 SOME OTHER INSECTS

Density-dependent continuous polymorphism also occurs in some other

1985a,b; Simmonds and Blaney, 1986; Fescemyer and Hammond, 1986;

3 Phase characteristics and related endocrine effects

Any characteristic which shows density-dependent changes in locusts is

3.1 MORPHOLOGY, MORPHOMETRICS AND ANATOMY

The morphological differences between gregarious and solitary locusts are

Cassier and Delorme-Joulie (1976) and Cassier (1977) reported that

3.2.1 General aspects, hoppers and associated hopper-adult features

Acridids frequently exhibit environmentally regulated or phenotypic colour

More or less respective shades of these colours

FIG. 2 Diagrammatic presentation of the three different kinds of superimposed

conditions show a wide colour variation-green, yellow-green, olive green,

densities great variations of intermediate colourations are observed (see for

responsible in Locusta also for the dark-blackish colour of the “homo-

colouration! Thus, although the relationship between JH and green colour

Girardie, 1974; Bouthier, 1976). However, this NSC-CC factor, or a factor of

3.2.3 Some conclusions

The available experimental evidence clearly demonstrates that endocrine

Phase colour polymorphism is much less frequent in acridids than “green-

3.3.1 Maturation and maturation-accelerating pheromone

The period elapsing between fledging and sexual maturation is shorter in

3.3.2 Male sexual hehaviour

A further reproduction-related phase characteristic is that crowded Locusta

3.3.3 Female reproductive parameters and maternal effects on hatchlings

The reproductive potential or fecundity of isolated females is higher than

crowded females. The effect of the density is cumulative; the number of

proportion of viable eggs in the isolated locusts. Owing to these better

nevertheless, the completion of the cycle was delayed in these females in

3.4 HOPPER DEVELOPMENT

In Schistocerca and Nomadacris, as well as in some non-locust acridids, a

activity or in JH titres. Furthermore, the case of Locusta indicates that there

3.5 PHYSIOLOGY, BIOCHEMISTRY AND MOLECULAR BIOLOGY

The rate of oxygen consumption is higher in crowded than in isolated

both isolated and crowded Locusta adults, whereas implantation of extra CA

One or two supernumerary chromosomes, termed B chromosomes, are often

between phase status, or density, and chiasma frequency in Schistocerca and

3.7 BEHAVIOUR AND ACTIVITY

The most characteristic and impressive activity of a hopper band in the

more intensely than isolated ones (Michel, 1970a,b, 1980a,b); thus, in

drastically reduced flight duration in Schistocerca males, but implantation of

chemical characteristics. The vast literature on AKH cannot be reviewed

cited the opinion of Fuzeau-Braesch and David, as a personal communica-

4 Endocrine organs, hormones and their role in phase

4.1 THE CORPORA ALLATA A N D JUVENILE HORMONE

Staal(l961) reported that the volume of the CA is larger in isolated than in

primary cause of locust phase transformation. However, Fuzeau-Braesch et

1 . E/F morphometric ratio + Effect may be related to 3.1

7. “Homochrome” + CA/JH induce green colour 3.2.1

G = gregarious or crowded locusts; S = solitary or isolated locusts.