AMER. ZOOL., 25:955-964 (1985)
Periods of Nutritional Stress in the Annual Cycles of Endotherms:
Fact or Fiction?1
JAMES R. KING AND MARY E. MURPHY
Department of Zoology, Washington State University,
Pullman, Washington 99164-4220
SYNOPSIS. An animal's nutritional status depends on (1) nutrient accessibility, (2) nutrient
demand, and (3) physiological, metabolic, morphological, and behavioral compensations
that avert or minimize discrepancies, if any, between the first two. The main thesis of this
essay is that the diversity and potency of such compensatory mechanisms have often been
underrated, and hence the frequency and intensity of nutritional stress in free-living
animals have often been exaggerated. This theme is explored in conjunction with an inventory of the modes of compensation for actual or potential dietary deficiencies.
INTRODUCTION
ticism. In particular, we are skeptical about
two attitudes.
First, in spite of recent advances in nutritional ecology, the viewpoint seems to
remain widespread in certain circles that
the attainment of adequate nutrition by
endotherms in nature is a relentless challenge. For instance, this viewpoint surfaces
as an assumption in recent theories of competition, optimal foraging, and space or
resource defense, and is also often invoked
to explain periodic shifts in body mass or
composition of animals. The prevalence of
such a viewpoint is an enigma if we stop to
consider how little we know of the nutrient
requirements of free-living endotherms. It
seems to us that it is unjustified to assume,
and even more so to conclude, that there
is "not enough" when "enough" has not
been defined.
The second commonplace attitude (a
corollary of the first) that warrants skepticism is that the annual cycle of endotherms necessarily includes periods of nutritional stress. Because processes such as
molt, reproduction, or winter thermoregulation each involve a "price" that is presumably added to the maintenance
requirement, these periods of the annual
cycle have often been singled out as nutritional bottlenecks (times when malnutrition is most likely to take its toll). This line
of reasoning is qualitatively sound as far as
it goes, but is ultimately ambiguous. An
increased nutrient requirement is a burden
1
From the Symposium on Animal Energetics: to an animal only if the animal is already
Amphibians, Reptiles, and Birds presented at the Annual exploiting its environment fully to support
Meeting of the American Society of Zoologists, 27—
maintenance functions alone. Otherwise,
30 December 1983, at Philadelphia, Pennsylvania.
The subtitle of this essay, "fact or fiction," might just as well have been "fact
and fiction." It is known from sound evidence that endotherms sometimes die or
fail to reproduce because of starvation or
hypothermia. That is a fact. There is an
ample literature of such accounts, most of
it anecdotal and some of it dramatic (e.g.,
Gessaman and Worthen, 1982). The summary of a typical publication might be: "I
toured the woods after a bad snowstorm
and found many dead birds and some deer
that seemed very weak." Most reports are
more thorough than this rhetorical example, but all fall into one category: positive
evidence of episodic death or debilitation,
sometimes as a result of malnutrition. The
countering evidence, since it is negative, is
rarely published. One can easily imagine
the reaction of a journal editor to a manuscript whose summary might be: "I toured
the woods after a bad snowstorm and did
not find any dead birds or scrawny deer."
It is, of course, the positive evidence that
lingers in mind and comes to dominate our
impressions. The negative evidence is
neglected. As a result, we feel that some
questionable perspectives and a few outright mistakes (the "fiction" of our subtitle) have persisted in nutritional ecology
for an uncommonly long period of time,
and should be subjected to a bit of skep-
955
956
J. R. KING AND M. E. MURPHY
there is some buffer in nutrient supply to
support production and other demands
above the maintenance level. Furthermore, the extent of this buffer depends not
only on the difference between an animal's
maintenance requirement and nutrient
supply, but also on the animals's metabolic
and behavioral plasticity.
In actuality, the viewpoint that nutritional poverty is imminent in the lives of
endotherms springs more from deductive
reasoning than from empirical facts. It
seems to us that, in most cases, there are
but two incontrovertible facts about the
connection between animal welfare, animal numbers, and nutrient supply. First,
animal numbers do not increase indefinitely. Something counteracts the inherent
growth of populations. Second, animals
sometimes die of starvation or fail to reproduce because they are malnourished. From
these two facts it follows only that food supply is a plausible limiting factor (and probably the ultimate limiting factor) in the
absence of other constraints. It seems,
however, that the maxim that food supply
is the ultimate regulator of animal numbers in the theoretical sense has been translated into the non sequitur that food supply
must also be the prepotent proximate regulator. Put another way, this reasoning
implies that because animal populations are
regulated somehow, there must be a lot of
malnourished animals. The prevalence of
such deductions has biased our viewpoints
for a long time, and alternative viewpoints
from multiple sources have only recently
begun to surface. In the examples that follow we attempt to illustrate that the animals themselves are telling us that they are
not the victims of chronic or recurrent
nutritional poverty.
ELEMENTS OF ADJUSTMENT TO VARIABLE
NUTRIENT AVAILABILITY
Unlike their domesticated counterparts,
free-living animals typically confront a
dynamic profile of nutrient accessibility in
terms of both quality and quantity.
Although, in the minds of many, this fact
may immediately conjure up visions of periodic malnutrition, at least two distinct
advantages are associated with such variability. First, variability of food types provides options for selective feeding and
dietary complementation that enable an
animal to "formulate" nutritionally adequate whole diets from a variety of individually subadequate food types (Thompson, 1982, p. 18). Secondly, the dynamic
profile of nutrient accessibility through
time may include periods of surfeit nutrition when an animal can accumulate
nutrient reserves. These reserves can later
be mobilized either to complement or to
substitute for dietary input when food is
short (see beyond). In the first case, an animal's vital functions are supported and
protected by exogenous/exogenous
nutrient complementation, while the second case involves exogenous/endogenous
complementation. The continuous exogenous supply of all essential nutrients to an
animal is the most obvious case of adequate
nutrition, and may in fact describe the rule
in nature. It is less obvious that transient
reliance on stored nutrients or recruitment
of alternative compensatory mechanisms
when exogenous nutrients are scarce can
likewise result in adequate nutrition.
In evaluating the nutritional status of
free-living endotherms we have chosen to
concentrate on examples in which animals
use compensatory mechanisms to adjust to
variable nutrient accessibility. It is these
episodes that are most likely to be misdiagnosed as malnutrition or nutritional
stress.
Compensatory mechanisms
Nutritional limitations may result from
a direct scarcity of food in terms of either
quantity or quality, or from an indirect
scarcity. Indirect scarcity results from the
resolution of competing demands {e.g.,
defense against predators, courtship, incubation, sheltering against bad weather) that
subtract from the time available for foraging. Furthermore, scarcity may be either
episodic and unpredictable or regularly
recurring, as on a seasonal basis. The
potential interactions of these sources of
variability in nutrient supply provide a rich
matrix for the diversification of compensatory mechanisms that buffer animals
NUTRITIONAL ECOLOGY OF ENDOTHERMS
against either direct or indirect privation.
The efficacy of such compensations in forestalling nutritional stress until conditions
improve defines an animal's zone of tolerance. In general, compensatory mechanisms include (1) building and drawing on
nutrient reserves, (2) reducing or reallocating nutrient expenditures, and (3) combinations of the two.
Nutrient reserves
Surplus nutrients may be accumulated
either as food (exogenous reserves) or its
metabolites (endogenous reserves). The
storage of surplus food in caches is perhaps
the exception rather than the rule among
endotherms, but is nevertheless widespread among both mammals (Hamilton,
1939) and birds (Calder and King, 1974).
Both carnivores and herbivores cache food,
but the habit is understandably more common among the latter. Food hoarding is
most highly developed in small-bodied nonhibernating or non-migratory herbivores
(e.g., beavers and smaller) and in many cases
is crucial to overwinter survival. For
instance, Haftorn (1956) estimated that as
much as 60% of the midwinter food supply
of Great Tits in Sweden is obtained from
hoards accumulated during the autumn.
On a briefer time-scale, food may be
retained or stored in the anterior parts of
the digestive tract as a reserve to aid overnight survival. This form of external storage is rare, but is an indispensable element
of the energy budget of several species of
boreal birds that possess capacious crops
or esophageal diverticula that they pack
with food before retiring at dusk to their
nighttime refuges (Calder and King, 1974).
Endogenous reserves may function to
buffer the results of a general food shortage, as in fasting, or shortages of specific
nutrients. The annual cycle of the Emperor
Penguin provides an extreme example of
reliance on endogenous reserves. These
birds feed only sporadically, and subsist
during long periods of fasting (1-4 months)
on reserves accumulated during their foraging cycles. Egg-laying, incubation, and
molt are all accompanied by absolute fasting during which endogenous reserves supply the full complement of energy and spe-
957
cific nutrients needed for self-maintenance
and production. The characteristics of
long-term fasting by penguins do not differ
in any conspicuous way from those of the
domestic goose (Le Maho, 1983), and are
probably an extreme exaggeration of ubiquitous metabolic capacities. Several species
of geese that nest in the Arctic rely on
endogenous reserves while fasting during
egg-laying and incubation (Ryder, 1970;
Ankney and Maclnnes, 1978; Raveling,
1979), and illustrate this point. Lactating
Gray Seals (Davies, 1949) and rutting Red
Deer (Mitchell et al., 1976) and Elephant
Seals (Bartholomew, 1952) also depend on
a tolerance of fasting to enable them to
carry out these reproductive activities. We
suggest that "fasting" be purged of
anthropocentric connotations and viewed
in an ecological context as not necessarily
a nutritional stress, but in many cases as a
tactic for averting stress in the face of competing demands for time or other resources.
The foregoing examples concerned generalized food shortage and the resultant
release from reserves of a profile of
nutrients that efficiently fulfills metabolic
requirements. Stores or reserves of specific
compounds are also evident in certain cases,
and can be drawn upon to counteract specific dietary deficiencies. There are examples from all of the major classes of
nutrients. The role of lipid storage in overnight energy homeostasis and as a buffer
against energy shortages during migration
or winter, for instance, is too well known
to merit discussion here (for review, see
Pond [1981], and several papers in the
symposium convened by Derickson [1976]).
Whether amino acids are stored as peptides
or proteins solely in anticipation of future
need is not clear. The annual cycles of protein mass that have been detected in various species (e.g., Ankney and Maclnnes,
1978; Raveling, 1979; Kendall etal, 1973)
may, in fact, be the result of selection for
maximum protein reserves in times of
potential need, akin to the better-known
cycles of fat storage. However, the ebb and
flow of protein mass is also related to use/
disuse and attendant hypertrophy/atrophy, and so it is difficult to distinguish proximate and ultimate causes. Regardless of
958
J. R. KING AND M. E. MURPHY
the impetus for protein accretion, it is well
documented that amino acids can be withdrawn from muscle protein (Fisher, 1967;
Swick and Benevenga, 1977) or from peptides such as glutathione (Tateishi et al.,
1977) or carnosine (Baker, 1977) for use
elsewhere in the body.
Relatively little is known about specific
storage of vitamins and minerals, but it is
nevertheless clear that the body contains
reserves of many such nutrients. Fat-soluble vitamins accumulate in adipocytes and
are liberated during lipolysis. At least certain water-soluble vitamins accumulate in
hepatocytes, and presumably can be withdrawn when need exceeds dietary income
(Kodicek, 1954). Among the minerals, bone
as a reserve of calcium is the most thoroughly studied example; but whether bone
can function also as a selective reserve of
other minerals is still controversial (Murray and Messer, 1981; Tao et al., 1983).
Various chelates of minerals, such as zincmetallothionein complexes (Whanger etal.,
1981), potentially also function as stores or
reserves of certain minerals.
Our ignorance of the nutritional programs and capacities of free-living animals
in all but a handful of cases has obliged us
to rely thus far on studies of domestic animals when trying to understand the significance of nutrient reserves in natural
settings. We are fearful that this may leave
us with a myopic view of the role of nutrient
reserves in wild animals. In the first place,
practical nutritionists have no commercial
reason to search for nutrient reserves, and
so may have overlooked them. In the second place, nutritionists typically study
domestic animals, in which selection for
nutrient reserves has been relaxed if not
absent for untold generations.
Nutritional economies
For convenience, we have summarized
the mechanisms by which animals minimize nutrient expenditures in the categories of adult self-maintenance and
production, respectively, with the understanding that these categories often overlap and interact. Economies in self-maintenance involve hypothermia, adaptive
reduction of body mass, and various kinds
of behavioral adjustments.
Regulated reductions of body temperature may be mild, as in day-to-day torpor
in birds and mammals, or may be profound, as in mammalian hibernation or
aestivation. Although adaptive hypothermia has usually been regarded as mainly
an energy-sparing mechanism, it also slows
the depletion of any kind of nutrient
reserve. Seasonal hibernation is dependent
on an endogenous rhythm in at least some
species of mammals, and thus reflects the
evolution of a regulatory system that anticipates the recurrence of intolerable seasons. Daily torpor, in contrast, is most commonly linked to immediate shortages of
food (Calder and King, 1974; Hudson,
1978). Energy economies can be impressive, for instance amounting to an average
reduction of 88% relative to the euthermic
metabolic rate in Richardson's Ground
Squirrel during hibernation (Wang, 1978).
Substantial metabolic economy results also
from shallower nighttime (or daytime) torpor {e.g., Tucker, 1965; Chaplin, 1974).
Even small tropical birds, apparently in
response to sporadic food shortages, accrue
noteworthy savings (58%) by hypothermia
through a 12-hr night (Bartholomew et al.,
1983).
Reductions of body mass by wild animals
have typically been interpreted as a loss of
"condition" in response to environmental
stress. Recently, however, several investigators have delineated cases in which loss
of body mass is voluntary, beneficial, and
perhaps an expression of adaptive anorexia
(Mrosovsky and Sherry, 1980). We have
already mentioned the astonishing performance of Emperor Penguins, which make
themselves independent of a remote food
supply by long-term fasting. Other animals
undergo periodic mass losses even when
food is freely available—for instance, overwintering deer (Wood et al., 1962; Silver
etal., 1969)orducks(Reinecke^a/., 1982),
incubating birds (Sherry et al., 1980), birds
feeding nestlings (Freed, 1981), and birds
initiating the annual molt (Chilgren, 1977;
Murphy and King, 1984). In the cases just
cited, it is clear that mass loss is an innately
programmed process that will occur even
NUTRITIONAL ECOLOGY OF ENDOTHERMS
in captives with easy access to food. The
evolutionary impetus for adaptive anorexias and attendant loss of body mass no doubt
has differed among species and phases of
the annual cycle. Freed (1981) suggested
that mass loss reduces wing-loading and the
costs of flying (by an estimated 23%) in
small birds that are foraging to feed nestlings. Sherry et al. (1980) thought that it
allows better nest attentiveness during
incubation. Loss of body mass in wintering
deer and ducks is thought to reduce energy
demands both in transporting the body and
in maintaining it. Pre-molt body-mass loss
in birds may be an adjustment that reduces
wing-loading and the hazard of damage to
regenerating remiges.
Behavioral adjustments to nutritional
challenge are probably far more common
and important than we currently perceive,
and occur as genotypic adaptations of life
style as well as phenotypic adjustments to
day-by-day exigencies. As shown by the
sample of activity budgets assembled by
Herbers (1981), many species of birds and
mammals spend the large majority of their
daily activity periods "resting," and a much
smaller proportion in foraging. Ettinger
and King (1980) also highlighted this phenomenon, and proposed that the ostensibly
idle time in the daily routine served as a
buffer against unpredictable episodes of
energy shortage, or other stresses that
affect nutrient budgets indirectly. Herbers
called this inactivity "laziness," and Ettinger and King called it "loafing." Both terms
are anthropomorphic and should be
replaced by a neutral descriptor. "Idleness" might suffice until a better term surfaces. The origin and meaning of idleness
in activity budgets merits much more
debate than we can afford in this essay. The
simplest of the alternative hypotheses (and
hence the one favored by the rule of parsimony) is that endotherms can afford idleness because they are not usually confronted by food shortage, or that idleness
reflects satiety.
Proximate adjustments of the activity
budgets and other kinds of facultative
behavioral compensations are also known.
Two examples will have to suffice. Many
species of birds sharply curtail locomotor
959
activity during the annual molt (see King
[1980] for review). Although this "conservation of movement" undoubtedly results
in a reduction of energy expenditure in
this category of the budget, it is not at all
clear whether the impetus for the reduction is to compensate for the energy costs
of molt (as is commonly assumed), or to
minimize damage to regenerating feathers, or simply a reflection of impaired ability to fly.
Many kinds of voluntary behaviors are
known that alleviate heat or cold stress
(Cabanac, 1979). Perhaps one of the most
spectacular examples of this is the huddling of Emperor Penguins during their
periods of fasting during the antarctic winter. Le Maho et al. (1976) estimated that
these birds would not be able to balance
their heat budget unless they huddled
together.
Finally, nutrient economies accrue from
improvements in the efficiency with which
nutrients are utilized. Improved efficiency
can result from decreased excretion or oxidation of a substrate, or from enhanced
digestion, transport, or assimilation. The
ability of rabbits and macropods to subsist
in sodium-poor montane regions of Australia depends on the capacity of these animals to minimize sodium excretion in the
urine, feces, and saliva, and to exploit a
specific sodium appetite (Blair-West et al.,
1968). Winter-dormant black bears, by
means of shifts of protein kinetics that favor
the re-utilization of amino acids, maintain
a stable lean body mass in spite of a 1525% decrease of total body mass during
the winter (Lundberg et al., 1976). Shifts
of gut morphology and presumably the
efficiency of digestion and absorption are
often correlated with shifts of food types
or with stages of the annual cycle (Sibly,
1981). Finally, it is often argued that the
heat increments of feeding and of locomotion can substitute for thermostatic heat
production in the cold, but the subject is
controversial (Paladino and King, 1984).
In sum, there are many options for the
frugal use of nutrients. Some of them offer
only small advantages, but it is through the
summation of small advantages that selection leads to successful organisms.
960
J. R. KING AND M. E. MURPHY
Productive processes
By "production" we mean recrudescence of reproductive organs, formation of
gametes, pregnancy, lactation and the
analogous esophageal secretions of birds,
postnatal growth, and the replacement of
the integument during molt. The formation of storage products, such as fat, and
special phases of external work, as in
migration, are also productive processes in
the formal sense, but have relatively nonspecific nutrient demands {i.e., any energyyielding substrate).
Because the costs of production are
added to the costs of self-maintenance,
periods of production are commonly
regarded as "bottlenecks" in the annual
cycle. We think that this viewpoint exaggerates the average case, even though it
may be true in the extreme. We have
already reviewed many of the adjustments
that an animal can deploy in coping with
the added costs of production (e.g., partial
or complete reliance on reserves, various
economies in maintenance costs), and so
we concentrate attention here on the ways
in which production itself can be adjusted
to conform with limitations of nutrient
supply. A general point is germane, however, before we begin this inventory. An
increase of food requirements, as may occur
during production, is typically viewed as
an ecological burden, but nevertheless
entrains compensating advantages. The
increased food intake associated with
increased energy demands automatically
results in an increased supply of all nutrients
(Thompson and Boag, 1976; Murphy and
King, 1984). This means that the specific
nutrient requirements of either maintenance or production can be satisfied with
foods of lower quality when energy flow
through the organism is high. In the case
of production alone, it is the ratio of the
increments of energy and specific nutrients
that will determine the variety or quality
of foods that will sustain production.
The ways in which animals can avert or
reduce the strains of production include
seasonal programs that minimize the overlap of nutritionally demanding events or
permit storage in one season in preparation for a later event, compensating reductions in the units of production (eggs,
fetuses) or in the rate of production (molt,
lactation, growth), or in extremis the suspension or deletion of production.
The idea that selection has programmed
the annual cycle of animals so as to avert
or minimize the overlap of nutritionally
expensive events has been repeated so often
as to seem a truism. Such non-overlap does
indeed minimize per diem nutrient
demands, but this interpretation has then
been transmuted rather often into the
viewpoint that each event is itself stressful
or imminently so. We hesitate to invoke
nutritional selection pressures as the only,
or even most important, factors that have
guided the evolution of annual cycle patterns in endotherms. There are alternative
hypotheses that are no more speculative
than the nutrient-limitation hypothesis. It
is equally likely, for instance, that molt is
relegated to a phase of the annual cycle in
which flying time can be minimized so as
to reduce damage to soft, regenerating
feathers. In short, we think that the typical
annual cycle, with its segregation of events,
is the result of selection for a life-history
program that averts or at least minimizes
the various strains of competing processes.
Whether any given phase of the annual
cycle is itself potentially stressful in nutritional terms is a separate question that in
most cases still needs an empirical answer.
Some of the options for nutritional compromises when production and self-maintenance compete for limited substrates have
already been described in relation to
adjustment of patterns of self-maintenance. Additional options involve adjustments of production itself. Some of these
are unit reductions, as in clutch size (e.g.,
Bengston, 1971; Jones and Ward, 1976;
Ankney and Maclnnes, 1978), or number
of concepta (Cheatum, 1947; Bodenheimer, 1949; Huey, 1956; Viljoen, 1981;
Thomas, 1982). Others involve the slowing of processes that are not susceptible to
unit reductions, such as growth (Ricklefs,
1983), molt (French et ai, 1956;Ling, 1970;
Kendeigh [in Tollefson, 1982]; M. E. Mur-
NUTRITIONAL ECOLOGY OF ENDOTHERMS
phy, unpublished data), lactation (Rook and
Witter, 1968; Widdowson and Cowen,
1972), and gestation (Racey, 1981).
Deletion or cessation of production is the
ultimate response to food shortage when
an animal's compensatory options have
been used up. It appears that the endocrine
system of endotherms has been programmed to suspend reproductive processes before affecting production for selfmaintenance, as would be advantageous for
iteroparous animals. Mulinos and Pomrantz (1940) described the prompt endocrine responses leading to reproductive
failure in malnourished animals as "pseudohypophysectomy." We suppose that this
mechanism improves adult survival and the
opportunity for future reproduction.
Production for self-maintenance appears
to be much more resistant to malnutrition
than does reproduction. It is well known
that somatic growth slows but nevertheless
continues in malnourished subadults. Less
is known about the responses of molt to
malnutrition. Mammals may delay and prolong the molt and produce rough coats
(Ling, 1970) when on restricted diets, but
evidently continue to molt. Molt in House
Sparrows fed a diet containing 9% protein
was described as "normal," but was prolonged and of lesser intensity in other
House Sparrows fed diets containing 3%
protein, and "intermediate" when the diet
contained 5% protein. There were no consistent differences of body mass or energy
metabolism among the groups (Kendeigh
[in Tollefson, 1982]). Exploratory experiments (unpublished) in our laboratory have
shown that severe food restriction (75 and
50% of ad libitum intake) or nutrient deficiencies (a valine-free diet) reduce body
mass to near-lethal levels and proportionately reduce the rate of feather growth in
White-crowned Sparrows, but do not stop
feather growth completely.
The ultimate significance of nutritional
compromises in self-maintenance and production resides in the ways in which these
adjustments are translated into inclusive
fitness. This is an intricate topic in the realm
of evolutionary ecology that is beyond the
scope of this essay. Nevertheless, we hope
961
that we have succeeded, in this necessarily
brief account, in casting some perspectives
and unearthing some evidence that will help
biologists to view old subjects in new ways.
It seems obvious now that an animal's
nutritional status can be properly evaluated only in the context of its own lifehistory pattern, with attention paid not only
to nutritional requirements and accessibility, but also to the repertoire of adjustments available to the animal to avert or
minimize discrepancies between the two.
It is this integrated viewpoint that is the
essence of nutritional ecology.
APPENDIX
There are three terms used in the foregoing essay that we find troublesome
because they have been used by various
authors in diverse ways, and often without
being defined at all. We believe that it is
important to state the definitions that we
implied in our essay, but our intramural
referees objected that a glossary interrupted the flow of logic when included in
the text. Hence, we relegated it to this
Appendix.
Nutritional stress
Discordant usages of the word "stress"
(Franz, 1981) have rendered this descriptor nearly meaningless in the sense that the
prospects for a standard definition seem
forlorn. Nevertheless, it also seems unlikely
that the term will be abandoned, and so
we must attempt to cope with it. For use
in nutritional ecology, we borrow, with
certain modifications (italicized), Ankney's
definition (1979): " . . . a situation in which
[an animal's] nutrient demands exceed its
nutrient ingestion, resulting in net catabolism in body tissues to the extent that one or
more vital physiologicalfunctions are impaired."
Any depletion of reserves short of this
result does not reflect "stress" in our lexicon, but merely the functioning of an animal within its limits of tolerance.
Nutrient stores
Storage means the accumulation in the
body, in anticipation of a future need, of
any nutrient for which there is no imme-
962
J. R. KING AND M. E. MURPHY
thermia in two tropical passerine frugivores,
diate metabolic demand (Pond, 1981). GlyManacus vitellinus and Pipra mentalis. Physiol. Zool.
cogen storage and triglyceride storage are
56:370-379.
the most obvious examples, and the accu- Bengston,
S. A. 1971. Variations in clutch-size in
mulation of calcium in the medullary bone
ducks in relation to the food supply. Ibis 113:
523-526.
of female birds shortly before egg-laying
Blair-West, J. R., J. P. Coghlan, D. A. Denton, J. F.
is another clear-cut case (Simkiss, 1975).
Nelson, E. Orchard, B. A. Scoggins, R. D. Wright,
K. Myers, and C. L. Junqueira. 1968. Physiological, morphological and behavioural adaptaReserves are compounds that are stored
tion to a sodium deficient environment by wild
native Australian and introduced species of aniin the aforementioned sense plus any other
mals. Nature (London) 217:922-928.
tissue components that can be drawn upon
Bodenheimer,
F. S. 1949. Problems of vole poputo forestall stress, but are not otherwise
lations in the Middle East. Report on the popudemonstrably accumulated for the purpose
lation dynamics of the Levant vole (Microtus
of buffering potentially stressful condiguentheri D. and A.). Research Council of Israel,
Jerusalem. 77 pp.
tions. Examples include bone calcium that
is resorbed in the event of calcium priva- Cabanac, M. 1979. Le comportement thermoregulateur. J. Physiol. (Paris) 75:115-178.
tion (Simkiss, 1975), and muscle protein Calder,
W. A. a n d j . R. King. 1974. Thermal and
that serves as a supply of amino acids for
caloric relations of birds. In D. S. Farner and J.
both energy and synthesis of proteins
R. King (eds.), Avian biology, Vol. 4, pp. 259-413.
Academic Press, New York.
needed elsewhere. The distinction between
"stores" and "reserves" may seem trivial Chaplin, S. B. 1974. Daily energetics of the Blackcapped Chickadee, Parus atrtcapillus, in winter.
in analyzing proximate metabolic adjustJ. Comp. Physiol. 89:321-330.
ments, but is nevertheless crucial in under- Chilgren, J. D. 1977. Body composition of captive
standing the ultimate origin of these
White-crowned Sparrows during postnuptial molt.
Auk 94:677-688.
adjustments. Storage is the result of genotypic adaptation, but other categories of Cheatum, E. L. 1947. Whitetail fertility. N.Y. State
Conservationist 1:18-32.
reserves result from phenotypic plasticity. Davies,
J. L. 1949. Observations on the gray seal
(Hahchoerus grypus). Proc. Zool. Soc. London 119:
673-692.
ACKNOWLEDGMENTS
W. K. 1976. Introduction to the symThis essay is a by-product of investiga- Derickson,
posium: Lipids in animal life histories. Amer. Zool.
tions supported by the National Sci16:629-630.
ence Foundation (DEB 8116206, DEB Ettinger, A.O. andj. R. King. 1980. Time and energy
budgets of the Willow Flycatcher (Empidonax
8207511). We thank J. N. Thompson and
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