Download When and How Much to Reproduce: The Trade

AMER. ZOOL , 16:763-774 (1976).
When and How Much to Reproduce: The Trade-Off Between Power and Efficiency
CHRISTOPHER C. SMITH
Division of Biology, Kansas State University, Manhattan, Kansas 66506
SYNOPSIS A compromise between speed and efficiency of energy conversions gives the
maximum power of useful energy conversion at intermediate efficiencies. Organisms are
selected to maximize the power of energy conversions to a useful form. However, most
species have very little capacity to vary the efficiency of their energy conversions in response
to variation in the intensity of the environmental power supply. Plants can respond slowly to
horizontal variation in the availability of energy by growth. The trade-off between power
and efficiency which is dependent on the compromise between speed and efficiency of
energy conversions does seem to apply to the relative efficiencies of successive species in a
sere of secondary terrestrial plant succession. The application of the power trade-off to
species in a sere predicts the common general properties of growth and reproduction in
succession. The power trade-off may also help to explain reproductive patterns in animals
that differ in the concentration of their food supply. The thermodynamic basis of causation
provided by the power trade-off could be a valuable tool for connecting evol utionary ecology
with community and ecosystem studies.
INTRODUCTION
The problem of when and how much to
reproduce is central to all aspects of natural
selection and evolution. Any trait of an
animal or plant relates either to how quickly
it can accumulate resources for reproduction, how likely it is to stay alive to use those
resources for reproduction, or how it distributes those resources in reproduction.
All genetically determined traits ultimately
derive their relative fitness from their influence on the reproductive contribution to
future generations of the organisms that
carry them.
Any approach to the problem of when
and how much to reproduce should be
broad enough to have universal application
while still giving insight into the evolution
of any particular species. In this paper and
the following paper by Pianka two different
approaches will be outlined. Pianka develops the trade-offs that evolve when there
is selection for concurrently maximizing
the efforts in time and energy for three
conflicting demands: (1) to acquire more
energy, (2) to reproduce, and (3) to avoid
death. My approach will be to develop the
generality proposed by Odum and Pinkerton (1955) that natural selection tends to
maximize an individual's power of conversion of environmental energy to its own
use. Pianka and I attack the same problem
from opposite directions. Pianka shows
how the components of reproductive effort
interact to form a complete pattern. I
assume a complete pattern and work backwards in order to demonstrate how the
components of reproductive effort should
interact to form that pattern.
POWER AND EFFICIENCY
The idea that selection favors the
maximum power of energy conversion to a
useful form is essentially a way of stating, in
energetic terms, that selection favors
I profited from the helpful criticism of the ideas in maximum contribution to future generathis manuscript given by Mitchell Taylor during tions. The equivalence of the two expresnumerous long discussions of the subject. Martin sions assumes that excess energy can be
Stapanian also provided some helpful suggestions. converted into successful offspring. It also
Thomas Porter helped in developing the graphical assumes that if some material is limiting,
representations in the figures and drew the final
figures. Sharon Martin and my wife, Ann, gave patient there exists a positive feedback between
acquiring more energy and more of the
assistance in preparing the manuscript.
763
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CHRISTOPHER C. SMITH
limiting material. In fact, maximizing contribution to future generations is equivalent to maximizing the power of reproduction where genes or offspring are substituted for Units of energy.
Odum and Pinkerton (1955) stress the
contrast between maximizing the power of
energy conversion and the efficiency of
conversion. They use Atwood's machine
(Fig. 1) as a simple example to demonstrate that when there is a constant rate
of energy input, the efficiency of energy
conversion that gives the highest power
output is well below the highest possible
efficiency. All energy conversions follow
the pattern of Atwood's machine where an
increase in the efficiency of energy conversion to a usable form results from a decrease in the speed of the energy conversion. The trade-off between speed and
efficiency leads to a maximum power when
the efficiency is 61.8% for Atwood's
machine (Fig. 1), not at 50% as in Odum
(1971).
The heavier weight in Atwood's machine
is analogous to the environmental input of
energy in a biological system and the lighter
weight is analogous to the biologically useful energy that the biological systen can
derive from the environmental energy. In
Atwood's machine the lighter weight is varied and the heavier kept constant in order
to generate different efficiencies and powers of energy conversion. However, in the
evolution of biological systems it is the
energy input from the environment that
varies independently and the speed and
efficiency of energy conversion in the
biological system that evolves to exploit the
environmental energy. In making the analogy between Atwood's machine and biological systems, it is valid to vary the large
weight as well as the small (Fig. 1), and to
have the change in the large weight precede
the small. By decreasing only the larger
weight, or by analogy the input of environmental energy in a biological system,
the speed and power of energy conversion
are decreased while the efficiency is increased (Fig. 1).
The analogy between Atwood's machine
and biological systems requires close consideration. Because the weights are connected
in Atwood's machine, any increase in the
heavier weight will result in an increase in
the power of energy transfer to the small
weight. However, an increase in energy in
the environment of an organism may not
result in an increase in energy uptake by the
organism. Most animals can be given more
food than they can eat. The analogy with
Atwood's machine breaks down in living
systems because individual organisms do
not have a completely flexible facultative or
homeostatic response to variation in the
environmental power supply.
Some levels at which individuals could
respond homeostatically to varying energy
supplies are: 1) biochemically by substituting metabolic pathways with different
numbers of steps and different equilibrium
constants, 2) physiologically by varying the
rate of food intake and the efficiency of
digestion, and 3) behaviorally by varying
the foraging effort in response to energy
supply. A slower facultative response to
high levels of environmental energy flow is
growth. In the analogy with Atwood's
machine, growth is equivalent to increasing
the size of the smaller weight. Its increase
will increase the efficiency of the energy
conversion. The following sections describe
the probable extent to which organisms
adjust their power of energy conversion by
short term homeostatic mechanisms and by
the longer term action of growth. Where
growth is the more effective adjustment the
question remains whether the growth
should be invested in the existing organism
or in reproduction. It is this dichotomy that
will be the basis of decisions as to when and
how much to reproduce.
Homeostatic Responses to Environmental Power
Supply
The efficiency of converting chemical
energy from one form to another by a series
of coupled reactions in a metabolic pathway
could theoretically be increased by substituting another pathway with more steps
each with a lower equilibrium constant.
Such a substitution should decrease the rate
of energy conversion. The trade-off between speed and efficiency should give a
power curve similar in shape to that given
765
WHEN AND H O W MUCH TO REPRODUCE
15-
TIHE 10 FALL
20 METERS
2:0
2.6
35
5.3
WEIGHT (Kg)
TIME OF FALLtseo
2.0
W
2.6
20
35
30
53
40
°°
POWER
(kilowatts)
EFFICIENCY
80 Kg
40Kg(J
20 M
I
FIG. 1. The power trade-off expressed on Atwood's
machine. The two examples show the effect of changing the size of the large weight on Atwood's machine
while keeping the smaller weight (shown by points on
the curves) constant. The upper curves show speed of
energy conversion when the smaller weight is varied
on Atwood's machine. The lower two curves show the
relationship between power and efficiency when varying the smaller weight. Because efficiency is directly
proportional to the size of the smaller weight, the
abscissa of the upper curve is the same as the lower
curve for each of the two machines represented.
by Atwood's machine. However, the broad phylogenetic spectrum and are rarely
metabolic pathways of intermediary substituted within an organism (Lehninger,
metabolism are very conservative over a 1970). Lehninger explains the conser-
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CHRISTOPHER C. SMITH
vatism of intermediary metabolism on the
basis of ATP being the universal intermediate in the coupled reactions of biological energy transformations. The equilibrium constants of catabolic and anabolic
reactions should be of the same general
magnitude as those used for the conversion of ATP to ADP. Although this limitation still leaves some theoretical possibility
for alternate metabolic pathways of different power output, the genetic and structural costs of maintaining alternate pathways would seem to have prohibited their
evolution. Instances where parts of pathways are uncoupled, as in uncoupled oxidative phosphorylation, are equivalent to Atwood's machine with no light weight attached. All the energy input is converted to
heat, which in cold acclimation and arousal
from torpor, may have a biological function
(Hochachka and Somero, 1973). These uncoupled reactions are not necessarily used
in direct response to variation in the environmental energy input in the case of
arousal from torpor. However, the ultimate
biological function of uncoupled reactions
probably is to influence the rate and timing
of the use of environmental sources of
energy.
The alternate pathways of carbon fixation in plants (the Calvin cycle = C3 plants
and the C4 — dicarboxylic acid pathway =
C4 plants) could function to adjust the
power of energy fixation of plants in response to variation in the environmental
supply of energy and/or water (Hatch and
Slack, 1970; Black, 1971). However, C3and
C4 plants differ in the structure of their
leaves and chloroplasts and the alternate
pathways are probably not found together
in many, if any, plants as alternate responses to changes in the environmental
power supply (Hatch and Slack, 1970).
Other than uncoupled oxidative phosphorylation, where heat energy assumes
a biological function, it would appear that
homeostatic mechanisms based on alternate biochemical pathways are rarely used
in response to variation in the environmental power supply.
Richman (1958) provides an excellent
example of the interaction of food supply,
feeding rate, and efficiency of digestion
giving a power trade-off analogous with
Atwood's machine (Table \). Daphniapulex
were fed on four different concentrations
of the single celled algae, Chlamydomonas
reinhardi. Over a 34-day period of feeding
at the four concentrations, adult animals
fed the higher concentrations ate more,
digested their food at a lower efficiency, but
had a higher power of assimilating usable
energy. The study is of particular interest
because Daphnia uses the same leg movements for feeding and respiration and so it
filters the same volume of water at all four
concentrations of algae, probably to maintain its respiratory rate. The confusing
interaction resulting from feeding behavior and assimilation efficiency each
varying independently of the other in response to variation in the environmental
power supply is absent in Daphnia. Richman
supplied food at a rate which adult Daphnia
TABLE 1. Environmental power supply, food consumption, assimilation efficiency, and power of assimilation of Daphnia
pulex oftwo age groups fed on Chlamydomonas reinhardi at four concentrations. (Adapted from Richmond, 1958)
Food concentration
(environmental power)
(cells/ml/day)
Energy
consumed
(cal/time)
25,000
50,000
75,000
100,000
5.671
13.004
19.351
27.328
Per cent
assimilation
Power of
assimilation
(cal/time)
31.72
20.17
16.84
14.22
1.80
2.62
3.26
3.88
Adults over 34 days
25,000
50,000
75,000
100,000
Preadults over 6 days
0.469
0.582
1.388
1.910
23.88
15.81
8.36
6.60
.112
.092
.116
.126
WHEN AND HOW MUCH TO REPRODUCE
could utilize, but for the first six days of
their life the Daphnia did not significantly
increase the power of assimilating energy
with the four levels of environmental
energy he supplied (Table 1). It is likely that
digestion can assume a power trade-off
analogous to Atwood's machine over only a
limited range of environmental power
supplies. This range of power supply is
probably the range that is most commonly
found in the environment of the animal.
Most studies of feeding rates and assimilation efficiency employ foods of different
quality among which the animals choose.
Both the difference in quality of food and
the behavioral response to it tend to hide
any power trade-off analogous to Atwood's
machine. For example, Robel et al. (1974)
found /.hat bobwhite (Colinus virginianus)
feeding on two types of food in two habitats
in the wild ate more of the less digestible
food and passed it through the gut faster
than the more digestible food. However, it
was at least partly the nature of the food
and not the power of its supply alone that
made one diet less digestible than the other.
In fact, the food that was consumed at the
higher rate provides a lower power of
assimilated energy.
In order for feeding behavior to work as
a power trade-off analogous to Atwood's
machine, an animal would have to expend
more effort in feeding as food became
more abundant. Such a response could be
expected at a threshold between conditions
in which foraging did not acquire enough
food to pay for itself and conditions in
which it did. Such a threshold would be
expected only for organisms that have a low
resting metabolism. Once over the
threshold where foraging pays for itself, an
increase in the power of food supply would
actually decrease the behavioral cost of
finding it (Holling, 1966). A second
threshold is often reached where feeding
stops because the animal can hold no more.
Therefore, feeding behavior should not
form a continuous power trade-off analogous to Atwood's machines.
The one group of organisms which
might be expected to have a homeostatic
adjustment of the efficiency of energy conversion to maximize the power of energy
767
conversion would be filter feeders such as
Daphnia, barnacles, sponges, clams, etc. In
these organisms, feeding and respiration
are combined in the same activity while the
power of food supply can vary independently from oxygen supply. Thus, a constant
movement of water by the filtering
mechanism to supply oxygen can result in a
varied supply of food which should be
handled as Daphnia does. Animals that
forage for food might have a digestive
efficiency that gave a power trade-off similar to Atwood's machine, but that relationship should usually be hidden by a feeding
behavior that works in the opposite direction.
Growth in response to power supply
In analyzing growth in response to variation in power supply, green plants are more
easily understood because there is much
less variation in the nature of their energy
or material resources than there is in animals. The group of plant species in a sere of
secondary terrestrial succession serves as a
good example of species which have the
same broad pattern of energy and material
input but vary in the power of available
energy and material per gram of plant as a
result of increasing competition during
succession. The variation of environmental
power in time should be the same for all
successional stages, and the power supplied
by the environment will be considered
constant for simplicity of analysis. A
hypothetical analysis of how the power
trade-off should be expressed in successional species should demonstrate the effect of a wide range of power supplies on
the growth patterns of plants and give some
hint as to what to look for in animals.
The power available to a plant can be
considered as varying in two spatial components that will be considered separately
before looking at their interaction. (1)
There can be variation in the intensity of
light striking a unit of surface of a plant. (2)
There can be variation in the area of
ground over which light of some given
intensity is striking free of competition
from plants other than the one being considered. For practical purposes the two
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CHRISTOPHER C. SMITH
components measure the point and horizontal variation, respectively, in the power
of light available to a plant. The first
component could be responded to by a
power trade-off in the plant that would be
analogous to Atwood's machine. As previously discussed, it would appear that one
plant does not encompass the variation in
biochemical and physiological adjustments
necessary to produce a broad power
trade-off similar to Atwood's machine.
However, successive plant species in a sere
could each have a pattern of energy conversion that would, when combined, fit such a
power trade-off.
Variation in the intensity of the power supply
Successive species in the sere should each
be adapted to a lower light intensity as the
sere progresses. To be analogous with Atwood's machine a unit of surface area in the
leaves of successive species would trap less
light energy per unit time, but do it more
efficiently. More efficiently implies that a
smaller per cent of the light energy that is
trapped is lost as respiration. This relationship is diagrammed by the relative heights
of the two curves (dotted and solid) for each
of the two species in Figure 2 and is
analogous to the diagram of Atwood's
machine in Figure 1. I assume that the
biochemistry of plants has not evolved to
the point where leaves can be 62% efficient
in utilizing the most intense sunlight, an
assumption that is consistent with measurements of the efficiency with which
plants use sunlight. Therefore, the power
trade-off should be operating at efficiencies
of less than 62% as diagrammed in Figures
1 and 2. The area of leaf surface or, in
Atwood's machine, the lighter weight is
held constant while the intensity of light or
the heavier weight is decreased with successive species. Because we are dealing with
successive species which probably have little
phenotypic plasticity in terms of a power
trade-off, each species grows faster than the
others in the light intensity to which it is
specifically adapted. In high-intensity light
a late-successional species will grow more
slowly than an early-successional species
because it can not trap as much energy per
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FIG. 2. Growth of individual plants to fill a horizontal area free of competition. Diagram A represents the
growth of an early-successional species in intense light
and corresponds to Atwood's machine A in Figure 1.
Diagram B represents the growth of a latersuccessional species in less intense light and corresponds to Atwood's machine B in Figure 1. The dotted
line in each diagram is the light energy trapped (TE)
and the solid line the energy lost as respiration (R).
The vertical distance between the two lines is the
energy available for growth. The relative heights of
the lines shown to the right of the diagram are
consistent with the power functions of Figure 1. The
curves move to the left as growth proceeds and the
area is filled at a geometric rate. The constant proportional height of the two curves in each diagram
assumes that all growth is in new photosynthetic tissue.
See the text for the consequences of the inaccuracy of
this assumption.
unit area. In low-intensity light the latesuccessional species will trap the same
amount of light as the early successional
species, but will use less of it for respiration
and have more left for growth.
The greater speed of growth of a pioneer
species in high-intensity light might appear
to give it an ability to keep its leaves above
later-successional species for an indefinite
period so that it could continue to utilize the
high intensity of light for which it is
specialized. However, such an argument is
based on the assumption that all growth
produces new tissues that trap light of the
same intensity. If an increasing per cent of
the growth goes into support tissue with a
respiratory rate proportional to that in the
leaves for each serai stage, then the proportionally high respiratory rate in the support
WHEN AND HOW MUCH TO REPRODUCE
tissues of pioneer species would eventually
decrease their geometric growth rate of
new leaves below that of later successional
species. In other words, a slow but efficient
conversion of environmental energy
should allow maintenance of a higher
proportion of tissue that is not directly
involved in trapping more energy.
Another component of plant growth that
does not add to the amount of tissue used
for trapping light is the secondary plant
substances and structures that inhibit the
feeding of herbivores (Fraenkel, 1959). The
longer a plant tissue remains in one place
the more likely it is to be fed upon by a
herbivore (Janzen, 1969 and Smith, 1970),
and the more intense the herbivore feeding, the higher the proportion of growth
that is directed at inhibiting the feeding
(Smith, 1970 and Cates, 1975). Therefore,
as succession proceeds and successive species grow more slowly and stay longer in the
same place, the plants should be under
more intense selection for placing a higher
proportion of their growth in herbivore
defenses (Feeny, 1975 and Cates and
Orians, 1975). Individuals of early-successional species adapted to high light intensities could not maintain their position in a
community unless they increased their proportion of growth in herbivore defenses.
Such an increase would lead to the same
problems as an increase in the proportion of
growth in support tissue; the early successional species with fast but inefficient
energy conversions would spend more
energy to build a given amount of support
and defense tissue than would a more
efficient, later-successional species. Eventually the early species would have less
energy for growth of leaves and would lose
out in competition for light.
Variation in the horizontal availability of power
When a seedling spreads its first leaves in
a light intensity to which it is adapted, it
usually does not cover all the area in which
energy is potentially available. The only
response open to it for increasing the per
cent of this light that it uses is to grow
laterally. Figure 2 represents the efficiency
of utilizing all the energy available in the
769
area free of competition by a plant species
as it grows to cover that area. The two
diagrams (A and B) represent patterns for
two species that are adapted to different
light intensities. Each curve represents all
points of equal power conversion per gram
or unit surface area of plant tissue. As the
plant grows to cover an area, there is less
energy in the total area per gram of plant
tissue and a higher percent of the energy
available in the area is being used. Therefore, the product of the two axes (x = the
relative flow of environmental energy per
total uncontested area per gram of tissue of
the whole plant times y = the percent
efficiency of utilizing the area) is a constant
flow of environmental energy per gram of
tissue. These constant products of the two
axes are hyperbolic functions. Any vertical
line in the diagram will intersect the dotted
function for energy trapped per gram of
leaf and the solid function for respiration
per gram of leaf at the constant ratio of
heights shown to the right of the diagrams.
The rate with which growth progresses and
the function moves to the left is proportional to the vertical distance between the
dotted and solid lines at each point in time
and should be geometric if the growth of
support tissue is ignored. The direction of
growth, succession, and homeostatic
changes in response to differences in environmental power supply are illustrated in
Figure 3.
In predicting the combined response to
point and horizontal variation in the environmental power supply, support and
protective tissue can not be ignored. It is the
increasing proportion of energy expended
on these tissues as growth is prolonged that
should allow plants with slow but efficient
energy conversions to succeed plants with
fast but inefficient energy conversions. As
the later-successional species do grow
above the earlier species in the sere the light
intensity they experience is increased.
Horn (1971) has demonstrated how the arc
cut by the sun in the sky prevents the
casting of complete shadows and allows an
adaptive geometric layering of leaves to
utilize a higher per cent of the incident
radiation than one solid layer could. The
consequence of this geometry is that with
770
CHRISTOPHER C. SMITH
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2
3
RELATIVE FLOW OF ENVIRONMENTAL ENERGY
PER AREA PER GRAM OF TISSUE
FIG. 3. The response of plants to variation in the
environmental power supply. The arrows point the
direction of growth, homeostatic and successional responses of plants to variations in the environmental
power supply. The relative magnitude of homeostatic
and successional changes are represented by the
length of their arrows. Dotted curves A and B
correspond to the solid curves of diagrams A and B of
Figure 2.
the use of support structure to layer leaves a
species with a slow but efficient conversion of energy can use an increased per cent
of high intensity light once it outgrows the
shade of earlier successional stages. A
parallel consequence of the layering is that
the height to which successive stages must
grow before they are free of the shade of
earlier stages is prolonged and there are
likely to be fewer stages before the absolute
limitations of support tissue are reached.
These absolute limitations are dictated by
the maximum tensile strength of wood and
the fact that the diameter of support tissue
must grow in proportion to the threehalves power of the height of the plant
(Thompson, 1917). As succession proceeds
and the proportion of support tissue is
increased, the horizontal area covered by a
plant should also increase. Therefore the
size of plants should increase in three
dimensions as succession proceeds and the
effect of variation in the intensity of light
during succession should allow plants to
increase their effectiveness in responding
to horizontal variation in the availability of
light. The advantages of growing slowly but
efficiently should eventually allow plants to
compete more effectively for light in the
horizontal as well as the vertical dimension.
WHEN AND HOW MUCH TO REPRODUCE
Both growth and reproduction have potential rates of increase that are geometric.
Moreover, the growth of energy-trapping
structures has a direct feedback on allowing
an increased rate of reproduction. Natural
WHEN AND HOW MUCH TO REPRODUCE
771
selection is differential contribution to future generations by individuals within a
population. However, competition with
other species often determines the relative
reproductive success of individuals within a
species. To understand the effects of the
trade-off between power and efficiency on
the evolution of reproductive patterns we
should start with competition between
species and its effect on growth in order to
understand which growth pattern within a
species feeds back to a maximum reproductive rate.
Ad
Consider two species in a sere starting to
grow together in the same horizontal area
at the same time under a light intensity to
which the earlier species is adapted. The
earlier species will grow faster at first because it can trap more of the light per unit
surface area of leaf. Even though it uses a
higher per cent of its trapped energy as
respiration in accordance with the power
trade-off, the earlier species still has more
energy left for growth. Its geometric rate of
growth will exceed that of the later species.
As growth continues, the proportion that
goes into support and defensive tissues
increases and less is available for growth of
new leaf surface. As the geometric rate of
growth of new leaf surface decreases it will
eventually reach the rate of the latersuccessional species (Figure 4). It is at this
point when the geometric rates of growth
of the two species are equal that the earlier
successional species should start to divert
some of its net new growth into reproduction in order to maximize its rate of reproduction. As the second species grows under
the first it too should have a decreasing FIG. 4. The growth rate of leaf surface area of three
species in a terrestrial sere that results in
geometric rate of growth of new leaf sur- plant
maximum reproductive rates for the first two species
face. The first species should continue to (A and B). Starting at the top, the three diagrams are
put enough energy into net new growth of plots of the time course of changes in I) the amount of
leaves and structural material to keep its leaf surface area, II) the rate of change of leaf surface
and III) the geometric rate of change of leaf
potential geometric rate of growth of leaf area,
surface area. The doited lines starting at Ar and Br in
surface the same as the species succeeding each diagram are the changes in growth of leaf surface
it. The remainder of its net growth should area resulting from earlier successional stages followgo into reproduction. This strategy of re- ing the geometric growth rates of leaves of the
productive effort would allow each indi- following stage in the sere. The dotted lines end at Ad
Bd when the earlier successional species are
vidual in each successional species to pro- and
shaded by the following stage in the sere and die. The
duce the maximum total reproductive ef- areas integrated under the dotted lines in diagram II
fort if it is under maximum intraspecific represent the net production during the period of
competition for its power supply. The as- reproduction for species A and B; the cross-hatched
of the net production being reproduction and the
sumption of maximum intraspecific com- part
unhatched part being leaf growth.
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CHRISTOPHER C. SMITH
petition is consistent with the earlier assumption of a continuous power supply in
time. The selective advantage of reproducing early in times of superabundant resources could only come after a temporal
increase in the power supply.
Because successive species in a sere are
growing at slower rates and having to reach
a greater height before they reproduce,
each successive species should reproduce at
a later age. As the time necessary for
successive species to replace each other
increases, the period over which the potential geometric rate of the early and late
species are equal and track each other
should increase. Therefore, both the life
expectancy and period of reproduction
should increase with successive species.
In summary, the trade-off between
power and efficiency, when applied to successive plants in a sere which experiences
no temporal variation in power, predicts a
number of common properties of succession. (1) Early species can not gain a
monopoly on resources. (2) Early species
grow faster and have a higher proportion
of their growth in photosynthetic tissues.
(3) Early species reproduce at an earlier age
and for a shorter time.
THETRADE-OFF BETWEEN POWER AND EFFICIENCY
IN ANIMALS
The power trade-off gave most insight
into the pattern of plant growth and reproduction when the intensity of light or point
variation of power was considered. A comparable measurement for animals is
difficult because animals can move to their
food. Those sessile forms which filter food
are superficially like plants. However, filtering water does not create an energy shadow
comparable to a leaf intercepting light. It is
unlikely that succession among sessile filter
feeders would be explained by the power
trade-off. In planktonic systems both the
single-celled algae and small herbivores
undergo succession after mineral upwelling (Margalef, 1968). The succession is not
the consequence of intercepting an increasing per cent of a steady environmental
resource supply, but rather a steady decrease in the power of the supply as a finite
resource is used up. However, the effect on
successive species in a sere is likely to be the
same and could be studied more easily in a
planktonic system than in secondary terrestrial plant succession. The presence of
homeostatic power trade-offs within filter
feeding species might complicate the picture.
Among terrestrial animals, the intensity
of the power supply of food might be
expected to be inversely proportional to the
mobility of the organism using it for
growth. Golley (1968) provides some interesting data that support this picture. He
found that the production efficiencies,
which are measured as the per cent of the
food assimilated from the gut that ends up
as secondary production, fell into two distinct groups of values for a wide variety of
animals. The values for nine species of
birds and mammals and one ant ranged
from 0.3 to 3.0% while 10 species of orthopterans, homopterans, mites, isopods,
molluscs, and nematods ranged form 9.1 to
37.2%. Golley thought the split was a consequence of the difference between
homeotherms and poikilotherms and called ants an exception. However, ants, which
had the lowest of the 20 efficiencies, fit the
separation if it is made on the basis of
whether or not the parents progressively
provision their offspring with food. The
birds, mammals, and ant forage over a wide
area expending neuromuscular effort to
gather the energy that is used during the
period of growth of the young. The other
10 species have no parental care and the
young feed themselves to mature size from
a localized food source. The difference in
production efficiency resulting from different forms of parental care could be best
demonstrated with species of wasps with
different feeding habits ranging from those
that lay an egg on the food, through those
that carry one item of food to each egg, to
those that carry several chewed food items
to the young as they develop (Malyshev,
1968).
The separation of these two groups of
animals parallels the trade-off between
power and efficiency in some ways. The
species that feed on the most concentrated
food supply grow faster and reproduce
WHEN AND HOW MUCH TO REPRODUCE
earlier. However, they appear to be more
efficient as well as more powerful in energy
conversion. This apparent contradiction to
the power trade-off may be a consequence
of the difference in what constitutes useful
energy to plants and animals. Essentially all
adaptations to survival and reproduction
are accomplished by growth in plants. In
animals all energy used in neuromuscular
activities is released as heat and for
homeotherms heat itself may be a useful
form of energy. It is still an open question
as to which of the two groups of animals is
slower and more efficient at energy conversions and whether the trade-off between
power and efficiency helps to explain the
difference.
CONCLUSIONS
The trade-off between power and efficiency demonstrated by Atwood's machine
is based on the thermodynamic principle
that energy conversions can not be both fast
and efficient. The conversion that gives the
most power is of intermediate efficiency. It
appears that most species are programmed
to a narrow range of efficiencies of energy
conversions and have very little capacity for
homeostatic adaptation to variation in the
environmental power supply. Because each
species is adapted to a narrow range of
power supply, competitive replacement of
species in a sere may be on the basis of their
relative efficiencies of energy conversion.
An analysis of the consequences of the
power trade-off on succession in an environment with constant power supply is
consistent with the general properties of
succession. The present analysis seems
promising enough to warrant the cooperation between biochemists, physiologists,
and ecologists that will be necessary to
firmly establish the connection between the
power trade-off and patterns of succession
and reproduction. The power trade-off
could be a very valuable tool by providing a
thermodynamic basis of causation for connecting evolutionary ecology with studies
of communities and ecosystems along the
lines attempted by Margalef (1968) and
Odum (1971) in a more descriptive manner. The constancy of the environmental
773
power supply assumed in my analysis is
significant because the same reproductive
patterns can be explained by the frequency
of density independent mortality in the
environment (Gadgil and Solbrig, 1972).
Fluctuations in the environment are the
contingencies for which lipid storage is
usually adaptive. My analysis of reproductive responses in succession in a constant
environment can serve as a control for
responses to fluctuating environments.
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