Design, limitations and sustained metabolic rate: lessons from small mammals
Centro de Estudias Avanzados en Ecologa & Biodiversidad and Departamento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, CP 6513677, Santiago, Chile
* Author for correspondence (e-mail: lbacigal{at}genes.bio.puc.cl)
Accepted 18 July 2002
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Summary |
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Key words: sustained metabolic rate, energy budget, physiological limit, central limitation, peripheral limitation, symmorphosis
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Introduction |
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Rates of energy expenditure sustained over longer periods are limited to a
lower level than rates of expenditure over shorter periods. In fact, SusMR are
almost fivefold lower than short-term (burst) expenditures, and they rarely
exceed the resting levels by sevenfold, in contrast to burst rates, which can
reach values 36 times above resting levels
(Bozinovic, 1992;
Bundle et al., 1999
). For small
mammals in particular, asymptotic ceilings on SusMR could limit individual
reproductive effort (since number and quality of offspring depends on milk
production and quality; Knight et al.,
1986
; Rogowitz and McClure,
1995
; Rogowitz,
1996
,
1998
), activity (i.e.
foraging, escape from predators), thermoregulatory capabilities and survival
to long-term cold exposure (Konarzewski and Diamond, 1994;
McDevitt and Speakman, 1994a
),
as well as geographic distributions and breeding ranges. This is because
ceilings on sustainable energy expenditure represent the upper limit for all
energy consuming activities performed by an individual. Given the ecological
and evolutionary consequences that sustained energy budgets have on many
aspects of animal life, it is important to determine which factors impose
ceilings on SusMR.
It has frequently been suggested that energy acquisition, transformation,
absorption, allocation and expenditure are intrinsically limited, and that
these intrinsic design constraints act before potential extrinsic limitations
such as food availability (Karasov,
1986; Wieser,
1991
; Stearns,
1992
; Weiner,
1992
; Speakman,
2000
). Drent and Daan
(1980
) suggested that a
`prudent parent' should not allocate more than four times its basal level of
energy expenditure to reproduction. Since this seminal work there have been
several studies of the design constraints on energy budgets (e.g.
Weiner, 1992
;
Speakman, 2000
). There are
three principal hypotheses to explain the physiological limitation on energy
budgets. (1) The `central limitation hypothesis', where the shared central
machinery limits SusMR; (2) the `peripheral limitation hypothesis', where the
energy-consuming machinery limits the SusMR; (3) symmorphosis (sensu
Taylor and Weibel, 1981
),
where the capacity of the central machinery closely matches that of the
peripheral tissues.
It should be noted that firstly, we are considering physiological
constraints and not restrictions imposed by the environmental food supply (see
Speakman, 2000). Secondly,
recognized authors in the field have already extensively reviewed the
hypotheses proposed (Peterson et al.,
1990
; Weiner,
1992
; Hammond and Diamond,
1997
; Speakman,
2000
), but we contend that particular assumptions, as well as
various empirical procedures used to identify the type of physiological
limitation, have not been completely correct. Consequently, it is not entirely
clear which factors impose metabolic ceilings in small mammals, precluding a
clear understanding of the ecological and evolutionary consequences of design
constraints on energy budgets. Thirdly, we will only discuss limits on SusMR,
not on sustained metabolic scope (SusMS) (i.e. potential trade-off aspects of
intake with future life history traits) (for a review, see
Speakman, 2000
).
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The central limitation hypothesis |
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Although there are different basic processes of central limitation
(Speakman, 2000), most authors
have suggested that the capacity of energy assimilation is the principal limit
for sustainable energy budgets (Weiner,
1992
). For small mammals, one way to confirm the presence of
metabolic ceilings, and at the same time to determine if they are centrally
limited, is provided by laboratory studies in which animals, fed ad
libitum, are forced to reach their maximal SusMRs under different modes
of energy expenditure (e.g. lactation, thermoregulation, activity). This
procedure tests whether the metabolic ceilings for each activity reach the
same value, as predicted by this hypothesis.
The main evidence for the proposal that energy budgets are centrally
limited is that the observed body-mass-independent linkage between resting and
sustained metabolic rates (RMR and SusMR, or Field Metabolic Rate) are not
linked to body mass (Drent and Daan,
1980; Kirkwood,
1983
; Weiner,
1989
; Speakman,
2000
). It is argued that animals with higher sustained energy
expenditures support their demand by increasing food consumption which, at the
same time, increases the mass of the central organs (i.e. liver, kidneys,
heart, lungs and small intestine). Given the high specific metabolism of these
organs and their direct contribution to the RMR
(Schmidt-Nielsen, 1995
), then
RMR and SusMR should increase jointly. There is abundant evidence of a
phenotypic linkage between both traits, but the data are controversial
(Koteja, 1987
,
1991
;
Nagy, 1987
;
Daan et al., 1990
;
Peterson et al., 1990
;
Bryant and Tatner, 1991
;
Lindström and Kvist,
1995
; Ricklefs et al.,
1996
; Hammond and Diamond,
1997
; Speakman,
2000
). Furthermore, there is abundant evidence of phenotypic
flexibility in central organ mass, and the conclusions from these observations
are more generally agreed (Bozinovic et
al., 1990
; Daan et al.,
1990
; Hammond and Diamond,
1992
; Hammond et al.,
1994
; Konarzeswski and Diamond, 1994,
1995
;
Speakman and McQueenie, 1996
;
Derting and Austin, 1998
;
Konarzweski et al., 2000). It means that a high energy budget depends on
expensive metabolic machinery (Diamond,
1993
), which could explain why SusMR do not exceed RMR values by
more than sevenfold (Hammond and Diamond,
1992
).
Many studies have assessed the possible link between SusMR and RMR, and
demonstrated the important consequences of it
(Speakman, 2000). The
existence of such a link would provide a theoretical framework for
understanding variations in RMR among species, and also evidence to support
the `energy assimilation model' for the evolution of endothermy
(Koteja, 2000
), although it
would not disprove the aerobic capacity model
(Crompton et al., 1978
;
Bennet and Ruben, 1979
;
Bozinovic, 1992
;
Hayes and Garland, 1995
;
Ruben, 1995
). In addition, if
RMR and SusMR are indeed linked, one could argue that high RMR would allow
high SusMR, which could explain differences observed in activity patterns and
life history traits (McNab,
1980
; Hayssen,
1984
; Thompson and Nicoll,
1986
; Derting and McClure,
1989
; Harvey et al.,
1991
; Hayes et al.,
1992
; Thompson,
1992
; Koteja and Weiner,
1993
; Johnson et al.,
2001a
).
Finally, the central processing and transport organs may be able to supply energy and nutrients faster, the peripheral organs would not be able to convert this increased supply into work and heat at the same rate. SusMR would therefore be limited at the site of energy use (i.e. peripheral limitation).
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The peripheral limitation hypothesis |
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Peripheral organs and tissues may be limited by the rate at which ATP is
generated and mobilized at these sites
(Speakman, 2000). However, a
very important exception in mammals is the heat generated by non-shivering
thermogenesis in brown adipose tissue, which is one of the most important
mechanisms for thermogenesis in small mammals in seasonal habitats (e.g.
Heldmaier, 1993
; Merritt et
al., 2001). The peripheral limitation hypothesis predicts different metabolic
ceilings for different modes of energy expenditure. This is because limits are
set by the particular limitations of the tissues and organs using the energy,
whereas central organs have an excess capacity
(Hammond and Diamond, 1997
).
Thus, as for the central limitation hypothesis, a key approach to empirical
evaluation of peripheral limitations on SusMR is provided by laboratory
studies in which animals fed ad libitum are pushed to their maximal
SusMRs under different modes of high energy expenditure (e.g. lactation,
thermoregulation and activity).
It has been proposed that different patterns of energy expenditure among
species (i.e. central versus peripheral, and within this latter
category, differences in levels and modes of energy expenditure) could be
related to each species' life-history strategy
(Koteja and Weiner, 1993;
Koteja, 1995
,
1996a
;
Hammond and Diamond, 1997
).
Accordingly, there is an implicit assumption that SusMR are adaptive. However,
at present it is difficult to confirm this assertion (but see
Koteja et al., 2000
).
It is possible that organisms do not have excess capacities, and the
capacity of central organs to supply energy has evolved to match expenditure
capacity in peripheral tissues. This hypothesis, with no limiting step on
SusMR, but with optimal organism design, is called symmorphosis
(sensu Taylor and Weibel,
1981).
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The optimal design debate: symmorphosis |
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Optimization models in biology make assumptions about (i) constraints
acting on phenotypes, (ii) the optimization function and (iii) heredity
(Maynard Smith, 1978), so is
it possible for natural selection to lead to symmorphosis? In other words, is
it possible for natural selection to produce an optimal design? Answers to
both of these questions have been as controversial as the optimization models
(e.g. Gould and Lewontin,
1979
; Garland and Huey,
1987
; Dudley and Gans,
1991
; Garland,
1998
; Gordon,
1998
). In particular, Garland
(1998
) and Gordon
(1998
) point out reasons for
refuting symmorphosis: (i) organisms must perform different functions
simultaneously, which probably creates constraints that prevent them from
reaching an optimal solution for all processes; (ii) biological materials have
limitations related to their own histories; (iii) in general terms,
environments are always changing, and natural selection often cannot follow
the rhythm of change; and finally (iv) genetic drift can be an important
factor in some populations. Nevertheless, even if animals are not optimally
designed, Garland (1998
)
pointed out that optimization models can be useful tools for understanding the
evolution of physiological systems. In this sense, they can indicate the
`best' design that an organism could achieve, and therefore the concept is
useful as a reference for understanding the reasons for departure from
optimality. To summarize, the main reason why symmorphosis would not be
widespread is that particular structures, and even systems, are often used in
different functions, making it unlikely that optimization could be achieved
for each one (Lindstedt and Jones,
1987
).
How can we test for symmorphosis? In accordance with Taylor and Weibel
(1981) and Weibel and
collaborators (1998
), the
limit of the functional process must be determined. Furthermore, it must be
established whether this limit is related to the organism's design. A clear
description of how to do this is given by Weibel
(2000
). In brief, the first
step is a quantitative physiological study in which, with different levels of
demand, functional performance is pushed to its maximum (i.e. its limit). The
next step would be a morphometric study of design properties related to
functional capacities, followed by evaluation of any agreement between the
functional performance and the morphometric parameters. The original approach
by Taylor and Weibel (1981
)
was between species, using adaptive variation (i.e. animals with the same body
size adapted for different levels of functional performance) and allometric
variation (i.e. animals of different body mass, in which scaling of
morphometric structures should be similar to functional requirements), but the
concept of symmorphosis could be evaluated within a particular species, using
a similar protocol. As mentioned above, in the context of physiological
limitations on SusMR, the symmorphosis principle predicts a match between
central and peripheral organs and tissues. To test for this match, SusMR
should be determined under different levels of demand (e.g. SusMR at
temperatures of -10°C, 0°C and 10°C during cold exposure). The
next step is to evaluate the adjustment between the different SusMRs obtained,
and the morphometric parameters of central and peripheral organs and tissues
(e.g. the dry mass of these organs might be considerEd a good first
approximation). Nevertheless, we must bear in mind that a better quantitative
approach is neccesary to test for symmorphosis
(Weibel, 2000
).
Evidence in favor of symmorphosis (e.g.
Taylor et al., 1996;
Weibel et al., 1996
;
Suarez, 1998
;
Bundle et al., 1999
; Chappel et
al., 1999; Hammond et al.,
2000
; Weibel,
2000
) is as abundant as the evidence against it (e.g.
Garland and Huey, 1987
;
Diamond, 1992
;
Diamond and Hammond, 1992
;
Alexander, 1998
;
Ricklefs, 1998
). At present
the optimal design debate remains unresolved. Furthermore, even when evidence
against symmorphosis is strong, it does not invalidate the usefulness of the
concept (e.g. Diamond, 1992
;
Diamond and Hammond, 1992
)
and, as Diamond and Hammond
(1992
) stated: `the
concept is worth posing not because we believe it to be literally true, but
because only by posing it as a testeable hypothesis of economic design can one
hope to detect where it breaks down, and to identify the interesting reasons
for its breakdown'.
Sorting out the evidence
As mentioned above, SusMR refers to the energy expenditure that can be
sustained over long periods of time by concurrent energy intake while animals
are in mass balance. Consequently, food intake has been extensively used as a
measure of SusMR. This does not present a problem when most food is
metabolized, as occurs in cold acclimation
(Konarzweski and Diamond,
1994; Koteja, 1996; McDevitt
and Speakman, 1994a
), and in these cases, limits on intake could
be considered limits on expenditure. However, during lactation (a widely used
stressor) not all ingested food is metabolized. In fact, an important part is
exported as milk (i.e. it does not represent an expenditure per se)
(Johnson et al., 2001b
). In
this case, the actual level of energy expenditure would be expected to be
lower than expenditure estimated from food intake, as has been demonstrated in
a few scant studies (Johnson et al.,
2001b
; Johnson and Speakman,
2001
; Scantlebury et al.,
2000
). Then, even though food intake in animals subjected to
various stressors may be different (i.e. possible peripheral limitation), the
real expenditure may be equal (i.e. possible central limitation). Certainly,
more work is needed to determine the extent to which these two estimates
differ.
In the particular case of the central limitation hypothesis, Koteja
(1996a,
b
) proposed that: `the
alimentary bottleneck hypothesis is supported by numerous observations and
experiments demostrating that changes in current energy demand or food quality
are associated with changes of gut size...'
(Gross et al., 1985
;
Bozinovic et al., 1990
;
Loeb et al., 1991
;
Toloza et al., 1991
; Hammond
and Diamond, 1992
,
1994
;
Hammond et al., 1994
;
Konarzewski and Diamond, 1994). Nevertheless, this assertion does not validate
the central limitation hypothesis. A change in morphology of the digestive
tract with increasing energy demands, or a decrease in food quality, does not
mean that the digestive tract is the limiting step to energetic expenditure.
It simply shows that the digestive tract is plastic enough to change according
to demand, and that there is a cost for supporting high performance levels
when these levels are not required (DeWitt
et al., 1998
). So, a possible reason why these organs grow under
high food intake or energy requirements is that they possess limited
functional reserves under conditions of low demand
(Hammond and Konarzweski,
1996
; Hammond and Kristan,
2000
). Similarly, if metabolic ceilings reach the same value under
different modes of expenditure, most authors would agree that a central
limitation exists. However, this procedure does not exclude the possibility of
a peripheral limitation on SusMR because, by chance, different modes of energy
expenditure might have equal values. A way of discriminating between both
hypotheses is through a combination of peak energy demands. If central
limitation really is the cause of the metabolic ceiling, one would expect a
conflict in energy allocation when different high-energy-demanding activities
are being performed simultaneously. Conversely, if limits on SusMR are set
peripherally, no conflict in energy allocation would be expected since central
organs possess an excess capacity.
With the exception of a few studies
(Hammond et al., 1994;
Derting and Austin, 1998
;
Hammond and Kristan, 2000
;
Johnson and Speakman, 2001
),
this topic (i.e. design constraints and conflict among demands) has not been
explicitly approached, even though it plays a key role in determining, at
least theoretically, the signs and magnitudes of genetic correlations among
high-energy-demanding activities and, consequently, their response to natural
selection (Stearns et al.,
1991
; Stearns,
1992
). In particular, the response of any two genetically
correlated traits to natural selection is dependent on the sign of the
correlation (Stearns et al.,
1991
). If the correlation is negative, a positive response to
selection in one trait would generate a negative response in the other. Thus a
central limitation on SusMR could generate a negative correlation among
different activities using energy in parallel, with the consequences manifest
in the response to natural selection. Furthermore, in many aspects of ecology
and evolutionary biology (e.g. mechanistic aspects of life history evolution)
(Stearns, 1992
), an implicit
central limitation, in the form of the Principle of Allocation
(Cody, 1966
), is always
assumed. Nevertheless, the presence of peripheral limitations could challenge
this view and force it to change or to be restricted to particular situations
(i.e. when central limits are in fact operating).
Even though methodology that combines energy demands might distinguish
between central and peripheral limitations, it does not exclude the
possibility that structure and function adjust to the new conditions (i.e.
symmorphosis). The central and peripheral limitation hypotheses assume that
organisms have evolved with certain limiting steps in energy expenditure,
while other steps have kept unused reserve capacities. In this sense, it is
not enough to demonstrate the site of limitation; one must also demonstrate
the existence of excess capacity in the central machinery (if the limitation
is set peripherally), or excess capacity of peripheral organs (if the
limitation is central) (Fig.
1). This has only been tested on a few occasions, however, and
always using laboratory species (Toloza
et al., 1991; Diamond and
Hammond, 1992
; Hammond and
Diamond, 1992
; Hammond et al.,
1994
; Konarzewski and Diamond, 1994), so we are not able to draw
firm conclusions as to whether limits are set centrally or peripherally.
|
Considerations of optimal design necessitate caution in interpreting
changes (morphological or physiological) associated with phenotypic
plasticity. At first glance, it may seem that such changes are a consequence
of symmorphosis or optimal design (e.g.
Lindstedt and Jones, 1987;
Weibel, 1998
); however, more
detailed inspection may eliminate optimal design
(Toloza et al., 1991
;
Diamond and Hammond, 1992
).
For example, food intake by lactating females increases almost linearly with
the total mass a mother must support (mass of mother and young), plus time of
lactation, because each young requires more milk as it grows (e.g.
Hammond and Diamond, 1992
).
Although there is an increase in food intake following parturition, however,
the digestive efficiency of Mus musculus does not change either with
number of young or the duration of lactation
(Hammond and Diamond, 1992
).
How can digestive efficiency be maintained under these high-energy-demanding
conditions? One possibility is that the small intestine has excess capacity,
and efficiency can therefore be maintained in spite of the increase in food
intake. In this case, according to the symmorphosis principle, design is not
considered to be optimized due to this excess capacity. Another
possibility is that the small intestine grows rapidly enough during lactation
to match the increasing food intake. Here, optimal design is implicated,
because there is an adjustment between structure and function. In general,
both kinds of changes are happening
(Toloza et al., 1991
;
Diamond and Hammond, 1992
;
Hammond and Diamond, 1992
). As
shown, a morphological change in accordance with changes in functional needs
seems to be the result of an optimal design; however, a detailed analysis
could show another point of view, that is, excess capacities should indicate a
suboptimal design.
The presence of a link between RMR and SusMR is the principal idea behind
the proposal of a central limitation on energy budgets
(Speakman, 2000, and
references therein). However, we contend that caution is needed when
considering the argument that this link is determined by a central limitation.
In mammals, the greatest increase in energetic demands occurs during lactation
(Millar, 1978
;
Mattingly and McClure, 1985
;
Kenagy, 1987
; Kenagy et al.,
1989a
,b
,
1990
), and also cold exposure
(e.g. Konarzweski and Diamond,
1994
; Merritt et al., 2001;
Nespolo et al., 2001
). Both
activities result in an increase in food consumption
(Hammond et al., 1996
). This
involves processing (i.e. digestion, absorption and transport) of greater
amounts of nutrients, which could produce hypertrophy of the central organs
associated with these processes and a resultant increase in RMR. In this
respect, SusMR and RMR may be correlated, but the type of limit on SusMR (i.e.
central or peripheral) remains an open question. The observation of a link
between both traits alone is not enough to confirm a central limitation, nor
is the absence of a link enough to support the opposite conclusion (i.e.
peripheral limitation). Thus there is a need for correlational studies,
complemented by experiments. For example, values of RMR and SusMR in Mus
musculus (Hammond and Diamond,
1997
) using different modes of energy expenditure, provide
evidence that there is an important correlation between the two rates, which
would suggest a central limitation on SusMR. However, the combined works of
Hammond and coworkers on the physiological limitations in white mice
demonstrated that the limitation is not central (Hammond and Diamond,
1992
,
1994
; Hammond et al.,
1994
,
1996
; Konarzewski and Diamond,
1994).
In summary, we feel that these hypotheses lack strong empirical data to demonstrate that central and peripheral physiological limitations hold true both in animals in the laboratory and in the wild (Fig. 1). We propose that the following steps are necessary to identify the intraspecific physiological limits on SusMR: (1) use of a combination of peak energy demands to differentiate between central limitation and peripheral limitation; (2) pushing animals to their physiological limits (e.g. asymptotic food intake), (3) testing for a central excess capacity if the limit is set peripherally, or a peripheral excess capacity if there is a central limitation, and (4) utilizing different levels of energy demand to test for symmorphosis. Finally, without more empirical evidence it is not possible to determine which design is most common in nature and why, nor can we identify the ecological and evolutionary consequences of each type of physiological limitation. In addition, studies that incorporate locomotory activity as a stressor are needed. Testing for symmorphosis with this stressor, could be done by comparing SusMR of non-selected versus selected lines for different levels of running activity.
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Concluding remarks |
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The answer to the first question has been associated with the potential
decrease in fitness that a mammal might experience if it were to expend more
energy than it routinely does (Murie and
Dobson, 1987; Wolf and
Schmidt-Hempel, 1989
; Stearns,
1992
; Martin and Palumbi,
1993
; Daan et al.,
1996
; Finkel and Halbrook,
2000
; Speakman,
2000
). However, the evidence for this trade-off (i.e. energy
expenditure versus fitness) is not conclusive
(Tuomi et al., 1983
;
Hare and Murie, 1992
;
Speakman, 2000
). As to the
second question, organisms could function at or near their physiological
limits, but are prevented from doing so because of energy limitations imposed
by the environment (e.g. Stenseth et al.,
1980
; Speakman,
2000
). At present there is insufficient evidence to offer
definitive answers to these questions, and we cannot conclusively identify
which physiological factors may impose limits on SusMR. Hence, there is a need
for further studies aiming to unravel the nature of the physiological limit on
SusMR (i.e. central, peripheral or symmorphosis) and the steps where this
limit occurs.
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Acknowledgments |
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