Locusts are potentially the most destructive pest
insects in the world. They often form swarms and
migrate over long distances. Locust swarms may
consist of billions of individuals and cause serious
damage to agricultural crops (Chapman, 1976).
The outstanding characteristic of locusts is their
ability to show density-dependent phase polymor-
phism, involving graded changes in morphological,
physiological and behavioral traits. At low density,
nymphs of the migratory locust, Locusta migrato-
ria L., assume various body colors including green,
yellow, brown, reddish and black depending on the
habitat background color and humidity. Adults are
either greenish or brownish in color. Both nymphs
and adults show little tendency to aggregate and
they are sedentary. At high density, all nymphs
look similar with black and orange body col-
oration. They show a strong tendency to aggregate
and move in bands. Adults are dark brown and
often undergo long-distant migration in swarms.
Because of the distinct differences in appearance
and behavior, the individuals at low density were
once designated as L. danica and those at high den-
sity as L. migratoria until Uvarov (1921) formu-
lated the phase polymorphism theory. He described
that these two species constitute a single species
that changes from one phase to another in response
to population density and suggested this species be
called L. migratoria. This theory was extended to
include the desert locust, Schistocerca gregaria
Foskål (Uvarov, 1923, 1966). One of the most im-
portant characteristics of phase polymorphism is
the presence of intermediate forms called transient
phase in addition to the two extreme phases, soli-
tarious and gregarious phases occurring at low and
high density, respectively. A shift from solitarious
to gregarious, or vice versa, does not take place in
one generation, but takes several generations
Appl. Entomol. Zool. 41 (2): 179–193 (2006)
Corazonin and locust phase polyphenism
Laboratory of Insect Life Cycles and Physiology, NIAS at Ohwashi, Tsukuba 305–8634, Japan
(Received 11 November 2005; Accepted 26 January 2006)
Phase polyphenism is an adaptive phenomenon in which some traits vary continuously in response to population den-
sities. In locusts, two extreme phases, solitarious and gregarious, that occur at a low and a high density, respectively,
are known and intermediate forms called transient phase also occur in a transition between the two phases or at an in-
termediate density. Establishment of an albino strain of Locusta migratoria led to the discovery of a neuropeptide,
corazonin that is involved in the control of the expression of some phase-related traits in this and another locust,
Schistocerca gregaria. This paper describes a summary of phase polyphenism research with a particular emphasis on
recent studies about the roles of corazonin in locusts. In L. migratoria, injection of the neuropeptide causes albino
nymphs to express various body colors often observed in not only solitarious but also gregarious forms irrespective of
the rearing density. Both juvenile hormone and corazonin are necessary to express the green solitarious form normally
observed in the ﬁeld. It has also been suggested that this neuropeptide may be involved in the control of phase-related
morphometric ratios of F/C and E/F (Fhind femur length; Cmaximum head width; Eelytron length) as well as
the development of antennal olfactory sensilla in the two locusts: injection of the peptide mimics crowding effects,
thus inducing gregarious characteristics in solitarious (isolated-reared) locusts. Corazonin and related compounds are
widespread among insects. Transplantation of the brain and corpora cardiaca from various donors to albino locusts in-
dicates the presence of corazonin or corazonin-like substances in all 18 insect orders so far screened except for the
Key words: Corazonin; Locusta migratoria; Schistocerca gregaria; phase polyphenism; body color
* E-mail: email@example.com
(Uvarov, 1966). Locusts during the transient period
or at intermediate densities show intermediate
characteristics. Thus, the variation is continuous,
the situation being different from other types of
polymorphism or polyphenism in which morpho-
logically distinct morphs such as long-winged and
short-winged or apterous morphs occur without
forming intermediate morphs (Harrison, 1980;
Pener, 1985; Dingle, 1996).
Numerous studies have been conducted in rela-
tion to phase polymorphism (Uvarov, 1966, 1977;
Fuzeau-Braesch, 1985; Dale and Tobe, 1990;
Pener, 1991; Pener and Yerushalmi, 1998; Apple-
baum and Heifetz, 1999) and the phase polymor-
phism theory has been widely accepted. However,
the endocrine mechanism controlling phase poly-
morphism has not been well understood. Our labo-
ratory started working on this subject 15 years ago
and our ﬁndings shed some new insights into the
physiological mechanisms for the control of phase-
related body color and morphological changes in
L. migratoria and S. gregaria. Here, I will brieﬂy
review the history of research on this subject and
outline our ﬁndings including some unpublished
Because the term ‘polymorphism’ is often used
for genetically controlled variations, the term
‘polyphenism’ is more appropriate to describe en-
vironmentally induced variations (Dingle, 1996).
Therefore, phase polyphenism instead of phase
polymorphism will be used in this paper.
Phase polyphenism has been recognized in sev-
eral species of locust (Faure, 1932; Uvarov, 1966,
1977). L. migratoria and S. gregaria are the most
intensively studied species, mainly because of their
economic importance. Table 1 compares phase-re-
lated differences in the former species. Body color
is one of the most conspicuous phase-related traits
observed in both species. Solitarious nymphs show
cryptic body coloration, whereas gregarious
nymphs develop black patterns in both species, al-
though the black patterns can be induced relatively
quickly by crowding even before the locusts attain
the gregarious phase. Differences in adult body
shape, often expressed as F/C and E/F ratios
(Fhind femur length; Cmaximum head width;
Eelytron length), are another important phase-re-
lated variation. Gregarious locusts have a lower
F/C ratio and a higher E/F ratio than solitarious
ones (Dirsh, 1951, 1953). Locusts in the two
phases also show differences in shape of the prono-
tum (Dirsh, 1953) and numbers of sensilla on the
antennae (Greenwood and Chapman, 1984; Heifetz
et al., 1994; Ochieng et al., 1998).
Locusts display characteristic changes in behav-
ior in response to population density. Solitarious
locusts tend to avoid each other, whereas gregari-
ous locusts tend to aggregate. Gregarious nymphs
form bands and display a behavior called march-
ing, and adults swarm and often conduct long-dis-
tant migration. Their behavior in each phase is not
ﬁxed but ﬂexible. For example, solitarious individ-
uals can be induced to behave in a gregarious man-
ner by giving them a chance to experience crowd-
ing for 2 h (Ellis, 1962). Tactile and visual stimuli
are involved in the induction and maintenance of
gregarious behavior (Ellis, 1962). Interestingly,
stimulation of solitarious locusts with ﬁne wires or
a crowd of different species induces gregarious be-
havior. These observations have been conﬁrmed by
similar studies (Simpson et al., 2001; Lester et al.,
2005). Pheromones play a role in the control of be-
havior in locusts (Loher, 1990; Byers, 1991; Pener,
180 S. T
Table1. Phase related-differences in L. migratoria
(for references, see text)
Traits Solitarious Gregarious
Body color Green, brown Black patterns
Pronotum Convex Concave
No. of antennal sensilla Large Small
Aggregation No Yes
General activity Low High
Flight capability Low High
Copulation Short Long
Slow (5 or 6 instars) Rapid (5 instars)
Fertility (No. of eggs) Large Small
(Egg size) Small Large
F, hind femur length; C, maximum head width; E, elytron
is the proportion of offspring sired by the second male
1991; Pener and Yerushalmi, 1998) and their chem-
ical structures and signiﬁcance were intensively
studied in the last decade (Torto et al., 1994, 1996;
Ferenz and Seidelmann, 2003; Hassanali et al.,
Recently, it was demonstrated that prolonged
pre-copulatory mounting increases the length of
copulation, which in turn increases the P
, the pro-
portion of offspring sired by the second male to
mate, in L. migratoria showing multiple mating
(Zhu and Tanaka, 2002). This phenomenon was
conﬁrmed and found to be speciﬁc to gregarious
(crowd-reared) populations (Tanaka and Zhu,
2003). The P
value, length of pre-copulatory
mounting and length of copulation are all different
between phases (Table 1), suggesting a phase-spe-
ciﬁc reproductive strategy in this locust.
THE ROLE OF JUVENILE HORMONE (JH)
Half a century ago, Joly and Joly (1954) demon-
strated that implantation of extra corpora allata
(CA) induced a green body color in gregarious
(crowd-reared) nymphs of L. migratoria, indicating
that JH produced by the glands is responsible for
the induction of green color. This green-color in-
ducing effect was conﬁrmed by many workers
using a similar means (e.g. Staal, 1961) and by the
administration of synthetic JH and JH analogs (e.g.
Applebaum et al., 1997). Destruction of the CA in
solitarious green nymphs caused the green color to
fade away, but failed to develop the black and or-
ange coloration typical for gregarious forms in
those individuals, and the involvement of another
factor inducing the expression of gregarious body
coloration was pointed out by Pener et al. (1992),
although the mechanism inducing the gregarious
coloration remained unknown.
PIONEER STUDIES ON THE DARK-COLOR
Nickerson (1956) suggested a steroid factor in
the hemolymph as a dark-color inducing substance
in gregarious nymphs of S. gregaria. He observed
that injection of hemolymph from gregarious
nymphs increased the black patterns in solitarious
nymphs. Staal (1961) carried out a series of elegant
experiments to test the roles of various organs in
the control of phase-related traits and found that
nymphs of L. migratoria implanted with extra cor-
pora cardiaca (CC) increased the black patterns,
whereas surgical removal of CC produced an oppo-
site effect. Ellis and Carlisle (1961) reported that
removal of the prothoracic glands from isolated-
reared nymphs of S. gregaria led to the appearance
of black patterns and yellow background color ob-
served in gregarious forms. However, Staal (1961)
found that implantation or removal of these glands
did not produce such effects in L. migratoria. Gi-
rardie and Cazel (1965) observed that the dark
body color became lighter when the C cells of pars
intercerebralis were destroyed by microcautery in
gregarious nymphs of L. migratoria. Although
these studies indicated the presence of dark-color
inducing factors in the brain, CC, prothoracic
glands and hemolymph in locusts, their chemical
identity remained undetermined. Besides the black
patterns and green color, locusts develop other
dark colors such as yellow, brown, beige, orange,
reddish and black (Faure, 1932; Tanaka, 2005).
However, no information was available about the
hormonal factor(s) responsible for the induction of
DISCOVERY OF AN ALBINO MUTANT DE-
FICIENT IN THE DARK-COLOR INDUCING
Albinism is not a rare phenomenon in animals
(Halls, 2004). This is particularly true for locusts
in the laboratory (Hunter-Jones, 1957; Pener, 1965;
Verdier, 1965). We established an albino strain of
L. migratoria by selecting albino mutants that had
appeared spontaneously in a laboratory stock origi-
nally derived from Okinawa, Japan. The albinism
in this strain is controlled by a simple Mendelian
unit (Hasegawa and Tanaka, 1994). Locusts of this
strain are all whitish in color under crowded condi-
tions, but capable of expressing the green color
under isolated conditions, as reported for an albino
strain of a European L. migratoria (Verdier, 1965).
We discovered that this albino strain lacks a dark-
color inducing factor that is normally present in the
brain, CC and thoracic ganglia of this species: im-
plantation of the organs taken from normal (pig-
mented) nymphs into albino nymphs caused some
of the latter to turn gray, yellow, brown, or black,
looking like normal solitarious individuals, and
others to develop black and orange coloration like
Corazonin and Locusts 181
that of normal gregarious hoppers (Tanaka, 1993).
Using the same technique, a factor inducing dark
color in albino L. migratoria was also suggested to
be present in the CC of S. gregaria (Tanaka and
Yagi, 1997) and another acridid, Gastrimargus
marmoratus (Tanaka, 2000c). The partial charac-
terization revealed that the CC factors in L. migra-
toria and S. gregaria were peptidic substances be-
cause their dark-color inducing activity was re-
tained after heating, but lost after incubation with a
proteinase (Tanaka and Pener, 1994a, b; Tanaka
and Yagi, 1997).
IDENTIFICATION OF THE DARK-COLOR
We made methanol extracts of CC from normal
L. migratoria and S. gregaria to determine the pri-
mary structures of the dark-color inducing neu-
ropeptides using the albino bioassay developed
by Tanaka and Pener (1994a). Interestingly, the
methanol extracts show a dark-color inducing ac-
tivity only when mixed with oil for injection, but
fail to do so if dissolved in an aquatic solution and
injected. Thanks to recent progress in analytical
technology, the two neuropeptides extracted from
these locusts were determined to be identical to
Sca-corazonin (Tawﬁk et al., 1999) that had been
isolated previously from the American grasshop-
per, Schistocerca americana by Veenstra (1991)
without known function (Fig. 1). This grasshopper
exhibits so-called green-brown polyphenism and
variation in intensity of black patterns in response
to environmental factors, particularly temperature
(Tanaka, 2004a). Recently, it was demonstrated
that corazonin induces black patterns in this
grasshopper when injected, but does not affect the
background color (Tanaka, 2004b).
Antisera against corazonin were developed to
observe the distribution of immunoreactive cells in
the central nervous system of locusts. As expected
from the results of implantation experiments in a
previous study (Tanaka, 1993), we conﬁrmed that
strong immunoreactivity was detected in the brain,
CC and thoracic ganglia in normal individuals of
L. migratoria but not in albinos (Schoofs et al.,
2000, 2001; Baggerman et al., 2001; Roller et al.,
The dark-color inducing factors in the brain and
CC suggested by Staal (1961) and Girardie and
Cazel (1965) are likely to be corazonin, because
nymphs of L. migratoria, deﬁcient in this neu-
ropeptide (i.e. albino mutant) fail to express all the
non-green dark colors observed in normal individ-
uals. Nickerson (1956) suggested the presence of a
steroid factor with dark-color inducing activity in
the hemolymph in S. gregaria. Whether or not this
hemolymph factor is identical to the CC factor or
corazonin has not been demonstrated.
The presence of corazonin or corazonin-like
substances in other locusts and related insects was
indicated by the albino bioassay (Tanaka, 1993,
2000c): implantation of brain or CC taken from
these insects caused darkening in albino locusts.
The CC of Gryllus bimaculatus induced black pat-
terns in green solitarious nymphs of normal
S. gregaria when implanted (Tanaka and Yagi,
1997). We attempted to identify the chemical na-
ture of the factors from G. bimaculatus and Bombyx
mori and found another corazonin molecule type,
Pea-corazonin (Fig. 1; Hua et al., 2000). This mol-
ecule was ﬁrst isolated from a cockroach, Periplan-
eta americana, as the most potent cardiostimula-
tory peptide (Veenstra, 1989). It is as potent as
Sca-corazonin in terms of dark-color inducing ac-
tivity in locusts (Hua et al., 2000), but neither of
them is involved in the control of pigmentation in
non-locust insects. In B. mori, both types of cora-
zonin reduce silk spinning activity slightly when
injected (Tanaka, Y. et al., 2002). Likewise, a third
type of corazonin synthesized based on the ge-
nomic library of the European honey bee, Apis
mellifera (Fig. 1), was recently shown to exert a
dark-color inducing effect in albino L. migratoria
and a suppressing effect on spinning activity in B.
mori (Roller et al., 2006; Verleyen et al., 2006).
182 S. T
Fig. 1. Corazonin molecule types. Different amino acids are emphasized.
Thus, three types of corazonin have been identiﬁed
in insects (Tanaka, 2005).
THE ROLE OF CORAZONIN AND ITS IN-
TERACTION WITH JH IN THE CONTROL
OF BODY COLOR
In solitarious nymphs, the body color depends on
various environmental factors including humidity,
habitat background color and temperature (Pener,
1991). In response to environmental conditions, they
change their body color rather quickly, although it
may take one or two molts before changes occur.
The variety of colors they express and the way they
change their body color in response to environmen-
tal factors appeared to indicate a complicated hor-
monal mechanism involving various hormones.
The possibility that a relatively few hormones
may explain this body-color polyphenism was indi-
cated by implantation experiments in which CC
taken from a cricket, G. bimaculatus were system-
atically transplanted into albino locusts (Tanaka,
1996). As mentioned, the CC of this cricket con-
tains Pea-corazonin that can induce darkening in
locusts when injected. In response to different tim-
ings of CC implantation, the albino recipients ex-
pressed various body colors looking similar to
those observed not only in solitarious but also gre-
garious forms (Tanaka, 1996).
Using synthetic Sca-corazonin, the role of this
neuropeptide in the control of body color was ex-
amined with albino locusts (Tanaka, 2000a). Al-
bino nymphs were variously treated during the
third stadium and their body color was observed
after ecdysis to the following stadium. The results
indicated that albino nymphs injected with the pep-
tide at the beginning of the third stadium turned
black completely after the following ecdysis. How-
ever, when a low dosage was applied, they devel-
oped purple, brown and dark brown colors. Nymphs
injected at the end of the third stadium turned red-
dish without black patterns or spots in the fourth
stadium. These body colors were similar to solitari-
ous forms often encountered in the ﬁeld. Nymphs
with black and orange coloration looking like the
gregarious body coloration also appeared when in-
jected shortly after the mid stage of the third sta-
dium (Tanaka, 2000a, b). It should be noted that all
albino nymphs were kept crowded throughout the
experiments. This suggests that albino nymphs may
develop various solitarious body colors without ex-
periencing a low density or isolation if they receive
appropriate dosages of corazonin at appropriate
Implantation of extra CA, a JH analog (metho-
prene) and JH III all induced green body color in
albino nymphs (Tanaka, 1993; Hasegawa and
Tanaka, 1994; Tanaka, 2000b). However, these
nymphs failed to develop a brown or reddish color
on the ventral surface and legs that was characteris-
tically manifested in normal solitarious green
forms of this locust. Such body coloration can be
obtained in albino nymphs only when both JH and
corazonin are injected (Tanaka, 2000b). Thus,
green solitarious nymphs require both JH and cora-
zonin to express the characteristic body color. The
amount of corazonin present in the CC or brain ap-
pears similar between the two phases of a normal
strain (Tanaka and Pener, 1994a).
These results appear to suggest that corazonin
and JH can explain the body color polyphenism in
L. migratoria. If this is true, one may expect that
injection of corazonin would cause normal solitari-
ous nymphs to develop the gregarious coloration
without exposing them to crowding, and normal
gregarious nymphs to turn even darker. It was
demonstrated that such changes in body color actu-
ally could occur (Tanaka, 2000a, b).
Figure 2 illustrates a hypothesis to explain the
hormonal control of body color polyphenism in L.
migratoria. Some solitarious nymphs are black or
brown in color if they occur in habitats with a
black or brown background. Such body colors are
induced depending on the corazonin titer at the be-
ginning of the previous stadium. Black individuals
would be produced if the titer is high (Fig. 2D),
whereas brown ones would be produced if it is low
(Fig. 2E). If the peptide titer is very low until
shortly before ecdysis, the resulting nymphs would
develop reddish color after ecdysis (Fig. 2F).
Green solitarious nymphs with brownish color on
the legs and the ventral side of the body require
both JH and corazonin in the second half of the
previous stadium (Fig. 2C). With JH alone, the
body color turns green without developing the
brownish color (Fig. 2B). At high density, gregari-
ous nymphs with black patterns and an orange
background color appear. In this case, the JH titers
are low and the peptide titers remain low until
shortly after the mid stage of the previous stadium
Corazonin and Locusts 183
(Tanaka, 2000b). For a certain type of body col-
oration to be maintained in successive nymphal
stadia, the speciﬁc changes in corazonin and JH
titers required for the expression would be repeated
in each stadium.
Temperature inﬂuences the expression of body
color in locusts. In S. gregaria, intensive darkening
occurs at low temperature and light-colored indi-
viduals appear at high temperature (Husain and
Ahmad, 1936). The same phenomenon occurs in
L. migratoria in which normal nymphs reared at
42°C turn whitish, looking like albino individuals
(Tanaka, 2003). It appears that the loss of the dark
color at the high temperature is caused by reduced
concentrations of corazonin rather than by inactiva-
tion of the receptor system of this peptide, because
the sensitivity to injected corazonin remained un-
changed. Thus, whitish individuals turn darker
even at a high temperature if they are injected with
the peptide (Tanaka, 2003).
Body color polyphenism looks simpler in S. gre-
garia than L. migratoria. In the former, solitarious
nymphs have a green or beige background color,
whereas gregarious nymphs develop black patterns
with an orange or yellow background color (Faure,
1932). As in L. migratoria, JH is responsible for
the induction of the green color in this locust
(Roussel and Perron, 1974; Mordue (Luntz),
1977). Implantation of extra CC induced black pat-
terns in green solitarious nymphs (Tanaka and
Yagi, 1997). In this case, the background green
color was retained, but the compound eyes were
strongly pigmented like those of gregarious
nymphs. We examined the role of corazonin in this
locust by injecting the peptide into green nymphs.
Third stadium nymphs thus injected changed the
body color after the following ecdysis and they be-
came indistinguishable from gregarious ones of the
same (4th) stadium, in spite of the fact that they
had been kept in isolation continuously (Tawﬁk
et al., 1999), whereas green nymphs injected at the
penultimate (4th) stadium developed black patterns
after ecdysis to the last stadium but failed to de-
velop the reddish or yellow background color char-
acteristic of gregarious last stadium nymphs
(Tanaka, 2001). Therefore, in the last nymphal sta-
dium, corazonin is responsible for the induction of
black patterns only, and another factor seems to be
involved in the control of the background color in
this locust (Tanaka, 2001), the situation being simi-
lar to that for S. americana, in which injection of
corazonin induces the black patterns but not the red
wine background color (Tanaka, 2004b).
Corazonin can induce dark color in other acridid
species when injected. All ﬁve Japanese species in-
cluding Acrida cinerea, G. marmoratus, No-
madacris succincta, Oxya yezoensis, Atractomor-
pha lata (Tanaka, 2000c) and one Israeli species,
Oedipoda miniata (Yerushalmi and Pener, 2001),
have been demonstrated to turn darker after injec-
tion of this peptide. These results might indicate a
common function of this peptide in the control of
body color in this group of insects. As will be men-
tioned later, this neuropeptide or related sub-
stance(s) has been shown to occur in the brain and
CC of those Japanese species (Tanaka, 2000c).
184 S. T
Fig. 2. A hypothesis explaining the hormonal control of
body-color polyphenism in L. migratoria (Tanaka, 2000b).
Open squares indicates the presence of juvenile hormone and
closed ones that of corazonin. The titers of respective hor-
mones determine the type of body coloration expressed in the
following nymphal stadium. For a more detailed explanation,
see the text.
HORMONAL CONTROL OF OTHER PHASE-
Body dimensions. Probably the most interesting
question to be asked next is whether or not cora-
zonin is involved in the control of other phase-re-
lated characters. We tested this possibility by in-
jecting the peptide into solitarious locusts. The
shape of pronotum is more convex in solitarious
(isolated-reared) individuals than in gregarious
(crowd-reared) ones. In L. migratoria, injections of
corazonin in the second and third stadia caused iso-
lated-reared nymphs to develop a less convex
pronotum in the last (5th) nymphal stadium and
adult stage compared with that for oil-injected con-
trols (Tanakas, S. et al., 2002). In this case, it is im-
portant to separate individuals with different
nymphal instars, because individuals with an extra
(6th) stadium tend to have more solitarious charac-
teristics than those with ﬁve nymphal stadia. It was
also demonstrated that injections of corazonin into
isolated-reared nymphs caused a shift in morpho-
metric ratios of F/C and E/F at the adult stage to-
wards the values typical for gregarious forms in
L. migratoria (Fig. 3; Tanakas, S. et al., 2002) and
S. gregaria (Hoste et al., 2002b; Breuer et al.,
2003). In the latter, a signiﬁcant effect of the pep-
tide was obtained only in males. However, this con-
clusion was based on a mixture of individuals with
different nymphal stadia. Thus, we re-examined the
effect of corazonin in this locust. The results con-
ﬁrmed that the number of nymphal stadia had a
signiﬁcant effect on the adult morphometric ratios
and we thus analyzed data by separating individu-
als with different nymphal stadia (Maeno et al.,
2004). As a result, injections of corazonin into iso-
lated-reared nymphs were found to cause a signiﬁ-
cant shift in F/C and E/F ratios towards the values
typical for gregarious adults in both sexes. Further-
more, it was revealed that the earlier the injection
during the nymphal stage the larger the ‘gregariz-
ing’ effects of the peptide on these morphometric
ratios in this species as well as L. migratoria
(Maeno et al., 2004).
Corazonin inﬂuences the morphometric charac-
teristics of L. migratoria. However, the Okinawa
albino strain, deﬁcient in this peptide, displays
phase-related morphometric changes to some ex-
tent (Yerushalmi et al., 2001; Hoste et al., 2002a;
Tanaka, S. et al., 2002). This fact suggests that the
presence or absence of this peptide alone may not
explain the whole phenomenon. However, we can-
not exclude the possibility that this albino strain
has a mutated peptide that does not induce dark
color but retains other functions of the intact cora-
zonin. It has been demonstrated that the whole
amino acid sequence of corazonin rather than a
well-deﬁned active core sequence is necessary for
the dark-color inducing activity in albino L. migra-
toria (Yerushalmi et al., 2002; Tanaka et al., 2003).
On the other hand, Nolte (1967, 1968) reported
that albino locusts do not show gregarious charac-
teristics and constitute an extreme solitarious
phase. It is possible that the albinism is caused by
different mechanisms in different albino strains.
The role of JH in the control of phase-related
morphometrics has often been argued. Staal (1961)
obtained various intermediate morphometric values
in adult locusts by implanting extra CA during the
nymphal stage. He stated that it is desirable to dis-
tinguish, in the resulting adults, between the mor-
phometric changes produced during nymphal de-
velopment and those resulting from partial inhibi-
tion of metamorphosis. By reviewing relevant stud-
ies, Pener (1991) concluded that although the green-
color inducing effect of JH is not doubted, JH is
not a primary factor in the control of phase
polyphenism in locusts. Applebaum et al. (1997)
applied a JH analog on crowd-reared nymphs of
L. migratoria and S. gregaria and found that the
treatment did not induce solitarious morphometric
Corazonin and Locusts 185
Fig. 3. Effect of corazonin injections on adult F/C ratio in
L. migratoria. Solitarious (isolated-reared) adults (S) injected
with corazonin during the nymphal stage had signiﬁcantly re-
duced F/C ratios compared with oil-injected controls but their
values were similar to those for gregarious (crowd-reared)
controls. An asterisk indicates a signiﬁcant difference from
each of the other groups (Mann-Whitney U-test; p0.05)
(based on data from Tanaka, S. et al., 2002).
ratios in those individuals after adult emergence. In
some populations of L. migratoria, green body col-
oration is observed not only in solitarious individu-
als but also in gregarious ones. The proportion of
greenish adults sampled from a swarm population
in Jiminay, Uygur region of China in 2004 was
26.6% (Tanaka and Zhu, 2005). If high JH concen-
trations are responsible for the induction of both
green coloration and solitarious body shape, one
may expect greenish adults to have more solitari-
ous morphometric values than brown adults in such
populations. However, no signiﬁcant difference
was observed in morphometric ratios between
greenish and brownish adults in a sample taken
from the migrant population (Tanaka and Zhu,
2005). In fact, some individuals with a concave
pronotum shape and morphometric ratios typical
for gregarious forms were greenish in color. These
results, based on ﬁeld-collected individuals, appear
to support the notion that JH-inducing green body
color is not involved in the control of phase-related
Antennal sensilla. The locust antennae de-
velop various sensilla. Because pheromones are
important factors controlling locust behaviors, the
antennal olfactory sensilla are likely to serve a piv-
otal role in the control of phase polyphenism. Fur-
thermore, Ellis (1962) reported that grouping be-
havior was considerably reduced if the locusts that
had been reared in a crowded environment had the
antennae amputated shortly before the observa-
tions. In both L. migratoria and S. gregaria, the
numbers of antennal sensilla are larger in solitari-
ous locusts than in gregarious ones (Greenwood
and Chapman, 1984; Heifetz et al., 1994; Ochieng
et al., 1998), although the signiﬁcance of such dif-
ferences is not well understood. We explored the
possible involvement of corazonin in the control of
development of antennal sensilla by injecting the
peptide into isolated-reared nymphs of L. migrato-
ria at the second and third stadia (Yamamoto-Kihara
et al., 2004). Among the four types of olfactory an-
tennal sensilla, coeloconic, trichoid, basiconic type
A and basiconic type B, the abundance of coelo-
conic sensilla in the peptide-injected locusts was
signiﬁcantly reduced when compared with the oil-
injected counterparts kept in isolation, but similar
to that for untreated crowd-reared adults. This re-
sult indicated that the injection of corazonin mim-
icked a crowding effect. We also tested this ‘gre-
garizing’ effect of corazonin on S. gregaria by a
similar method (Maeno and Tanaka, 2004). The
total number of sensilla was signiﬁcantly reduced
in isolated-reared individuals after injection of the
peptide compared with oil-injected controls, and
the values became similar to those for crowd-
reared individuals (Fig. 4). In this locust, corazonin
inﬂuenced the abundance of all types of olfactory
sensilla except for the basiconic type B. It was also
found that the effect of corazonin varied with the
time of the injection in both S. gregaria and L. mi-
gratoria; the earlier the injection, the larger the ef-
fects on the abundance of total antennal sensilla
(Fig. 4), although the way in which the injection af-
fected the abundance varied with the sensillum
type (Maeno and Tanaka, 2004).
Hatchling characters. Phase-related differ-
ences in body color and behavior have been
noticed in the hatchlings of L. migratoria and S.
gregaria. Dark hatchlings tend to march more than
pale hatchlings and this behavior characteristic of
gregarious forms lasts at least until the second sta-
dium (Ellis, 1953, 1959). The hatchling body color
is inﬂuenced by the degree of crowding of the par-
ents as adults. Hunter-Jones (1958) systematically
examined this phenomenon and provided conclu-
sive evidence that crowded parents produce dark
hatchlings that are relatively heavy, and isolated
186 S. T
Fig. 4. Effect of corazonin injections on the abundance of
olfactory sensilla on the eighth antennal segment of adult fe-
males in S. gregaria. Corazonin was injected into solitarious
(isolated-reared) nymphs at the second, third and fourth
nymphal stadia. Controls were injected with oil alone at the
third stadium and continuously kept in isolation (S) or un-in-
jected and kept crowded as nymphs (G). Open circles indicate
individual datum points and closed circles the mean. Different
letters in the ﬁgure indicate signiﬁcant differences at p0.05
by ANCOVA followed by Fisher’s PLSD test (Maeno and
parents produce pale, lighter ones in both L. migra-
toria and S. gregaria. Therefore, the parental den-
sity during the adult stage is important in determin-
ing the body color and phase-related behavior in
the hatchlings of their progeny. These conclusions
were recently conﬁrmed for S. gregaria by Islam
et al. (1994a, b).
Cassier (1964, 1965) has shown that the implan-
tation of extra CA into gregarious adults of L. mi-
gratoria produces lighter colored hatchlings, indi-
cating that JH may have some role. Islam (1995)
demonstrated that JH analogs caused gregarious
(crowd-reared) adults of S. gregaria to produce
smaller but more eggs, just like those produced
by untreated solitarious (isolated-reared) adults,
although none of the eggs treated with the analogs
A small hydrophilic factor present in the foam
plugs of egg pods originating from the accessory
glands of crowded female adults was claimed to be
responsible for the darkening and gregarious be-
havior of hatchlings in S. gregaria (McCaffery et
al., 1998; Hagele et al., 2000), but the results were
not necessarily consistent (p. 359, McCaffery et al.,
1998). Furthermore, the dark-color inducing effect
of the accessory gland factor was not reproduced
by subsequent studies from the same laboratory
(Hägele et al., 2000). According to our preliminary
observations, eggs collected and isolated before the
deposition of a foam plug by the crowded female
produced black hatchlings, indicating that the foam
plug is not essential for the induction of darkening
(Tanaka and Maeno, unpublished data). It is possi-
ble that the mechanisms controlling body color and
behavior in hatchlings are different, as suggested
for L. migratoria by Ellis (1959). More recently,
Malual et al. (2001) examined this phenomenon in
relation to the behavior of hatchlings in S. gregaria
and provided experimental evidence to suggest C-8
unsaturated ketones as a gregarizing factor. In this
case, hatchlings that were exposed to these com-
pounds did not change their body coloration (Has-
sanali, A., personal communication). C-8 unsatu-
rated ketones have low solubility in water, and
whether this is sufﬁcient to account for the effects
observed by the former group in water extracts re-
mains to be established. The chemical structure of
the water-soluble factor from the accessory gland
should be determined to settle the problems.
The role of corazonin in the control of hatchling
coloration has not been tested directly. Preliminary
experiments indicated that repeated injections of
this peptide into solitarious female adults of S. gre-
garia did not cause their hatchlings to turn darker
(Tanaka, 2001). Effects of corazonin injection into
eggs or embryos on the hatchling body color have
not been tested.
Behavior. Solitarious and gregarious locusts
display conspicuous behavioral differences in late
stadium nymphs and adults, as mentioned above.
Whereas much has been learnt about the regulatory
roles of pheromones, particularly aggregation
pheromones, in the control of locust behavior
(Hassanali et al., 2005), relatively little is under-
stood about the hormonal mechanism. Many stud-
ies have reported phase-related differences in JH
and ecdysteroid titers and their functional roles in
the control of behaviors such as aggregation behav-
ior and marching activity, but no major role had
been demonstrated for either hormone (Dale and
Tobe, 1990; Pener, 1991; Applebaum et al., 1997;
Pener and Yerushalmi, 1998). However, a recent
study by Ignell et al. (2001) revealed that JH does
not change the sensitivity of antennal receptor neu-
rons to the aggregation pheromone, but inﬂuences
that of olfactory interneurons in the antennal lobe
of S. gregaria.
A possible function of corazonin in behavior has
been tested by Hoste et al. (2003) with L. migrato-
ria, but treatment of solitarious nymphs with the
peptide did not change their behavior towards gre-
gariousness. However, it is premature to conclude
that corazonin is not involved in the control of
phase-related behavioral change in locusts because
of some unsolved problems. First of all, only one
experiment with one dosage has been tested. Sec-
ond, none of the hormone-injected nymphs tested
by Hoste et al. (2003) assumed the gregarious body
coloration (i.e. orange and black coloration). In-
stead, they all turned black after the injections.
Such body coloration is often observed among
solitarious nymphs (see Fig. 2D). Thus, there is no
surprise that Hoste et al. failed to observe a shift in
behavior towards gregariousness in the above ex-
periment. However, it is known that behavioral
changes can be induced by a short period of isola-
tion or gregarization (e.g. 30 min, Ellis, 1963) that
is not sufﬁcient to cause any substantial change in
body color. Therefore, phase-related behavioral
changes are likely to be controlled by some other
Corazonin and Locusts 187
factor(s) that responds quickly to changes in
Recently, such candidates were suggested by
Rogers et al. (2004), who measured the amounts of
amino acids and biogenic amines in the central
nervous system in S. gregaria under various condi-
tions. A change in rearing density caused rapid
changes in some chemicals, but such changes were
not sustained under continuously crowded or iso-
lated conditions, indicating that these chemicals
cannot be the primary factors sustaining the gre-
garious behavior. The same researchers also exam-
ined long-term changes in those chemicals, but
their data are difﬁcult to interpret, because most
samples were based on a mixture of individuals at
different ages (2 to 5 d). Such compounds and hor-
mones often undergo substantial ﬂuctuations over a
few days or even hours. For example, several-fold
differences are observed in concentrations of some
biogenic amines in the brain and CC between 0-
and 1-day old, ﬁfth stadium nymphs of L. migrato-
ria (Tanaka and Takeda, 1996). Circadian varia-
tions of serotonin contents in the brain and he-
molymph of a cricket, Acheta domesticus have
been observed (Muszynska-Pytel and Cym-
borowski, 1978). In another cricket, Gryllus ﬁrmus,
the hemolymph JH titer exhibits a large diurnal
cycle (Zhao and Zera, 2004). Thus, to obtain mean-
ingful data, samples need to be collected and ana-
lyzed by considering those phenomena. Further-
more, it is to be kept in mind that a mere correla-
tion between phase and certain chemicals does not
prove any causal relationship, and experimental ap-
proaches are necessary to uncover the underlying
CORAZONIN IN OTHER INSECTS
The albino bioassay has revealed that corazonin
molecules or similar compounds are widespread
among insects. Table 2 shows a list of groups of in-
sects and related animals so far tested: albino lo-
custs implanted with brains and/or CC taken from
other animals developed dark color or remained
whitish. Insects belonging to a total of 18 insect or-
ders have been shown to have a dark-color induc-
ing activity when their brain or/and CC were im-
planted into albino locusts. These orders contain
both pterygote and apterigote species, indicating
that corazonin or corazonin-like compound is old
in origin. Heelwakers, belonging to a recently dis-
covered new insect order, Mantophasmatodea, also
gave a positive response (Fig. 5), although the
chemical identiﬁcation of the compound has not
yet been performed. On the other hand, no dark-
color inducing activity was shown by two non-in-
sect classes. In the isopod, no immunoreactivity
188 S. T
Table2.A list of insects and related arthropods tested by the
albino bioassay for dark-color inducing activity
Arachnida Araneida 0/2 *
Crustacea Isopoda 0/1 *
Insecta Thysanura 1/1 Roller et al. (2003)
Odonata 3/3 Tanaka (2000c)
Orthoptera 18/18 Tanaka (1993, 2004b), *
Phasmatidae 1/1 *
Mantophas- 1/1 *
Dictyoptera 3/3 Tanaka (2000c)
Dermaptera 1/1 Tanaka (2000c)
Isoptera 2/2 Tanaka (2000c), *
Plecoptera 2/2 *
Homoptera 3/3 Tanaka (2000c), *
Hemiptera 6/6 Tanaka (2000c)
Neuroptera 1/1 *
Coleoptera 0/13 Tanaka (2000c),
Roller et al. (2003), *
Mecoptera 1/1 *
Trichoptera 6/6 *
Lepidoptera 11/11 Tanaka (1993, 2000c), *
Diptera 7/7 Tanaka (2000c), *
Hymenoptera 7/7 Tanaka (2000c),
Roller et al. (2006)
*Tanaka (unpublished). The species tested include Araneus
sp., Nephila sp. (Araneida), Armadillidium vulgare
(Isopoda), Isonychia japonica, Epeorus latiforlium
(Ephemeroptera), an unidentiﬁed species (Isoptera),
Hemilobophasma montaguensis (Mantophasmatodea),
Paratenodera angustipennis (Phasmatidae), Oyamia
gibba, an unidentiﬁed sp. (Plecoptera), Atuphora stictica
(Homoptera), Leptocorixa cirbetti, Physopelta cincticollis
(Hemiptera), Panorpa japonica (Mecoptera), Mimela
splendens, Anomala sp., Dasylepidae ishigakiensis,
Hydaticus vittatus, Tenebrio obscurus (Coleoptera), Hy-
dropsyche orientalis, Oecetis nigropunctata, Cheumatopsy-
infascia, Lepidostoma orientale, Glossosoma sp., Gu-
mago sp. (Tricoptera), Ampelophaga rubiginosa (Lepi-
doptera) and Tipula aino (Diptera) collected as adults at
No. of species with a positive response/No. of species
was found when tested with an antibody against
Sca-corazonin (Tanaka and Kotaki, unpublished
data). Among all insect orders so far examined, we
have not been successful in obtaining a positive re-
sponse from the Coleoptera. The same conclusion
was reached by experiments with additional ﬁve
species including a ﬂour beetle, water beetles, and
scarab beetles (Table 2; Tanaka, unpublished). For
coleopteran species, 2–5 brains and CC pairs were
removed from each species and implanted into an
albino locust, but no positive response was ob-
tained. We conﬁrmed the absence of corazonin in
the central nervous system of a scarab beetle,
Anomala cuprea by immunohistochemistry (Roller
et al., 2003).
From these preliminary observations, it appears
that corazonin and similar compounds are common
among insects except for the Coleoptera. The pres-
ence of a particular molecule type of corazonin has
been determined only for a limited number of
species, but according to available evidence, Sca-
corazonin is found only in the Orthoptera (Veen-
stra, 1991; Tawﬁk et al., 1999), Phasmatodea (Pre-
del et al., 1999) and Hymenoptera (Roller et al.,
2006; Verleyen et al., 2006), whereas Pea-cora-
zonin is widely distributed among insect orders in-
cluding the Orthoptera (Hua et al., 2000), Dicty-
optera (Veenstra, 1989; Petri et al., 1995), Diptera
(Cantera et al., 1994; Veenstra, 1994) and Lepi-
doptera (Veenstra, 1991; Hua et al., 2000; Hansen
et al., 2001; Qi-Miao et al., 2003). Recently, it was
detected in the pericardial organs of a crab, Cancer
borealis (Lie et al., 2003). The corazonin-like sub-
stance from a honey bee (Tanaka, 2000c) is likely
to constitute another molecule type (Fig. 1), be-
cause the genome of this bee does not contain the
DNA sequence encoding the above two molecules
(Y. Tanaka, personal communications). Isolation of
corazonin-like substances in this and other species
as well as identiﬁcation of the functional role in
those insects will provide important information
about the evolution of neuropeptides (Tanaka,
Not all albino mutants in locusts are deﬁcient in
the same factor. For example, the CC of an albino
strain of S. gregaria contains corazonin. Implanta-
tion of extra CC taken from normal individuals is
not effective in inducing darkening in this strain,
but the CC of the latter can induce darkening in the
Okinawa albino strain of L. migratoria when im-
planted (Schoofs et al., 2000; Yerushalmi et al.,
2000). Thus, the albinism in S. gregaria is not
caused by the absence of corazonin. The establish-
ment of the Okinawa albino strain led us to identify
the dark-color inducing factor in normal strains of
the two locusts. We suggested earlier for this neu-
ropeptide to be called the dark-color inducing neu-
ropeptide (DCIN) (Tanaka and Pener, 1994a), but
now we know that it has other physiological func-
tions in locusts and other insects. Therefore, it is
no longer appropriate to keep the name for this
neuropeptide. In this review, ‘Sca-corazonin’ was
used simply because it was ﬁrst discovered from
Corazonin and Locusts 189
Fig. 5. Dark-color inducing activity of various organs from a heelwalker, Hemilobophasma montaguensis when implanted into
albino nymphs of Locusta migratoria.
S. americana (Veenstra, 1991). The recent ﬁndings
described above strongly indicate that Sca-cora-
zonin is involved in the control of the development
of some phase-related characters in locusts. Adult
locusts turn yellowish when they sexually mature
under crowded conditions (Pener, 1991). With the
albino strain, the possible presence of a yellow-
color inducing factor has also been suggested to be
present in the CC of adult L. migratoria (Hasegawa
and Tanaka, 1994), although the nature of this fac-
tor is yet to be determined.
The corazonin model proposed for the body
color polyphenism in the two locusts should be
tested in the future. The hormonal titers are deter-
mined by the balance of release and degradation of
the hormone. Determination of the corazonin titers
in locusts has not been carried out in relation to the
body color. The physiological activity depends not
only on the hormonal titers, but also on the pres-
ence and absence of the receptors in the tissue.
Therefore, it is important to obtain information
about the receptor system. Recent development in
molecular biology provides a unique opportunity to
test the above hypothesis and the possible roles of
corazonin in the development of other phase-re-
lated characters. In this sense, the isolation of the
corazonin-gene in Drosophila melanogaster (Veen-
stra, 1994) and in Galleria mellonela (Hansen et
al., 2001) is encouraging. Recent molecular studies
indicate phase-related differences in expression of
numerous genes in L. migratoria (Kang et al.,
2005), although how these genes are involved in
the control of phase polyphenism is not known.
I am deeply indebted to Dr. Y. Tamaki (former Department
Head of the National Institute of Sericultural and Entomologi-
cal Science) and Dr. S. Masaki (Professor Emeritus of Hi-
rosaki University) for having inspired me to start locust re-
search. Ms. S. Ogawa, Ms. H. Ikeda, Mr. K. Maeno and Mr.
M. Kaneko assisted with rearing insects. Dr. M. Shiga (former
Department Head of NISES), Dr. K. Kawasaki, Dr. T. Kotaki,
Mr. M. Watanabe, Dr. D. H. Zhu and Dr. T. Okuda gave me
much encouragement and valuable suggestions. Dr. K. Tojo
(Sinshu University) and Dr. T. Tsutsumi (Fukushima Univer-
sity) sent me heelwalkers and mayﬂies, Mr. Y. Tomioka (Ikari
Co.) sent me ﬂour beetles, Mr. M. Suenaga (NIAS) organized
light-trap trips to collect many insects for corazonin assays,
and Mr. N. Kawase identiﬁed caddish ﬂies. To all, I am most
grateful. Special thanks are due to Ms. N. Kemmochi for her
long-term assistance and dedication to this project. The grass
used was raised by the Field Management Section of NIAS at
Ohwashi. Figures 2 and 4 are reproduced with permission
from Elsevier Sciences Press. This study was partially sup-
ported by a grant (17580048) from Kakenhi (Japan). The two
anonymous referees and an editor improved the manuscript.
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