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AMER. ZOOL., 31:217-230 (1991)
Endocrine Effects on Migration 1
M. A. RANKIN
Department of Zoology, University of Texas, Austin, Texas 78712
SYNOPSIS. Migratory behavior and flight metabolism are influenced by many neuroendocrine factors. In fish engaged in migration from fresh water to the sea, prolactin and/
or thyroid hormones often play key roles in migration and salinity preference. Prolactin
induces migration to the water and the changes of second metamorphosis in a number
of amphibians, and thyroid hormone may stimulate movement away from water. In birds
there is evidence that prolactin, cortical steroids, thyroid hormones, gonadotropins and
gonadal steroids can all influence migration; considerable interspecies variation exists.
Juvenile hormone stimulates oogenesis and migratory behavior in several insects, but
has no effect or causes flight muscle degeneration in others. It may serve to coordinate
oogenesis, adult diapause and migration, particularly in colonizing species. Other neuroendocrine products have been implicated in control of migratory behavior or flight
metabolism of insects including ecdysone, adipokinetic hormones and octopamine.
In the amphibians this is because most
are associated with leaving the
migrations
This paper is intended to provide a brief
water
after
metamorphosis or returning to
overview of endocrine effects on migratory
breed.
Since
prolactin and thyroxin are
behavior in animals generally. Due to space
critical
to
the
control of metamorphosis
limitations the review must be limited to
to
the
physiological
changes that
and
the effects of those hormones with the
a
return
to
water,
it is perhaps
accompany
clearest effects on migration. It is imporare
not
surprising
that
these
hormones
tant to note that a great deal of variation
involved
in
controlling
migration,
thyexists between species in the actual effects
of specific hormones on behavior and phys- roxin promoting movement away from
iology, especially between migrants and water, prolactin the reverse. Indeed the
non-migrants, and I have largely ignored osmoregulatory effects of these hormones
these differences for the sake of brevity. were probably important in the evolution
Furthermore the number of species for of their effects on migration.
Thyroxin (T4) treatment increases prefwhich information is available is very limerence
for terrestrial substrate in aquatic
ited. Some taxa in which migration is a
well-known phenomenon have hardly been phase Notophthalmus viridescens larvae and
investigated in terms of hormonal controls, adults (with or without previous treatment
the mammals being the most obvious with prolactin) (Grant and Cooper, 1965).
example. Even where more work has been Tassava and Kuenzli (1979) obtained simdone, species investigated in detail are few. ilar results using N. viridescens aquatic phase
Because of these limitations, broad gen- adults (i.e., following "second metamoreralizations are dangerous, and many phosis" of terrestrial efts to aquatic adults)
groups must be omitted except to urge that except that both T4- and saline-injected
more work be done to fill the gaps in our controls returned to land while animals
treated with prolactin or prolactin and T 4
knowledge.
did not, suggesting that it may be the
absence of prolactin, rather than presence
PROLACTIN AND THYROID HORMONE
of
T 4 that produces "land drive." Similarly
EFFECTS ON MOVEMENT OF
Ambystoma tigrinum aquatic phase adults that
LOWER VERTEBRATES
had never been in contact with land preInvestigations of endocrine control of ferred terrestrial habitat when treated with
migration in fish and amphibians have T (Duvall and Norris, 1980). Moreover,
4
largely focused on prolactin and thyroxin. "landed"
and "migrating" individuals had
higher plasma T 4 levels (measured by RIA)
1
From the symposium on Recent Developments in the than those that remained in the water
Study of Animal Migration presented at the annual
(Duvall and Norris, 1980).
meeting of the American Society of Zoologists, 2730 December 1988, at San Francisco, California.
More than 40 years ago Chadwick (1941)
INTRODUCTION
217
218
M. A. RANKIN
showed that pituitary implants into the land Brown, 1973). Thus Moriya and Dent
form of Notophthalmus viridescens could (1986) suggest that prolactin effects on Na+
stimulate "water drive" or preference for balance increase water uptake and specific
submergence in water. A number of work- gravity. Thyroxin is thought to have oppoers including Grant and Grant (1958), site effects causing the animals to float, and
Grant and Cooper (1965) and Crim (1975) facilitating movement onto land. As noted
have shown that migration to water and above, prolactin can also increase locoassociated skin and tail changes can be ini- motor behavior. Whether this is via an
tiated in the intact or hypophysectomized effect on circulating electrolytes, peripheft by injection of prolactin, the pituitary eral skin receptors (Duvall and Norris,
hormone that antagonizes the metamor- 1980), or otherwise has not been addressed
phosis-promoting action of the thyroid experimentally.
gland. Similar results have been obtained
In contrast to urodeles, there is less eviin studies on Triturus alpestris (Tuchmann- dence to suggest endocrine involvement in
Duplessis, 1949), T. cristatus (Vellano et al., anuran migration. In toads (Rosenkilde and
1967), Ambystoma tigrinum (Carl, 1975), and Jorgensen, 1977) and frogs (Kuhn et al.,
Hynobius retardus (Moriya, 1982). In A. 1985) T 4 levels are elevated before the
tigrinum, Duvall and Norris (1977) found breeding season. In Bufo, Rosenkilde (1982)
that prolactin did not actually change sub- observed an increase in T 4 at the end of
strate preference since all untreated ani- hibernation. Tasaki et al. (1986) in Bufo
mals preferred an aquatic medium. How- japonicus formosus found that thyroid horever, prolactin did increase locomotor activity mones showed two peaks during the year,
of the terrestrial newts. Actually both hor- one before and one after the breeding seamones may be necessary for return to water son, possibly implicating T 4 in movement
since in hypophysectomized, thyroidec- both toward and away from breeding ponds
tomized N. viridescens a low dose of T 4 must in this anuran, but experimental rather
be supplied along with prolactin for sur- than correlative evidence is lacking. No
vival and to induce water drive and second effect of prolactin on water drive has been
metamorphosis in terrestrial phase efts described for anurans (Dent, 1985); no
(Gona^a/., 1973).
increase in prolactin levels is observed in
In prolactin-treated Hynobius retardus a Bufo japonicus associated with movement to
mucopolysaccharide fills the expanded water (Yoneyama et al., 1984).
Most studies of hormonal control offish
space between skin and muscle, possibly
absorbing water and causing serum osmo- migration involve movement between areas
larity and thirst to increase, and stimulat- of differing salinity. Less work has been
ing migration to water. Water uptake may done on hormonal regulation of other types
then increase specific gravity, causing the of fish migration, but given the effects of
newts to sink (Moriya, 1982). Moriya and these hormones on migration and other
Dent (1986) suggest a similar mechanism aspects of the annual cycles of amphibians
may be operating in Notophthalmus virides- and birds (see below), their involvement
cens because T4-treated animals float in may also be quite widespread among fishes.
aquaria (and prefer terrestrial substrate),
Smoltification is an event in salmon
controls and those injected with prolactin development, somewhat equivalent to
sink (and remain submerged). The specific amphibian metamorphosis, during which
gravity of T 4 -treated newts is less than 1; the darkly pigmented bottom-dwelling parr
controls and prolactin-treated animals have is transformed into a pelagic silver smolt.
specific gravities of 1 or more. Osmotic A number of investigators have implicated
pressure of the blood decreases after T4 T 4 in its induction (see reviews by Wedetreatment and increases after prolactin. meyer et al., 1980 and Folmar and DickHypophysectomy decreases the osmolarity hoff, 1980). Transformation to the smolt
of the serum, prolactin restores it. In this just precedes migration to the sea and is
species T 4 causes a drop in plasma Na+ and associated with a change in salinity prefprolactin prevents the T 4 effect (Brown and erence. Baggerman (1963) showed that a
ENDOCRINE EFFECTS ON MIGRATION
thyroid-mediated change from fresh to salt
water preference is induced in coho salmon
(Oncorhynchus keta) by lengthening photoperiods. It is preceded by a rise in thyroid
activity, can be induced precociously by
treatment with TSH, or reversed by exposure to thiourea, a thyroid inhibitor. Similar results have been obtained in other
species by Eales (1965), Wagner (1974) and
others. Dickhoff et al. (1982) demonstrated, in coho and chinook salmon (0.
tschawystcha) and steelhead trout (Salmo
gairdneri), a large, 1-2 month "surge" of
thyroid hormones during the period of
smoltification which may be cued by photoperiod, temperature and phase of the
moon (Grau et al., 1982 and references cited
therein).
A number of salmon species (Hoar et al.,
1952, 1955; Smith, 1982) as well as the
goldfish Carassius auratus (Hoar et al.,
1955), the cod Gadus morhua (Woodhead,
1970), and the guppy Poecilia reticulata
(Sage, 1968) increase swimming activity
after T 4 treatment. However, these locomotor effects were not related experimentally to actual migratory behavior. Birks et
al. (1985) tested the hypothesis that T 4
induces migration. Using a holding tank
that was connected through several bafflefitted channels to downstream tanks, they
assayed migration of juvenile steelhead
trout as movement to the downstream
tanks. T 4 inhibited rather than induced
migration; thiourea enhanced it. Furthermore, Ewing et al. (1984) showed that winter steelhead trout undergoing voluntary
migration from a hatchery had lower levels
of plasma T 4 than did non-migratory individuals from the same population. Thus,
Birks et al. (1985) propose that T 4 is necessary for "metamorphosis" to the smolt
or migrant form, but is actually antagonistic to seaward movement. They suggest that
high T 4 increases locomotor activity for
maintaining position in the stream during
smoltification, but since seaward movement is partly passive, involving decreased
locomotor behavior and a downstream orientation, the T 4 "surge" must precede and
probably inhibits the actual migration. In
support of this idea Folmar and Dickhoff
(1980) have also shown that groups of coho
219
salmon entering sea water near the end of
the T 4 surge had better survival rates than
those transferred to sea water during the
surge. Thus migration probably follows the
surge in this species as well.
In contrast, Godin et al. (1974) observed
a decrease in swimming activity, upstream
orientation, and aggressive behavior of
yearling Atlantic salmon {Salmo salar)
treated with T 4 or triiodothyronine (T3).
Atlantic salmon parr in a non-migratory
stage, orient against the current. Migrating smolts swim with the water current.
Reduction in upstream orientation,
aggressive behavior and active swimming
behavior in response to thyroid hormones
presumably allows the fish to school and
move more or less passively downstream as
they normally would during migration
(Godin et al, 1974). Furthermore, T 4
appears to mobilize lipids in salmonids
(Narayansingh and Eales, 1975) as it does
in mammals (Fain, 1980), an effect which
could be important metabolically during a
long migration. In Oncorhynchus kisutch and
0. nerka Baggerman (19606) found that T 4
levels remained high for several months
until shortly before the end of the migration season. In addition, thyroid activity in
migrating chums (0. keta), which do not
undergo smoltification, was found to be as
high as that in migrating coho and sockey
smolts that do (Baggerman, 1960&). Thus,
there may be some variability in the role
thyroid hormones play in fish migration.
Barrett and McKeown (1988) have suggested the involvement of another hormone in salmonid migration. These authors
find an elevated level of plasma growth
hormone in steelhead trout and coho
salmon subjected to sustained exercise.
When fish are starved and forced to exercise (as they would be during migration),
GH levels are further elevated, suggesting
that GH may be necessary for proper lipid
mobilization during migration.
Prolactin is essential for the survival in
fresh water of a number of euryhaline teleosts after hypophysectomy (Pickford et al.,
1965; Schreibman and Kallman, 1966;
Bern, 1967) or during periods of low
endogenous prolactin secretion (Leatherland and Lam, 1969). Tilapia (Sarotherodon
220
M. A. RANKIN
mossambicus) adapted to freshwater had 712 times higher pituitary and plasma prolactin levels compared to sea water-adapted
animals (Nicoll etal., 1981). This hormone
has also been implicated in the control of
salinity preference and migratory behavior
in the migratory gulf killifish, Fundulus
grandis (Fivizzani and Meier, 1978). When
prolactin and cortisol were injected simultaneously, F. grandis preferred water of
higher salinity than when the two hormones were injected at 12 hr intervals.
Simultaneous injection or injection of these
hormones at 18 or 24 hr intervals also stimulated fattening and an increase in gonadal
weight while injection at 12 hr intervals
had little effect or decreased these parameters (Meier et al., 19716). Fivizzani and
Meier (1978) and Meier and Fivizzani
(1980) proposed that the temporal relationship between the daily rhythms of prolactin and cortical steroids regulates seasonal migrations of F. grandis. According
to their model, hormonal rhythms are
entrained by photoperiod, and phase relationships are determined by temperature
(Spieler et al., 1976). Meier and co-workers
measured daily cycles of these hormones
in plasma of Fundulus at different times of
the year (Srivastava and Meier, 1972; Garcia and Meier, 1973). They found diel cycles
that varied with photoperiod and that generally coincided with predictions of the
model. However, similar investigations in
other species have not always agreed (see
Spieler, 1979 for review).
Audet et al. (1985) specifically tested the
Fivizzani and Meier model in two species
of migratory Canadian sticklebacks (Gasterosteus aculeatus and Apeltes quadracus).
Monitoring the effects of cortisol and prolactin on salinity preference offish that had
been acclimated to either short or longday photoperiods, Audet et al. (1985) found
that for both species, prolactin injections
shifted salinity preferences toward fresher
water, but there was little or no evidence
for a circadian relationship between the
two hormones in the control of salinity
preference. Furthermore, Audet et al.
(1986) found no significant diel variation
in cortisol titers in G. aculeatus. It is interesting to note in this regard that Bagger-
man (1957) found that thyroxin stimulated
preference for fresh water, and thiourea
induced preference for salt water in G. aculeatus. She also noted that thyroid activity
increases at the onset of migration (to fresh
water), although sticklebacks do not
undergo a metamorphosis equivalent to
that in salmon (Baggerman, 1957, 1959).
Clearly it is not possible to generalize as
to the specific effects of either thyroid hormones, prolactin or cortical steroids on fish
migratory behavior. All of these hormones
were probably involved in the pre-adaptations necessary for the evolution of
movement between areas of differing salinity. Differences in the specific details of the
hormonal regulation of the migratory
behavior itself may reflect the separate
evolution of such movements in a variety
of species and the opportunistic exploitation of osmoregulatory hormones along
lines dictated by specific selection pressures and physiological limitations.
ENDOCRINE CONTROL OF MIGRATION IN
HIGHER VERTEBRATES
In birds the earliest theories of hormonal control of migration (Rowan, 1926
et seq.) implicated the gonadal hormones as
causative agents. However, although
gonadotrophins and gonadal steroids can
play a role (see below), once again prolactin, thyroid hormones and possibly adrenal
steroids have been demonstrated to be primary in controlling migratory behavior.
Prolactin stimulates migratory restlessness (Zugunruhe) and fat deposition in the
white-crowned sparrow Zonotrichia leucophrys gambelii (Meier and Farner, 1964) and
the white-throated sparrow Z. albicollis
(Meier and Davis, 1967). In the latter,
Meier and co-workers have again shown
that the time of day prolactin is given is
important. Injections about 8 hr after lights
on (16L:8D) resulted in fat gains; injections
shortly after lights on did not, suggesting
that a second factor might be involved in
the response to prolactin. Meier?/ al. (1965)
examined the effect of prolactin alone and
in combination with other hormones on
body fat and nocturnal activity of Z. leucophrys gambelii. The conclusion of various
combinations of hormone treatments was
221
ENDOCRINE EFFECTS ON MIGRATION
that both prolactin and cortical steroids are
critical for migration.
Using Z. albicollis, Meier and Martin
(1971) investigated the effects on body fat
of injections of cortical steroids and prolactin given at varying intervals. They used
animals that had been made photorefractory by long exposure to long photoperiods, and they held these birds in constant
light—the assumption being that the animals then had little endogenous hormone
production and minimal or randomized
periodicity in whatever endogenous production did exist. Daily injections of prolactin that followed corticosterone by 4 or
12 hr resulted in fattening and increased
Zugunruhe. Furthermore Martin and Meier
(1973) reported that the direction of orientation of birds under the night sky was
to the south with a 4 hr treatment interval
and to the north with a 12 hr interval.
Meier et al. (1971a) showed that gonad
development of photostimulated birds was
enhanced by injections given at 12 hr intervals but not at 4 hr intervals; 8 or 20 hr
intervals were non-stimulatory for all
parameters in all experiments.
Seasonal variations in the diurnal cycle
of prolactin and cortical steroids were also
analyzed. Meier et al. (1969) examined diel
changes in pituitary prolactin content of Z.
albicollis via a pigeon crop bioassay at 4
times of the year. In the May and August
groups, daily fluctuations in pituitary prolactin (from pooled glands) were detected
(Fig. 1). In August the time of the peak was
shifted 12 hr out of phase with the May
peak. Dusseau and Meier (1971) determined plasma cortical steroid levels of Z.
albicollis at the same 4 times of the year.
Meier and Fivizzani (1975) determined
daily changes in corticosterone concentration using a more sensitive method (Murphy, 1967) in the same species at approximately the same times of the year, but
birds were maintained under artificial
lighting in either a long (16L:8D) or short
(10L:14D) photoperiod. Results for May
and Aug/Sept determinations taken from
the three papers are compared in Figure 1.
Dusseau & Meier (1971) Plasma Adrenal Steroids
Meier & Fivizzani (1975) Plasma Adrenal Steroids
Meier et al (1969) Pituitary Prolactin
zr <n
a> -p
3. <u
r- 55
u eo
(0 C
SI
38
E o.
0
2
4
6
8 10 12 14 16 18 20 22 24
Hour of the Day
FIG. 1. Circadian changes in plasma adrenal steroids
and pituitary prolactin levels in the white-throated
sparrow, Zonotnchia albicollis, at two times of the year.
Error bars = standard errors. Redrawn from Meier
and Fivizzani (1975), Dusseau and Meier (1971) and
Meier et al. (1969). See text for details.
al. (1969), that in May the difference in
timing between peak corticosterone and
prolactin release would be 10-14 hr,
according to their results a stimulatory
regime, while in August the interval would
be 5-9 hr, a non-stimulatory regime. The
data regraphed in Figure 1 do not seem to
support that conclusion. Furthermore,
using the diel periods of plasma adrenal
steroids as determined by Meier and Fivizzani (1975) for May and Aug/Sept, the
above relationships are also not obtained.
In May the peaks of prolactin and corticosterone are almost coincident, with prolactin leading by about an hour. If one
assumes that pituitary prolactin peaks
slightly precede plasma peaks, the two hormones would be maximum in the blood at
the same time. In Aug/Sept the peaks are
Meier et al. (1971a) state, based on results 12 hr out of phase; the latter would be a
of Dusseau and Meier (1971) and Meier et stimulatory relationship for gonadal devel-
222
M. A. RANKIN
changes in circulating T s and T 4 by RIA.
T 3 levels peaked in February and March
prior to vernal migration. T 4 levels were
high during April, May and June, peaked
again prior to the autumnal migration in
September, and again in January. It is
interesting to note that migratory Canada
geese show similar changes in thyroid hormones at these times of year (John and
George, 1978).
Investigating possible effects of prolactin, gonadotrophins, and gonadal steroids
on migratory physiology, Thapliyal and Lai
(1984) exposed spring-caught (photoresponsive) red-headed buntings to long photoperiods and various treatment regimes.
Testis and body weight decreased after
thyroidectomy; T 4 treatment of THX birds
elevated body and testis weight to that of
sham-operated birds. T 4 treatment of intact
birds had no effect.
After 4 mo under long days, the birds
were photorefractory (would no longer
respond to long photoperiods) and in all
treatment groups had decreased body and
testis weight; T 4 treatment administered at
that time had no effect even in THX animals. In such photorefractory animals prolactin injections either alone or in combination with testosterone or T 4 increased
body weight. However, prolactin could not
induce weight gain in thyroidectomized
animals, and T 4 injections either to intact
or THX animals did not stimulate weight
gain in photorefractory animals. It seems,
In another well-studied migrant, the red- therefore that both hormones may be necheaded bunting Emberiza bruniceps, the thy- essary for preparation for migration.
roid gland and prolactin seem to be the
A number of investigators (see Weise,
primary endocrine factors controlling 1967 for review) have reported that casmigration. Thyroidectomy (THX) per- trated birds of several species either
formed on animals recently captured in migrated as usual or underwent normal
their wintering areas reduced vernal pre- vernal premigratory fattening, apparently
migratory fattening and Zugunruhe; T 3 and refuting early ideas (Rowan, 1926) that the
T 4 replacement therapy restored fattening gonads played a major role in the control
and increased diurnal locomotor activity of migration. Weise (1967) reexamined this
(Pathak and Chandola, 1984). (However, question and found that if castration is done
for some reason, nocturnal activity was not in the autumn during the photorefractory
monitored in birds given replacement period, male white-throated sparrows
therapy. Since it is nocturnal activity that would not undergo premigratory fattening
usually increases substantially in migratory nor display migratory behavior in the
birds, failure to monitor this phase of the spring. Weise suggested that the effect of
activity is a puzzling omission.) Pathak and gonadectomy might be indirect due to a
Chandola (1984) also measured seasonal disturbance of the normal pituitary gonadopment according to Meier et al. (1971a),
but at that time, one would expect a nonstimulatory relationship if the model were
correct. Thus there are a number of problems with the Meier model. The prolactin
determinations were pituitary, not plasma
and were obtained by pooling glands from
several individuals. There were substantial
differences in the results of the two studies
on plasma adrenal steroids, and the possibility of handling effects on corticosteroid
levels and potential interference in the assay
by other steroid hormones were not adequately addressed. It would seem necessary
to repeat diel titer determinations of prolactin and corticosterone levels at various
times of the year using more sensitive techniques such as radioimmunoassay before
this model can be accepted even for the
white-throated sparrow. Nevertheless Miller and Meier (1983a, b) and Meier and
Wilson (1985) extend the model further,
reporting that the effects of prolactin and
corticosterone injections on gonadal development can be duplicated by injections of
DOPA (precursor to dopamine, the inhibitory factor for prolactin secretion in the
avian hypothalamus) and 5-HTP (a serotonin precursor), respectively. They report
that precursors had the same effects and
the same phase relationships with respect
to testicular recrudescence as injections of
prolactin and corticosterone. These experiments seem open to many sources of error,
and the results difficult to interpret.
ENDOCRINE EFFECTS ON MIGRATION
otrophin negative feedback loop and a consequent overproduction of LH that would
lead to diminished production of prolactin.
Schwabl et al. (1988), investigating this
question in female white-crowned sparrows found that ovariectomy in November
but not in January reduced vernal fat deposition, affected post nuptial molt, resulted
in lower than normal prolactin levels but
did not affect autumnal fat deposition.
They found, however, that the effect of
early ovariectomy on prolactin was not due
to abnormally high LH. The authors postulate that gonadal hormones may instead
regulate feeding behavior and/or induce
receptors for prolactin in the hypothalamus. This idea is supported by data from
Stetson (1971) indicating that lesions of the
anterior median eminence prevent fattening without affecting testicular growth.
Furthermore, intracranial administration
of prolactin in the ring dove (Streptopelia
risoria) increases feeding behavior (Buntin
and Tesch, 1985), and Buntin and Ruzycki
(1987) report specific binding of prolactin
in hypothalamic and other diencephalic and
telencephalic sites which may regulate
appetite.
223
Corticosterone levels did not vary consistently with migratory status in either study.
That only LH is suppressed in males, but
both gonadotrophins are reduced in
females may reflect the different reproductive strategies of the two sexes. Males
arrive at the breeding area with well-developed testes while most ovarian development occurs after arrival in response to
stimuli from mates and the local environment. Although interesting, these correlative studies do not demonstrate that the
gonadotrophins are part of the control of
migratory behavior or physiology, particularly since the correlations are opposite
in the fall and spring. However, the
approach of using partial migrants is a good
one. Experimental manipulations of the
endocrine system in such species may yield
excellent results.
In one of the few studies addressing hormonal control of migration in mammals,
Holekamp et al. (1984) examined the possibility that post-natal dispersal in Belding's
ground squirrels (which occurs solely in
males) was due to differences in androgen
levels between dispersers and residents. No
elevation in androgen levels was detected
Using a different approach to determine at the time of dispersal and no effect of
endocrine correlates of migration, Schwabl castration on dispersal was observed. Howet al. (1984a, b) measured levels of various ever, when females were injected immehormones in the blood of migratory vs. sed- diately after birth with testosterone proentary individuals in partially migratory pionate (TP), 67% of them underwent
populations of the European blackbird, dispersal 60 days later. TP-treated females
Turdus merula during the autumn and showed other signs of masculinized behavspring migrations, respectively. This ior as well. Unfortunately, no sham-injected
experimental paradigm allows comparison control females were recovered at the end
of hormone levels in conspecifics, only some of the experiment, raising the possibility
of which display migratory behavior when that all females (experimentals and conexposed to appropriate environmental trols) subjected to the manipulations of this
conditions. In the fall, rather than being experiment migrated. Thus, although these
lower in migratory animals as predicted, results suggest an organizational effect of
levels of gonadal steroids were higher in testosterone on the neonatal nervous sysfield caught first year migrants than in sed- tem which later results in dispersal, they
entary field animals. LH was low in all must be considered inconclusive. Clearly,
groups. In laboratory studies, some of the more work on the endocrine control of
same differences were seen but only during mammalian migration and dispersal is badly
one part of the day (Schwabl et al., 1984a). needed.
In contrast, in the spring Schwabl et al.
Thus prolactin and thyroxin, possibly the
(1984&) found that migratory males had two hormones with the most diverse effects
lower levels of LH and testosterone and among vertebrates (Gorbman et al., 1983),
females had lower levels of LH, FSH and emerge as the primary endocrine agents
5a-DHT compared to sedentary animals. influencing migratory behavior in a large
224
M. A. RANKIN
number of vertebrate species. Other hormones are also involved, but often their
role is not clear and may be secondary to
an effect of thyroxin or prolactin. These
two hormones influence migration from
the level of morphological and physiological changes that produce the migrant
morph to direct effects on behavior. There
has, however, been little work on the
mechanism of such behavioral effects at the
level of the nervous system, a fruitful area
for future research.
ENDOCRINE CONTROL OF
INSECT MIGRATION
As with vertebrates, there are many hormones that contribute to the regulation of
migratory behavior of insects, including:
adipokinetic hormones that are necessary
for fuel mobilization during flight; octopamine, which plays a role in fuel mobilization and may directly stimulate the flight
motor patterns in the thoracic ganglia in
some insects; ecdysone, which may affect
locomotor tendency of immature insects;
and juvenile hormone (JH), which can
affect development of the migratory morph
and migratory behavior in a number of
insects (see recent reviews by Rankin and
Singer, 1984; Rankin et al., 1986; Goldsworthy, 1983; Goldsworthy and Wheeler,
1989). This review will focus on the roles
ofJH.
Juvenile hormone has many functions
during the insect life cycle. Like prolactin
in amphibians, JH maintains the juvenile
morph. In the adult, it is usually necessary
for some aspect of oogenesis. It also affects
caste determination and dominance hierarchies in social insects, reproductive and/
or migratory behavior in other species. In
relation to its role in larval development,
the suggestion has frequently been made
that differences in JH regulate the development of winged vs. wingless morphs in
wing polymorphic insects.
Although the evolution of flight was
undoubtedly critical to the success of
insects, there are species from each of the
major orders of insects that are flightless
because all or part of the flight apparatus
is missing or non-functional. In some the
entire species is flightless, while in others
a polymorphism exists in which either environmental factors, genotype, or both control the alternate development of winged
and wingless (or long and short-winged)
forms within the same species (see reviews
by Harrison, 1980; Rankin and Singer,
1984; Rankin, 1989). One hypothesis often
proposed to explain the physiological basis
of this phenomenon is that wingless insects
are either juvenilized adults or sexually
mature larvae that have been produced by
supernormal exposure to JH during larval
development.
This question has been addressed in my
laboratory by Anthony Zera and Kristina
Tiebel in the wing polymorphic cricket,
Gryllus rubens. Zera and Tiebel (1988)
found that JH applications in the penultimate or early last larval instar could induce
short-wingedness in animals that had either
been selected for long wings (genetically
determined) or in which long wings had
been environmentally induced by exposure to high rearing densities (environmentally determined). Zera and Tiebel
(1989) also examined the levels ofJH esterase in the hemolymph of short and longwinged nymphs. This enzyme is responsible for degrading JH particularly at the
end of larval development prior to metamorphosis (Hammock, 1985). The hypothesis was that if short-winged animals have
higher levels of JH, they will have lower
levels of this enzyme. The reverse should
be true for larvae that will develop into
long-winged adults. When Zera and Tiebel
(1989) measured JH esterase levels in last
instar larvae from long and short-winged
stocks, they found significant differences
in the predicted directions between the two
morphs. Similarly JH titer determinations
showed that JH levels remain high longer
in animals destined to be shortwinged
adults (Zera et al., 1989). Differences in
ecdysteroid titers between morphs were
also detected. Taken together these results
clearly implicate JH in the control of development of the flight apparatus in this species. Previous work on other species of
hemimetabolous wing polymorphic insects
generally support these findings (see Rankin, 1989 for review). Zera and Tiebel's
studies on G. rubens are particularly impor-
ENDOCRINE EFFECTS ON MIGRATION
225
tant because they compare crickets whose ior. However, the opposite result was
wing morphology is genetically deter- obtained. Caldwell and Rankin (1972)
mined with those whose morph type is showed in Oncopeltus fasciatus that JH sigenvironmentally determined and find that nificantly increased the proportion of anithe hormonal controls are similar.
mals in a population making long-duration
Flight muscle degeneration at reproduc- tethered flights (a reliable indicator of tentive onset is a mechanism for rechanneling dency to migrate in this species). Precocene
resources from the flight apparatus into treatment caused a cessation of long durareproduction after long range movement tion flight activity and JH replacement
is no longer required (Nair and Prabhu, therapy restored it. Oogenesis was also
1985). In several species in which flight inhibited by precocene and restored by JH
muscle degeneration is associated with replacement therapy (Rankin, 1980). Thus
reproductive development, JH or JH mimic JH is necessary for both long-duration flight
applications or implantation of corpora behavior and reproduction in 0. fasciatus.
allata (the glands which produce JH),
Another insect in which the role of JH
induce flight muscle degeneration (see in migratory flight has been examined is
Rankin, 1989 for review). In the bark the ladybeetle, Hippodamia convergens
beetle, Dendroctonus rufipennis precocene II (Rankin and Rankin, 1980a). If prey are
(a chemical allatectomizing agent which scarce during the first several days after
causes deterioration of corpora allata and/ adult emergence, young adults enter
or decreased secretion of JH), delays flight reproductive diapause and an extended
muscle degeneration (Sahota and Farris, migratory phase. They move to montane
1980), and in D. pseudotsugae juvenoid aggregation sites where they may remain
applications increase flight muscle acid for several months before returning to
phosphatase activity, usually associated with lower altitudes to breed (Hagen, 1962;
flight muscle degeneration (Sahota, 1975). Rankin and Rankin, 19806). Juvenile horIn contrast, flight muscle degeneration mone is necessary for ovarian development
in the Colorado potato beetle Leptinotarsa in this species although, as with Leptinotarsa
decemlineata seems to be due to low JH lev- decemliniata, a cephalic factor seems also to
els. Flight muscle degeneration occurs after be necessary for completion of oogenesis
arrival at the diapause site and may be a (Rankin, 1982). JH mimic (altosid) stimumechanism to reduce metabolic rate (El- lates ovarian development in female//, conIbrashy, 1965) or ensure quiescence. Upon vergens, and long-duration flight behavior
re-emergence flight muscles regenerate as in both sexes. Precocene II inhibits flight
JH titers rise. Muscle regeneration may be activity and oogenesis for about 10 days;
entirely JH-regulated (DeWilde etai, 1968; application of altosid to precocene-treated
deKort el al., 1982), although the possibil- beetles increases migratory behavior and
ity of neurosecretory involvement has not stimulates oogenesis (Rankin and Rankin,
been excluded (Stegwee el al., 1963; 1980a).
deKort, 1969). JH seems to act directly on
Eurygaster integriceps is a hemipteran pest
the flight muscle (deKort el al., 1982).
of cereal and grain in Russia and the MidJH can also affect migratory behavior east with a life cycle similar to that of Hipdirectly and has been implicated in the podamia convergens. Precocene treatment
stimulation of migratory behavior in at least inhibits take-off behavior, suppresses
6 species of insects. Migration is pre-repro- migratory flight behavior and inhibits
ductive or inter-reproductive in most oogenesis in treated insects (Polivanova and
insects and full reproductive development Triseleva, 1985). The implication is that
usually coincides with a cessation or inhi- JH may coordinate both flight and reprobition of further migratory behavior. Since duction. Unfortunately, no JH-replaceJH is necessary for reproductive develop- ment therapy was given to precocenement in most insects, when the influence treated animals so that other explanations
of JH on migration was first investigated, are possible.
it was expected to inhibit migratory behavCoats et al. (1987) have investigated the
226
M. A. RANKIN
ready to begin reproduction immediately.
In insects in which migration may be
towards or away from an overwintering
habitat, there must, in addition, be a way
of stimulating flight without oogenesis. In
the ladybeetle, H. convergens, a second factor, probably from the brain, is also necessary for reproduction and its presence or
absence in conjunction with JH probably
determines whether or not the migrant will
initiate oogenesis. Variations on this physiological strategy are probably common
among insects with this type of life cycle.
The biogenic amine, octopamine, is the
substance most recently implicated in the
neuroendocrine control of flight behavior.
Octopamine is the only compound affecting insect flight behavior for which an
action directly on the nervous system has
been demonstrated (see Goldsworthy and
Wheeler [1989] for reviews). No experiments have distinguished between trivial
and migratory flight, but the response to
injected or iontophoresed octopamine can
be quite prolonged. When physiological
doses of octopamine are iontophoresed into
specific regions of the metathoracic ganglion of locusts, bouts of rhythmic stepping
or flight behavior are elicited, depending
We have also examined the effect of on the location of the electrode. Leg moveremoval of the CA in the monarch butter- ments characteristic of fast walking or
fly (Rankin et al., 1986). In this experiment marching can be elicited at certain sites
the equivalent of late winter animals were while flight is stimulated in each of two
allatectomized and given tethered flight regions of the ganglion. The octopaminetests. Some of the allatectomized animals stimulated flight motor output is always
received JH replacement therapy. Allatec- bilateral and proportional to the amount
tomy significantly reduced and JH restored of octopamine delivered to the preparathe tendency for long-duration tethered tion. Recovery from the drug is relatively
flight in monarchs.
slow, characteristic of modulatory action
Most recently we investigated the effect (Sombati and Hoyle, 1985). An interesting
of JH on flight behavior and oogenesis of area for future research might be an examAnthonomus grandis, the cotton boll weevil. ination of the possible interactions between
This species is especially interesting to us JH and octopamine in the control of insect
because it is probably a short distance migratory behavior.
migrant in which flight is a highly facultative response to a variety of environmenCONCLUSIONS
tal cues. Again JH stimulates both longduration flight behavior and oogenesis in
Hormonal control of migration can occur
this species (Rankin et al., ms. in prep).
at several levels. Hormones influence
Thus in some insects, possibly in partic- development of the migratory morph; they
ular those having a colonizing life history regulate fuel mobilization and other physstrategy (Rankingal., 1986),JH stimulates iological adjustments involved in long-disboth flight and oogenesis such that the tance movement; they induce migratory
migrant would arrive at its new habitat behavior itself by a general change in loco-
effects of a JH mimic, methoprene and a
JH inhibitor, fluoromevalonate (FM) on
flight behavior of the chrysomelid Diabrotica virgifera virgifera. Flight time and
distance on a flight mill, and take-off propensity in the presence of vegetative stimuli were measured. Only intact (rather than
ovariectomized) females were used, making results somewhat ambiguous. However, methoprene clearly increases longduration flight behavior among virgin
females. Mating induces both ovarian
development and long-duration flight
activity; JH mimic treatment of mated
females increases long-duration flight but
only briefly. FM first decreases and then
increases flight activity of mated females,
perhaps by producing intermediate JH levels. Treatment of virgins with the inhibitor
has no effect (neither FM-treated nor controls made a long flight). These results are
consistent with the interpretation that both
flight and reproduction are JH dependent,
but at high JH levels oogenesis is favored
and inhibits long-duration flight. Other
interpretations are possible, however, and
cannot be eliminated without more definitive experiments.
ENDOCRINE EFFECTS ON MIGRATION
motor tendency, habitat or substrate preference; and they may act directly on the
CNS to release or trigger motor programs
involved in long-distance locomotion and
cessation of movement when appropriate.
The specific effects of hormones on migratory behavior may have evolved secondarily to their control of the physiological
parameters that were important to successful migration (control of metamorphosis, osmoregulation, thermal tolerance in
the case of prolactin and thyroxin in vertebrates; control of adult morphology and
oogenesis in insects). More work needs to
be done at all levels of hormonal control
of migration. There is a particular need,
however, to broaden the number of species
and higher taxa in which endocrine effects
on behavior and on the nervous system have
been studied in detail.
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