AM. ZOOLOGIST, 12:77-93 (1972).
Adaptive Functions of Vertebrate Molting Cycles
JOHN K. LING
Department of Biology, Memorial University of Newfoundland,
St. John's, Newfoundland, Canada
SYNOPSIS. Cyclic epidermal cellular proliferation, with or without keratinization, is a
vertebrate characteristic. Such activity probably obeys an autonomous rhythm which is
regulated through neuro-humoral systems in response to environmental (proximate) stimuli and related to adaptive (ultimate) factors. In seeking cause and effect
relationships, however, it becomes apparent that the same environmental parameter
may be both an ultimate and a proximate factor, the latter also regulating the rate of
response. With regard to molting in homoiotherms, temperature acts in such a capacity
in many species.
Periodic shedding of the outer epidermis in fish, amphibians, and reptiles does not
appear to be correlated with seasonal factors to the extent that avian and mammalian
molts are.
The evolution of vertebrate molting cycles has amounted to the entraining of
inherent epidermal cycles with seasonal demands by the organism itself and the
environment; these demands act as regulating mechanisms. Preadapted structures such
as feathers and hairs function collectively as plumage and pelage in their various roles
but separately in their growth and replacement cycles which, however, are coordinated
for maximum functional efficiency. Molting is also synchronized with the seasonal
cycle according to the availability o£ energy resources and time to complete the
essential functions (in addition to molting) . The evolved molting systems, as
manifested in the great variety of patterns and types in the vertebrates, may thus be
regarded as almost individual responses to selective pressures acting on a universal
vertebrate character.
The basic regulatory system involves the neuro-hypophyseal complex which controls
target endocrines affecting various functions which themselves influence epidermal
mitosis and, ultimately, molting. The mechanism in its simplest form controls the
animal's metabolism through the thyroid acting independently in a permissive capacity
or synergistically with the adrenal and gonadal hormones which are regulated
directly and/or indirectly through negative feedback.
of longer periodicity involve practically
the whole of the outer coverings: skin,
Vertebrate epidermal cyclic activity is scales, feathers or hair.
adapted to continuous, frequent or infreTo this latter phenomenon I would apquent renewal of parts of the epidermis or ply the term molt (Latin: mutare = to
its derivatives. Even apparently continuous change), with all its ecological connotacell proliferation and desquamation in- tions, while preferring the term slough to
volve alternate active and quiescent phases be more apposite to the process of frag(Bullough, 1962). Less frequent epider- mentary desquamation. Thus, these two
mal cycles have a periodicity which may or kinds of epidermal cycles are not strictly
may not be regular, or related to seasonal confined in application to discrete verteregimes. Whereas the continuous desqua- brate classes. This essay, however, is conmation of epidermal derivatives is usually cerned largely with the relatively massive
marked by the shedding of small frag- changes which take place periodically and
ments, e.g. the dandruff of mammals, cycles result in complete renewal of the outer
integument. It will stress, moreover, the
. , ,. . . . need to understand and relate to ecological
„ . . . „ . .
c
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INTRODUCTION
Studies in Biology from Memorial University of
Newfoundland, No. 318. Contribution from the
Centre for Environmental Biology, No. 18.
...
and
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physiological conditions, not only the
externally visible changes, but also the
77
78
JOHN K. LTNG
subcutaneous activity which manifests itself
ultimately in the molt. The nature and
timing of these subsurface responses must
be known if cause and effect relationships
involving proximate (environmental) and
ultimate (adaptive) factors are to be elucidated.
The functional role of the integument is
broadly the same in all vertebrates, yet
highly variable with respect to particular
adaptations. As each of the classes have
adapted to various niches, the integument,
too, has undergone changes related to its
changing role. The mammals, however, occupy a wider variety of niches than any
other class of animals and the mammalian
integument shows commensurate variety of
function and form (Ling, 1970).
Periodic renewal of the outer zone or
derivatives of the integument provides a
heavier or lighter coat, a cryptic or conspicuous shade, a new plumage prior to migration or allows for growth or wear and
tear. All of these phenomena involve epidermal proliferation and shedding, processes which occupy variable periods of
time during different phases of the annual
cycle. The relationship of the molt to the
annual cycle is the pivotal point around
which revolve the adaptive functions of
this particular feature in the biology of
vertebrates (and, of course, invertebrates).
Krejsa (1970) has invoked the term
"functional epithelial extinction" to include the variously and vaguely defined
processes such as ecdysis, molting, shedding
and sloughing, all of which do not necessarily involve replacement of kcratinizcd
structures and are not confined only to the
integument. Krejsa believes his to be a
unifying concept under which the vertebrate integument in particular may be
studied as a functioning organ system.
For birds Humphrey and Parkes (1958)
proposed that a plumage cycle should extend from one point in feather replacement to the same point (of the homologous plumage) the next time around. Such
a c)tle could thus include several molts of
different plumages before the process was
repeated.
THE NATURE OF EPIDERMAL CYCLES
IN SPACE AND TIME
Continuous or periodic epidermal cellular proliferation takes place in all five vertebrate Classes. It manifests itself in fragmentary desquamation or the shedding of
whole cornified epithelia, feathers, or hair.
The cellular processes are essentially the
same, involving the germinative layer of
the epidermis or its homologue in the production of cells or structures which are
fated to migrate towards the skin surface
undergoing changes as they do, finally to
die and be cast away. While the details of
these aspects of the molting or sloughing
process are not within the scope of this
paper, the response to various factors controlling the grosser functions of molting is,
in the final analysis, at the cellular level.
When considering the time dimension of
molting, it is necessary to bear in mind
that each cycle includes active, transitional, and quiescent phases; e.g., anagen, catagen, and telogen in the mammalian hair
growth cycle (Dry, 1926). The shedding
phase, therefore, may occur almost at any
time during the growth of a new generation or even after one or more such new
generations have also entered a quiescent
state. Thus, while the adaptive role of
shedding or retaining the epidermal derivative in question may be obvious, the
proximate factors involved in timing the
process may be entirely obscured.
The duration of a complete epidermal
(molting) cycle must be regarded as the
period between the earliest cellular activity, which precedes growth and the actual
shedding of the dead structure. This period may vary in forms which retain an older generation after a new one has also
reached a resting stage or when molts occur at irregular intervals. The period of
active growth, however, will normally be
constant throughout the life of the animal
and will not vary greatly between individuals of a species.
VERTEBRATE MOLTING CYCLES
Fish
A general account of the structure and
functions of the skin and scales of fish is
given by Van Oosten (1957). The skin
proper is of typical vertebrate character,
having epidermal and dermal layers. The
characteristic scales of bony fish are entirely dermal in origin and are not subject to
periodic replacement but grow more or
less continuously throughout life unless injured, when new ones develop. Placoid
scales or denticles of the elasmobranchs are
derived from both dermal and epidermal
components and may be renewed when
old, worn out, or lost. As a general rule,
the skin tends to be thicker in fish having a
reduced scale covering.
The superficial epidermal cells remain
metabolically active until they die off and
are replaced. They secrete mucus and an
extracellular coating layer to which the
term cuticle has been applied. It seems,
however, that not all species develop a
cuticle. Replacement of worn out or injured cells takes place continuously, but,
apart from a slight flattening, the new cells
do not alter, e.g. to the extent of being
cornified, as they move to the superficial
zone from the germinal layer. Only in the
development of specialized pearl organs
does a process of cornification occur.
Gilchrist (1920) and Heldt (1927) describe a form of ecdysis which occurs in the
South African horsefish, Agriopus, and
the flying gunard, Dactyloplerus. In both
of these species the cast off material is
produced by the superficial epidermal cells.
The nature of the molt in Dactylopterns,
in which an extensive outer layer is lost,
suggests that parts of the epidermis itself
could be involved in the shedding process.
Products of the epidermis of fish rather
than the epidermis itself are important in
various life supporting functions. The mucus reduces body friction in the water
(Rosen and Cornford, 1971), acts as a barrier to various pathogens, regulates osmotic
action, and lubricates the skin surface so
that suspended particles may be precipitated and removed from the body. The
79
cuticle also acts in much the same way as
the mucus. It is evident from the fact that
the cuticle is easily torn off that it does not
have very great tensile strength. Over
finrays, however, it tends to assume a
fibrous texture in contrast to a rather more
fluid state over the body surface.
Epidermal mitotic activity in the integument of fish is thus geared to maintaining
a layer of active secretory cells at the skin
surface and replacing inactive dead cells.
This kind of desquamation probably follows a typical vertebrate pattern.
Amphibians
Life in both the aquatic and aerial environment manifests itself in a number of
adaptations in the amphibian integument.
The main functions of this organ are respiration and mechanical and chemical
protection, towards which ends we find the
development of mucous glands in waterinhabiting amphibians and keratin on the
outer surface of terrestrial forms. In the
more aquatically adapted members of the
Class, an outer cuticular margin is secreted
by the distal epidermal cells which comprise the cuticular layer.
The fully aquatic axolotl, Ambystoma,
does not develop a horny layer. Persistent
larval forms such as Proteus and Necturns
have only localized areas of keratinized
skin on the tips of the digits, but keratin
does not otherwise occur in the epidermis
(Dawson, 1920). Tadpoles have a nonkeratinized epidermis, but have horny
teeth. Frogs, toads, and salamanders develop a complete horny layer (Elias and
Shapiro, 1957; Spearman, 1968). The superficial stratum corneum consists of one
or two layers of closely joined keratin ized
cells.
Sloughing of epidermal surface material
occurs in amphibians having either keratinized or non-keratinized structures.
Only the outermost layer is generally shed,
while the cells below remain attached to
the underlying malpighian zone from
which a new generation will develop. In
the salamander the transitional cells below
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JOHN K. LING
the horny layer begin to cornify individually, and neighboring cells are generally
out of phase with each other. This is in
marked contrast to the uniformly keratinized surface cells of higher vertebrates.
Only the cells bearing the cuticular margin
are shed by Necturus. Fully keratinized
amphibian cells develop strong lateral attachments to each other through fusion
along their borders. Union between flat
upper and lower surfaces is much weaker
and consequently a complete one-cell thick
horny layer is cast off (Spearman, 1968).
Shedding probably does not occur, however, before the second layer — soon to become the surface —is entirely cornified
(Elias and Shapiro, 1957). Thus, in Bufo,
for example, the old skin surface can be
shed almost as a single sheet but not before
its replacement is able to provide the essentially tough and impervious outer layer. In
Rana, however, the horny layer is shed
fragmentally (Goin and Goin, 1971).
Molting in the Amphibia seems to be
subject to little or no seasonal control, although Necturus is said to molt only in the
winter (Dawson, 1920). The process appears to be primarily a means of eliminating unautolyzed material from epidermal tissues, so that it may serve an excretory function as in arthropods in which successive ecdyses accommodate increasing
body size. Most amphibians molt every few
days, either continuously over the entire
year or in bursts of a dozen or more molts
followed by a resting period. Ambystoma
sheds its outer skin every 4 to 5 days (J0rgensen and Larsen, I960). The spotted
newt, Diemyctylus viridiscens, spends
about 9.2 percent of its life shedding successive epidermal generations, each molt
taking about 14 hours to complete at 20° C
(Adolph and Collins, 1925). The duration
of the intermolt period (d.i.p.) at 20°C in
Bttfo bufo is 7 to 11 days and 7 to 8 days
in B. mnrinus (J0rgensen and Larsen,
1961). Bensden (1956) reported that the
d.i.p. for B. bufo ranged from 8 to 19
(mean: 12.4) days at 16 to 18°C and
from 5 to 13 (mean: 8.9) days at 20 to
30 °C. The mean d.i.p. at 20 °C for B. regu-
laris is 5.8 ± 0.1 days, for B. carens 4.3 ±
0.1 days, and for Breviceps mossambicus
5.7 ± 0.2 days (Bouwer et al., 1953). In
Bufo regularis actual shedding takes 1 to 2
hours at 20°C, but is completed in only 20
minutes at 30°C; it is also rapid in B.
americanus.
A mid-dorsal split from the level of the
parotid glands to the base of the urostyle
marks the beginning of a molt in B. regularis. Using the hind legs the toad then
loosens the slough from the upper flanks
forward, then to the lower flanks and forward again over the head and finally into
the mouth to be eaten (Taylor and Ewer,
1956). A similar process has been described by Bensden (1956) in B. bufo. The
purpose of ingesting the slough is unclear, but possibly it may be partly recycled
to provide new materials for subsequent
epidermal generations which turn over
with such rapidity. Molting begins on the
head, extends over the trunk, and ends on
the tail and limbs of Diemyctylus, or it
may occasionally take place over the whole
body simultaneously. The epidermal layer
frequently comes off in a single sheet and
parts of the slough may be consumed
(Adolph and Collins, 1925).
Reptiles
Molting in reptiles is a more widely
known phenomenon than it is in amphibians and, certainly, fish. Sloughing cycles in
snakes and lizards have attracted more attention than those of crocodilians and chelonians, and most descriptions of reptilian
molts are concerned with squamates.
Among recent investigators, Maderson
(1963, 1964, 1965a,6,c, 1966) and coworkers (Lillywhite and Maderson, 1968;
Maderson, May hew, and Sprague, 1970)
have opened up whole new areas of knowledge on the structure, development, and
shedding of squamate reptile epidermis.
While these and other exhaustive histological studies are highly relevant to the
present discussion, they are really beyond
the scope of this essay. They will be
referred to only in relation to adaptive
VERTEBRATE MOLTING CYCLES
features of reptilian molting.
The scaly surface of (squamate) reptiles
is essentially a greatly folded epidermis of
which the "hills" and "valleys" are the
scales and hinge regions respectively. Saggital sections of scales reveal that the outer
surface and folded hinge regions and inner surface are different in structure. Basically, a scale consists of deep and superficial dermal strata and an epidermis. The
epidermis is composed of a germinal layer,
a zone of living cells and an inner (tt)
and outer (/3) layer of keratin. The three
last-named strata make up the outer epidermal generation and represent a resting
condition of the epidermis. On the outer
surface of each scale, the /?-layer of keratin
is thick and sculptured with patterns that
may even be species specific. The a-layer of
keratin is relatively thinner than the
/J-layer in this region and relatively much
thicker on the inner scale surface and
hinge region.
During a squamate molt, the outer epidermal generation separates from a newly
formed inner epidermal generation of the
same composition. The mechanism by
which the outer epidermal generation becomes separated from the rest of the animal is still a matter of some conjecture.
There is a growing evidence, however, that
enzymatic digestion in the splitting zone
(Maderson, 1967) is not involved in the
process as previously thought. This splitting zone is originally comprised of two
layers of living cells below the /3- and a-layers of keratin in the resting condition of
the epidermal cycle. As epidermal cellular
activity proceeds prior to another molt a
clear layer replaces the two living cell layers. Just before shedding actually occurs,
this clear layer undergoes a sequence of
nuclear and cytoplasmic degeneration
which results in the destruction of the living connection between the new and old
epidermal generations (Maderson, 1965c,
1966). The outer two layers of keratin are
finally shed in small or large sheets or even
as a complete skin, the outer pattern of
which is reproduced on the surface of the
underlying new generation. This state
81
marks the end and the beginning of the
squamate molting cycle.
Maderson (1965c) divided the squamate
sloughing cycle into six stages beginning
with the "resting" condition (stage 1) and
ending in the shedding of the old skin
(stage 6). The actual duration of complete
cycles or the times occupied by individual
stages are known accurately for very few
of the many species which Maderson has
studied. This is because much of the material came from museum collections or animals raised in the laboratory under variable ambient conditions. In Anolis carolinensis, however, the proliferation-renewal
phase (stage 2 to stage 6) occupies 7 to 9
days, and the mean intermolt period is 22
days (Maderson and Licht, 1967) . Temporal data for Elaphe taeniura are incomplete (Maderson, 1965c), but, by interpolating a duration of 1 day each for stages 3
and 4, a proliferation-renewal time of 9 to
13 days is obtained. Structural changes in
the adult epidermis merely repeat those
stages in development which follow early
histogenesis of embryonic epidermis. It is
not known whether the same time sequence is followed as in morphogenesis,
but this would be expected to occur. All
body regions of most species are closely in
phase with respect to histological changes
in the adult epidermis before molting. In
the embryo, however, histogenesis over
different body regions is out of phase until
just before the first molt (when the periderm is shed); here a pause takes place
while all regions "catch up" on the histologically most advanced loci.
Except in a very few instances, therefore, shedding occurs simultaneously over
the whole animal either in large flakes or
as a complete skin. There are certainly a
number of molts each year; tropical forms
may shed almost all year round while temperate forms molt one, two, or three times
each year.
Retention of layer upon layer of old
horny cells appears to be peculiar to chelonians and crocodilians. These layers often develop annual rings in winter hibernating tortoises (Spearman, 1969).
82
JOHN K. LING
Oliver (1955) suggested and Smith
(1935) stated that all geckos eat their shed
skins which are generally softer than those
cast off by other lizards and snakes.
Birds
The ecological and physiological aspects
of avian molts are perhaps better understood than for any other vertebrate class.
Studies of molt patterns and timing, however, not to mention the histological basis
of plumage changes, are still only scantily
documented. Thus, accurate information
about integumentary changes in terms of
both space and time is largely lacking.
This is surprising in view of the relationships being sought between molting and
other phases of the annual cycle, proximate and ultimate factors and other cause
and effect phenomena. Welty (1964)
gives a lucid general account of avian
molts and their environmental correlates.
However, Voitkevich (1966) has provided
the most comprehensive treatment of the
subject to date. The extensive studies reported by Rawles (1960) and by Voitkevich (1966) largely concern plumage development and changes in domestic chickens and pigeons. Morphological events in
other species of birds would be expected to
resemble those of pigeons and fowls, but
the time factors would be very variable.
Voitkevich (1966) concluded that development of a new feather anlage and
shedding of the old plume are directly
related. Feather growth which may be induced by plucking can thus be timed and
growth rates thereby established. It would
be necessary to perform such an experiment for each species, however, in order to
determine the duration of growth from
the anlage to a definitive feather. Only
then would it be possible to correlate external factors with successive stages of
plumage development. The growth rate of
any individual feather during each molt is
the same as when the first feather was
formed. Moreover, feathers are replaced in
the same order as they were developed.
Feathers located in different regions or
tracts (pterylae) do not always grow at the
same rate; however, those of equal size do
have similar growth rates whether located
in the same or a different tract.
New feathers can be induced to grow if
old ones are plucked even outside the normal molting season. No more than three
generations can be induced, however, in
any given period between spontaneous
molts (Streseman, 1927). The anlage of
the new feather develops before the old
plume is shed; indeed the latter appears to
be pushed out by the former as it grows.
The young feather appears at the skin surface at the precise time the old one is shed.
Often, if a feather is pulled from its follicle before it is shed spontaneously, the new
feather shaft is also dragged out, attached
to the old quill. There is no doubt that the
developing feather is capable of pushing
out the old one. Voitkevich (1966) cites
his own experiments in which not only is
the old feather ejected when reinserted in
the follicle, but an extra feather held by
clamps to the upper edge of the follicle is
also pushed out.
Histological changes in the epithelial
wall of the follicle precede the growth of
the new feather anlage. Intensive keratinization and desquamation of the outer layers loosen the attachment of the old
feather to the follicle, enabling it to slide
more easily ahead of the growing shaft.
The follicle thus supports the fully developed feathers; the depth of the follicle
is directly related to the functional importance of the plume. There are two other
functions of the follicle. Its proximal
region passes directly into the feather germ
and its more distal tubular part guides the
growing feather (which may be induced
to follow another route to the skin surface
if the follicle is blocked but an aperture is
provided in the follicle wall).
Inductive relationships between dermal
and epidermal components of the feather
germ and old and new structures in the
follicle are beyond the scope of this broad
outline. An understanding of these morphogenetic phenomena is essential, however, it the nature of the responses of feather
VERTEBRATE MOLTING CYCLES
follicles to environmental stimuli is to be
fully comprehended. At the gross level, for
example, growing feather follicles are
influenced by adjacent more advanced
ones; individual feather tracts have their
specific growth gradients; local skin conditions, if established early enough, can have
a lasting effect on feather generations.
These conditions may change during the
life of the bird, however, correlated with
the survival value of the plumage.
Mammals
I have recently reviewed mammalian
pelage and molting in some detail (Ling,
1970) and any comments in the present
context would provide little more than a
rather inadequate resume of the more extensive survey. Even generalizations are
difficult to make; the most sweeping might
be the lack of a basic temporal and spatial
pattern underlying pelage replacement in
its various forms throughout the Class.
Mechanisms controlling mammalian molting certainly involve essentially the same
organ systems as in other vertebrates, but
in matters of detail and their relationship
to adaptive roles, many processes within
the pelage cycle remain uncomprehended.
Molts faithfully repeat morphogenetic
events beyond the stage of primordial folliculogenesis both in morphological and
temporal terms. There is no evidence,
however, to support the notion that pelage
replacement patterns follow the same topographic sequences as hair follicle development. This is borne out in particularly
striking fashion by the fact that two or
more seasonal molts may take place in different or even reverse directions over the
body. This invites further enquiry as to
what switches these replacement waves on
and off, and what adaptive function, if
any, the changed molt pattern provides.
Certain histological changes occur in the
epidermis and dermis during pelage replacement, including the appearance of
structures which are absent or greatly reduced at other stages of the pelage cycle.
For example, a granular layer is almost
non-existent in the skin of the elephant
seal, Mirounga, except during the annual
molt (Ling, 1965). In the fur seals, Callorhinus and Arctocephahis, and sea otter,
Enhydra, however, this layer is always well
developed. Keratohyalin seems to be associated in aquatic mammals with denser
pelage and its paucity in hair seals (Phocidae) is possibly related to the parakeratotic condition evident in the horny layer
of these forms. It is present mainly in the
vicinity of the hair follicles and gland orifices in sparsely haired phocids during
each molt, but occurs over the general skin
surface in more densely haired seals and
not only at the time of molting. The data
necessary to explore these evolutionary
trends are still too inadequate to allow
generalizations on universal differences between the skin and pelage of aquatic, amphibious, and terrestrial mammals.
Another feature, so far exemplified only
in the hair follicles of Mirounga and Phoca, is the failure of the bulb to degenerate
to any great extent as it enters the resting
stage (Ling, 1965; Montagna and Harrison, 1957). This is in contrast to, for
example, the mouse (Montagna, 1962) or
chinchilla (Lyne, 1965) in which the bulb
regresses to a small knot of cells connected
by a thin strand of dedifferentiated epithelial cells, the hair germ. This relatively
intact, though shrunken, follicle is perhaps
not to be expected, in view of the quite
precisely timed annual pelage change in
seals compared with the regular monthly
hair growth cycle in the mouse. Replacement of the pelage in phocids is comparatively quick, however, as is the regular hair
growth cycle of the mouse, so there is no
apparent advantage in either system.
Generally speaking, there is a great
dearth of comparative microanatomical
data on the pelage cycles of mammals, and
functional aspects at this level are almost
completely unaccounted for.
FACTORS WHICH INFLUENCE MOLTING
Seasonal Cycles
Most vertebrates' lives revolve around a
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JOHN K. LING
yearly cycle of events — breeding, feeding,
fasting, molting, etc. — but a few, particularly some of the very large mammals, have
two- and even three-year cycles. It is not
insignificant that these animals are virtually hairless and/or tropical, so that seasonal
molts do not manifest themselves anyway,
at least insofar as available data show. For
the purpose of the present discussion, vertebrate molting cycles will be considered in
relation to annual cycles unless otherwise
stated.
A hairless or featherless skin, whether
combined with an aquatic way of life or
not, is generally subject more to short-term
molts than to a few seasonal replacement
cycles. This applies with particular force to
fish, amphibians, and reptiles in which
molting does not appear to be directly
related to seasonal factors. On the other
hand, the warm-blooded birds and mammals, and more especially those of higher
latitudes, assume different plumages and
pelages having very definite seasonal roles.
Hirsute amphibious and aquatic mammals,
however, tend to molt once each year, but
the hairless cetacea undergo a continuous
process of epidermal sloughing. Neither
molting nor sloughing in these forms is
related directly to seasonal needs, but each
process is coordinated with respect to other cyclical phenomena. The aquatic environment appears to be sufficiently uniform
to preclude the need for different outer
coverings at different times of the year.
Even migratory aquatic mammals which
may move between sub-polar and warm
temperate latitudes do not compensate for
variable water temperatures, at least in respect to growing coats of appropriate quality to meet the environmental conditions.
The scaleless South African horsefish,
Agriopus, periodically sheds an outer covering of columnar outgrowths from the superficial epidermal cells (Gilchrist, 1920).
Although it is not known when this shedding process occurs or how frequently, it
seems to be related less to seasonal regimes
than the need for replacement of wornout tissues. Two other species of the same
genus undergo a similar form of ecdysis
which is equally unrelated to season and
has its counterpart in no other fish.
Epidermal molting is much more prevalent in amphibians than in fish. Since the
important functions of the amphibian skin
include respiration, water absorption, and
excretion of unautolyzed materials (Bensden, 1956; Adolph and Collins, 1925), renewal is almost continuous and, furthermore, it must be accomplished quickly.
Seasonal changes in molting frequency in
Bufo, if any, are slight, although there
may be a slowing down, i.e. greater
intermolt period with the passage of time
(Taylor and Ewer, 1956; J0rgensen and
Larsen, 1961). Molting certainly takes longer in toads nearing death (Adolph and
Collins, 1925) and is suppressed or nearly
so when they are taken from one environment to another. Drying also hastens the
onset of a molt (Dawson, 1920). In
nature, this could coincide with the onset
of breeding status or be related only to a
habitat change (J0rgensen and Larsen,
1961).
Taylor and Ewer (1956) found that
molts are not affected by age, size, or sex.
Feeding does not affect the frequency of
shedding, but raising the temperature increases the rate of molting. The molting
frequency is higher under conditions of
constant light than in constant darkness.
During alternating periods of light and
dark, shedding is more likely in the light
at temperatures between 25° and 30°C,
but this preference disappears at 20°C.
Adoption of an amphibious way of life,
the phases of which are certainly governed
by the seasonal cycle, must bring about
integumentary adjustments which enable
essential functions to continue under
changed conditions. While drying and increased temperature both cause a hastened
molt and consequently a greater metabolic drain on the animal, the return to water
to breed permits at least some metabolism
to be switched over to the production of
gametes. It is interesting, therefore, to
speculate on whether continuous and even
hastened molting will prevent the onset of
breeding status or if reproductive condi-
A
VERTEBRATE MOLTING CYCLES
tion governs the frequency of molting. In
either case, a rather neat adaptive relationship exists.
Having forsaken the water for the purpose even of breeding, the reptiles are
faced with the kinds of environmental conditions which appear to stimulate amphibian molts. The reptilian integument,
however, has evolved to prevent desiccation of the body and is itself dry and impervious, due largely to the massive production of keratinized scales. Some of these
structures have become modified to assist
in locomotion, for example, the development in snakes of large ventral scales
which are moved by series of muscles and
the presence in lizards of digital setae and
claws to increase traction. Apart from the
possibility that the reptilian integument
has certain heat absorbing and radiating
properties, it does not function in a thermoregulatory (i.e., insulative) role similar
to that of the homoiotherm integument.
Of all the functions mentioned above, locomotion associated with seasonal activity
seems the only likely one to be related to
any biological rhythm.
Maderson, Mayhew, and Sprague (1970)
have presented what appears to be the
only available information on the sloughing frequency of reptiles throughout the
active part of the animals' year. While species-specific patterns may exist, these do
not correlate with known ecological conditions and are not related to reproductive
status. From zero to 30 percent of animals
were about to shed in any month between
April and October. There was a consistently higher percentage of shedding animals
in April or May, followed by a drop and
then an increase again in October in one
species, Uma notata. In another species,
Dipsosaurus dorsalis, shedding was prevalent in April but became less frequent until it ceased in September upon the reptile
entering into hibernation. While there was
an apparent link between above-ground
behavior (solar radiation?) and molting
and a reduction in molts when below
ground for egg laying, similar discrepancies at other times indicate no real rela-
85
tionship between the reproductive cycle
and skin shedding. The consistently high
frequency of molting in spring, however,
could be explained by one of several seasonal factors following the winter dormant
period: (1) increased metabolism, (2)
growth, (3) the effect of warmth on the
epidermis. Otherwise obscure adaptive
functions may also be related to these or
unknown factors.
It should be apparent by now that the
most obvious adaptative features of seasonal changes in the vertebrate integument
are to be found in skin appendages rather
than the skin itself. The most highly developed appendages, of course, are the
feathers of birds and hairs of mammals —
the most characteristic external features of
these homoiotherms and their most essential structural thermoregulatory device.
Plumage is also vital to all flying birds.
Along with the pelage, which also subserves an indirect role in (particularly
aquatic) mammalian locomotion, plumage
is adapted for cryptic and display coloration, buoyancy, mechanical protection and
the brooding of young, as well as being
used for nest building purposes.
When not subjected to actual wear and
tear, plumage and pelage have several important seasonal roles to play, and these
require the donning of one or more "costumes," changes being effected "between
the scenes." In other words, seasonal
plumage and pelage changes or molts take
place in anticipation of the next functional role in the outer vestiture. Molt can be
presumed to take place in such a fashion
as to maintain this outer covering at the
highest possible level of functional efficiency commensurate with other demands.
Chief of these demands is the energy expenditure associated with the molt itself
both in maintenance of body heat during
the molt and the synthesis of — particularly in birds — large amounts of keratin over
a brief period.
Much more is known about the relationship of the reproductive cycle to other
phases of the seasonal cycle than to molting, and avian molts and their place in
86
JOHN K. LING
the life of the bird are rather better
documented than mammalian molts in the
same context. In extensive studies by,
among others, Davis (1971), Evans (1966,
1969), Holmes (1966aA 1971), Lofts and
Murton (1968), Miller (1961), and Ward
(1969), gametogenesis and breeding, nutrition, winter fat deposition, migration,
and molting are variously considered in
relation to one another and to the adaptive function of the annual cycle.
Because of the important function of
feathers in flight, most avian molts proceed
in such a manner as to preserve the power
of flight. Some birds, however, for example, the flightless penguins, lose their
plumage from the whole body simultaneously. Many other aquatic birds shed all of
their large flight feathers at once, so they
are rendered flightless for a short period,
during which time they seek shelter from
predators out on the water. The total molting time is greatly reduced through this
expedient.
In those birds which retain the power of
flight during the molt, the feathers are
shed symmetrically on both sides, i.e., homologous plumes are exchanged simultaneously. The exact order varies according to the species concerned, but it
appears to be a general rule that the most
essential flight feathers, e.g., the outer primaries, are last to molt. Each feather in a
molt sequence is shed after the preceding
one has completed about one third of its
growth; and the flight feathers begin molting after about one third of the smaller
feathers have been renewed. Some birds of
prey do not complete their plumage
change in a single year but take two years
for the process. Conversely, diurnal birds
of prey, such as eagles, often undergo a
continuous molt. Where both sexes care
for the young, molting takes place in only
one partner at a time, so that the other can
fulfill its parental obligations. If there are
two molts per year, one occurs before the
breeding season (pre-nuptial molt) and
the other before the following winter
(post-nuptial molt). Early spring molters
are often more productive in terms of eggs
laid than late spring molters (Voitkevich,
1966). A single annual molt usually occurs
after the breeding season, but may not
take place until later on in the winter.
The rock ptarmigan, Lagopus mutus, undergoes four molts in a year which result
in plumages differing both in structure and
color (Salomonsen, 1939).
The annual cycle itself is coordinated
with environmental conditions, particularly those prevailing during the breeding
and immediate post-breeding season. Molting follows the same general patterns as
breeding with respect to latitudinal differences. Both tend to be shorter and more
accurately timed at high latitudes than
nearer the equator, but equatorial forms
unquestionably do follow seasonal cycles
rather than breed and molt continuously
or erratically (Ward, 1969).
Seasonal cycles in tropical birds are
related to the availability of food for shortand long-term energy requirements, and
food sources themselves follow a seasonal
pattern of abundance. Food is thus a proximate and ultimate factor in the annual
cycle of, for example, the yellow-vented
bulbul, Pycnonotus goiavier, in which protein sources, protein levels, breeding, and
molting are closely related (Ward, 1969).
Miller (1961) correlated the two semiannual molts in equatorial South American sparrows, Zonotrichia capensis, with
rainfall which effects the foraging of this
species in grass. The cessation of heavy
rain appears to trigger the commencement
of molt with which is associated a resumption of feeding. A later study of this same
species by Davis (1971) indicated that
food was probably the most important
proximate factor and rainfall and photoperiod were unimportant in timing the annual cycle. Reproduction and molting
were mutually exclusive without exception
in females and also to a great extent in
males. Sea birds breeding on the Galapagos Islands demonstrate a variety of seasonal cycles. Some have precisely fixed annual cycles while others breed throughout
the year but have breeding peaks at less
than annual intervals. The latter appear to
VERTEBRATE MOLTING CYCLES
stop breeding only to molt the wing and
tail feathers. Only one species is known to
molt and breed concurrently. Food supplies are fairly constant throughout the
year, but those forms with a regular annual cycle which feed away from the islands
may encounter seasonally fluctuating food
supplies that could act as a proximate
(and ultimate) factor (Harris, 1969).
Evans (1966), in dealing specifically and
comprehensively with the lesser redpoll,
Carduelis flammea, reached several conclusions which may apply generally to temperate species which undergo migrations of
lesser magnitude than Arctic breeders and
whose seasonal cycles are also somewhat
less rigorous. Molting does not overlap
breeding functions which are carried out
by both sexes so that their molts begin
simultaneously. Redpolls migrate as soon
as, but usually not before, the molt concludes. Whereas these birds may raise two
broods in temperate latitudes before the
molt, in higher latitudes only one brood is
raised, and moreover, the post-nuptial
molt (at least in males) is slightly faster.
Pitelka (1958) reported a similar finding
for Steller's jays in America. There is a
general decrease in body weight during the
early part of the molt followed by an
increase in the final stages due to several
possible causes: (1) The new plumage will
be slightly heavier than the old; (2) birds
will resume active feeding; and (3) premigratory fat deposits may be laid down.
That the molt is physiologically a most
demanding process is indicated by its noncoincidence with other phases of the annual cycle and direct demands in terms of
energy resources.
In the case of migratory birds which
breed in the Arctic and overwinter farther
south, the young tend to be precocial at
hatching; they grow quickly and the fledging plumage also develops speedily in time
for the autumn migration. The adult
molt often begins before the breeding season is over, certainly before the gonads
regress, and different molt stages may be
compressed into one another. The energy
cost of the rapid molt is offset by the brief
87
abundance of food and the virtual absence
of predators, so that maximal growth and
development can be sustained. Molting
may continue during slow phases of migration, but will be suspended during rapid migrations (Holmes, 1966i>).
Chicks of the two high Antarctic species
of penguins, the emperor (Aptenodytes
jorsteri) and Adelie (Pygoscelis adeliae),
molt precociously contining to grow and
develop independently in the late summer
and allowing their parents time to complete a post-nuptial molt while food is
still plentiful. Subantarctic king penguin
(Aplenodytes patngonira) chicks reared
through the winter are also ready for the
sea in early summer, giving time for their
parents to molt and produce a late chick
before winter. The subantarctic cool temperate little blue (Eudyptula minor), yellow-eyed (Megadyptes antipodes), and
rockhopper (Endyptes crcstatus) penguins
l'aise their chicks to full weight before
starting their own post-nuptial molt
(Stonehouse, 1970). Early synchronized
breeding in the Antarctic fulmarine petrels, Daption, and Pagodroma, allows time
for a complete molt in the breeding area
before food becomes scarce in autumn.
Wing molt in unsuccessful breeders begins
before that of successful breeders. The
smaller crevice-nesting species of Pachypti}(i, Fregctta, and Occaniles follow a less
synchronized breeding pattern. Molt takes
place on the wintering grounds, because
time is too short and food insufficient at or
near the breeding colonies (Beck, 1970).
The relationships of reproduction and
molting to the annual cycle in mammals
has been discussed recently in some detail
(Ling, 1969, 1970). There is little further
to add here beyond reiterating that, generally speaking, molts from winter to summer pelage can usually proceed almost regardless of reproductive condition, but the
autumn molt to winter pelage involving
the growth of a heavier coat does not, and
probably cannot, take place, except during anestrus. Aquatic rodents, such as beaver and muskrat which undergo almost
continuous pelage replacement, suspend
JOHN K. LING
molting at the peak of the breeding season
in April-May, so that hair growth must be
suppressed shortly before this time. Other
aquatic mammals such as seals molt annually sooner or later after the breeding season, an exception being the subtropical
Hawaiian monk seal, Monachus schauinslandi, in which breeding and molting
overlap. Spontaneous hair growth occurs
in regular (3 to 4 weeks) waves in nonbreeding laboratory rats and mice, but is
suppressed by pregnancy (Mohn, 1958).
Wild terrestrial rodents have regular seasonal molts outside the breeding period. In
mammals which carry an unimplanted
blastocyst for some time after the annual
mating season, autumn pelage growth and
molting proceed during the free blastocyst
phase of the reproductive cycle. The
spring molt, however, occurs during the
early stages of estrus or even pregnancy.
Since the primary function of pelage is
thennoregulation — in terrestrial and amphibious mammals at least—pelage
changes may be expected to relate to seasonal environmental temperatures. While
molts may be stimulated by environmental
factors other than temperature, climate
must surely be involved in local control for
any survival values to be realized. Watson
(1963) has mentioned that hares at the
same latitudes in Baffin Island and Norway, which experience very rigorous Artie
conditions and a relatively mild climate
respectively, would be expected to molt at
different times (and rates). Flux (1970)
showed that Scottish mountain hares, Lejnts timidus scoticus, molted faster in a
cold year than in a milder one and their
coats were also whiter. Hares introduced
from Norway into the much milder Faroes
gradually eliminated the white color
phase over a period of 40 years (Salomonsen, 1939). Many northern terrestrial
mammals occuring over an extensive latitudinal range show a tendency towards
perennial whiteness at northerly extremes
and constant brownness at the southern
end of their distribution. Thus, %vhile temperature control is the ultimate factor in
pelage changes, temperature itself influ-
ences the progress of the molt in such a
way as to ensure maximum functional
efficiency of the fur. Pelage changes related
to roles other than thermoregulation,
such as providing a smooth outer body
surface in aquatic mammals, are geared to
the rest of the annual cycle rather than to
seasonal environmental conditions which
are relatively constant anyway. It would be
advantageous, however, for molts to be
rapid, whereas in the aquatic furbearers
whose pelage still has a thermoregulatory
role, as well as a streamlining function, the
speed of the molt would be related to
gradually changing temperatures and thus
itself be gradual.
Endocrines and Molting
Using the externally visible molt as an
index of response, numerous workers have
experimented with amphibians, reptiles,
birds, and mammals in attempts to relate
various endocrine states to molting. Since
the shedding process, whether it involves
the loss of skin, feathers, or hair, can be
quite precisely followed on the basis of a
sequence of appropriate stages, there has
been little attempt (or apparent need) to
correlate histological changes in the integument with hormonal status. Provided
the duration of the complete growth sequence is accurately known, microscopic
appearances are sufficient.
Such data are readily available for standard laboratory animals. We have a long
way to go, however, in establishing time
relations for skin cycles in wild animals.
Thus, the modus operandi of the many
individual and interacting hormones at
different stages of growth of the organism
as well as during integumentary cycles
must remain at best a matter of some
speculation. Nevertheless, a number of
schemes have been proposed which attempt
to explain the systems involved in vertebrate molting cycles. In developing these
models the authors (Ebling and Johnson,
1964; Jcirgensen and Larsen, 1961, 1964;
J(irgenscn et al., 196."); Ling, 1970; Maderson, Chiu, and Phillips, 1970; Voitkevich,
VERTEBRATE MOLTING CYCLES
1966) have thoroughly reviewed the effects
of the various endocrine organs on molt
in all but fish. It is therefore, appropriate
here only to seek an underlying pattern to
explain molting in the different vertebrate
classes.
Molting in urodeles, anurans, and squamate reptiles has long been thought to be
influenced by the thyroid gland under the
general control of the pituitary (e.g., see
Adams et al., 1932). J0rgensen and Larsen
(1961, 1964) and J0rgensen et al. (1965)
have proposed, however, that epidermal activity in amphibians follows an autonomous rhythm which is controlled by the
permissive action of the thyroid and
adrenocortical hormones beyond a critical
level in urodeles and anurans respectively.
Whereas epidermal proliferation is not
affected by the hypophysis, the shedding
process is, through the secretion of thyrotropic and adrenocorticotropic hormones.
The shedding cycles of the few squamate
reptiles investigated so far do not appear
to be affected by gonadotropins or sex hormones. Presently available data (Maderson, Chiu, and Phillips, 1970) suggest the
pituitary-thyroid complex as being the
most likely endocrine system involved in
the squamate molt, with prolactin possibility acting synergistically. ACTH appears to
suppress molting in both intact and thyroidectomized reptiles, possibly through inhibition of renewed mitotic activity at the
onset of a new epidermal cycle. Thus, the
system is somewhat similar to that which
controls amphibian molts, although inhibition of the latter seems to operate at the
shedding stage, whereas in reptiles the proliferative phase is inhibited. Indeed, it
would appear that the resting stage may be
maintained under an inhibitory factor,
the precise nature of which is not yet determined. Furthermore, variations between
reptile taxa are also to be expected.
In view of the fact that avian molting is
closely related to feeding regimes, it is not
surprising to find the thyroid dominant in
the control of plumage cycles. Voitkevich
(1966) devotes a considerable portion of
his extensive monograph to a detailed an-
89
alysis of the role of the thyroid and other
endocrine glands in avian molts. There is a
very close relationship between feather
formation, pattern, color, growth, and thyroid activity — much closer than with the
gonads. However, Lofts and Murton
(1968), in a brief review of photoperiodism, endocrines, and molting, indicate
that thyroid and gonadal hormones may
interact synergistically in the regulation of
avian plumage cycles (see reptiles). The
initiation of feather anlagen is less under
hormonal control than later events which
ultimately are co-ordinated with respect to
the annual cycle. There is greater uniformity of action throughout this Class than
other vertebrates, so that simple generalizations are perhaps more valid. The thyroid may also mediate the adaptive responses to temperature, through metabolic adjustment, thereby to some extent controlling the rate of molting. After the initiation of feather growth, thyroidectomized
birds molt more quickly (Voitkevich,
1966), which may be indictive of the removal of thyroid control over what is basically in all vertebrates an inherent
rhythm. Voitkevich invoked functional exhaustion of the pituitary to explain the
adaptations of the body to successively alternating periods of light and darkness
during a day.
Endocrine status and pelage growth in
mammals probably involve a more complex interrelationship than that pertaining
to avian plumage cycles. In the latter the
thyroid plays a dominant role; in the
former it may function only permissively
or in association with the adrenals and
gonads, both of which have a generally
inhibiting effect on hair growth (Mohn,
1958; Ling, 1970). While the hair growth
responses to specific endocrine states are
themselves frequently quite specific, their
ecological significance and the physiological links thereto can still only be inferred.
For example, Ling (1970) suggests that
the possible influence of nutritional status
on pelage growth may be monitored either
through thyroid feedback or manifestations of stress affecting adrenal output or
90
JOHN K. LING
both. Such interacting systems have not
been investigated in wild mammals in
which a variety of subtle factors would be
expected to act anyway. Laboratory studies
would, if anything, reflect simplified situations; yet, they too have not been carried
out to the extent of providing clues of the
mechanisms involved. Much remains to be
investigated in this field. The following
model may be regarded as incorporating a
concensus of the roles of various physiological states in regulating hair growth. The
degree to which a particular state might be
expected to occur in nature obviously is
an unknown but important factor to bear
in mind.
Growth of new pelage is a metabolic
event of small or large proportions, depending ultimately on the amount of keratin required to be synthesized relative to
tne total metabolism of the animal. It,
therefore, is regulated by the thyroid gland
to the extent of complete control or merely
in a permissive role. Nutritional status, as
such, will influence the hair growth cycle
directly or indirectly through the thyroid
system as a feedback mechanism. To the
extent that nutritional status may engender a state of stress, this will be monitored
by way of the adrenals, the secretions of
which themselves influence epidermal cyclic activity. The role of the gonads in
regulating hair growth is by no means
clear-cut and may indeed be dependent
upon a synergistic or modifying effect of
other endocrine glands. This would be logical in view of the need to synchronize
events with respect to the reproductive cycle which may include protracted periods
of post-natal care. Thus, the ultimate factors are closely linked with the interacting
endocrine glands all of which are coordinated with respect to the season through
the hypothalamic—hypophyseal axis.
EVOLUTION AND ADAPTIVE FUNCTION
OF VF.RTEBRATE MOLTING
The evolution of vertebrate molting is
essentially the evolution of periodicity in
the functional role of the integument of
the different classes. An understanding,
therefore, of the structure and function of
the skin and its appendages may very well
help to elucidate the evolutionary role of
the periodic changes therein. Molting concerns chiefly the ep< 'nis and its deriva;les appear to be a
tives and epidemic
basic vertebrate c acteristic; the structural changes follow similar patterns in all
vertebrates. Epidermal generations occurring in the New Zealand rhynchocephalian
tuatara lizard (Sphenodon punctatus),
for example, resemble closely those of
modern squamate reptiles. Skin shedding
in the latter would thus appear to follow a
very ancient course, unique, however, to
the subclass Lepidosauria (Maderson,
1968).
An inherent epidermal cycle, giving rise
to outer generations of epidermis per se or
derivatives (scales, feathers, hairs), need
only be synchronized with respect to environmental conditions for the integument
to achieve great survival value. A simple
rhythm in a highly versatile organ provides
an ideal point about which to adjust to
functional demands.
Unlike the rigid exoskeleton of many
invertebrates which must be shed periodically to allow for increased size, the vertebrate integument is more pliable and
there is no real evidence to suggest that
the shedding cycles in lower groups are
related to growth. Moreover, it has been
observed in some amphibians and reptiles
that distention of the body after a large
meal causes neither splitting of the skin
nor molting. Many of these forms, however, do shed their entire outer epidermis in
one sheet which must therefore involve local or systemic factors in synchronizing epidermal activity over the whole animal. In
contrast to this inductive mechanism, a
permissive action of the stimulatory (or
anti-inhibitory) factors is all that is required in continuous desquamation of
small fragments of skin. Certainly the evolution of keratin was not necessary to the
advent of periodic molting.
The functional roles of piscine, amphibian, and reptilian skin lie in the entire
VERTEBRATE MOLTING CYCLES
f
organ. These functions include slime production, respiration, and osmotic control
(including prevention of desiccation). It is
not known what role is played by the
molt observed in Agriopus, apart from replacement of we* '^ut structures. The
same may hold trux >•» skin shedding and
replacement in tht- more terrestrially
adapted amphibia and the reptiles in
which, however, wear and tear would not
seem to be a major problem. The fact that
many sloughs are eaten, particularly by
smaller animals which undergo a molt,
suggests that ecdysis may indeed be a demanding process in terms of metabolic materials, some of which may be recycled
from the injested slough. In truth, we do
not really know what functions are
fulfilled by epidermal cycles in lower vertebrates, but for such an ancient process to
persist, it would be presumed to serve an
important biological need. So far, the identity of this need has eluded us.
The origins of feathers and hairs as true
epidermal derivatives have been briefly
discussed elsewhere (Parkes, 1966; Ling,
1970). It is very probable that these structures are excellent examples of preadaptation — a term principally applied to single
organs originally evolved for one specific
biological role but which were present,
available, and suited to perform quite a
different role when the "need" arose.
Proavian and promammalian reptiles very
likely were capable of at least limited temperature control, and early birds and
mammals had undoubtedly developed even
more efficient mechanisms for thermoregulation. That feathers evolved as adjuncts to
flying (which was preceded by running,
hopping, and gliding) seems most likely on
the basis of comparative anatomy, embryology, and physiology. With increasing size
and relative fragility of feathers, however,
wear and tear would indeed become a
serious factor in survival and replacement of worn out plumage a necessity of
life. The basic anatomical and physiological groundwork for individual feather replacement had of course, been laid down
in the proavian reptiles whose closest liv-
91
ing relatives are the crocodilians which
also replace the outer layers of their scales
individually. It certainly appears that individual replacement of feathers had already
evolved in Archaeopteryx, because in one
of the fossil specimens, the first (innermost) primary of each wing seems to have
been growing (Parkes, 1966). The variety
of form and function of feathers in modern birds reflects postadaptive morphological and physiological features which are
related to the many biological roles now
performed by specialized plumage.
Hairs were preadapted to a mechanicosensory role in promammalian reptiles and
early mammals. Today, they still perform
this function to a greater or less degree,
with some specialized areas having specifically sensory fibers (Ling, 1970). The development of a sufficiently abundant hair
follicle population by various devices —
branching and multiplication — was also
made possible in the mammalian ancestors
through the "basic" trio group to which
almost all follicle groupings in modern
mammals may be related (Lyne, 1966).
The functional value of plumage and
pelage is principally related to the collective biology of the individual feathers and
hairs. The fact that these structures do act
in an individual capacity, however, is also
vital if seasonal needs are to be met. It is,
for example, the switching on and off of
activity in separate follicles which determines the speed, topographical sequence,
and extent of each molt. Provided the potential for epidermal activity required for
feather and hair growth is there, mechanisms need only be evolved to synchronize
such switching on and off according to environmental demands. That such mechanisms also are a basic part of the vertebrate
make-up is clearly apparent from very rapid adjustments in plumage and pelage cycles under short-term field and laboratory
experimental regimes, as well as differences
observed over the geographic range of a
species. The synchronizing system consists
of the neuro-humoral complex acting
through exteroceptor-hypothalamic-hypophyseal pathways to individual endocrine
92
JOHN K. LING
organs which control the continuous metabolic and periodic breeding functions inherent in all vertebrates. These regulatory
systems too are basically alike in all five
Classes.
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