A M . ZOOLOCIST, 8:83-93
(1968).
Animal Nutrition in Relation to Secondary Production
REZNKAT M. DARNKLL
Department of Biology, Marquette University, Milwaukee, Wisconsin 53233
SYNOPSIS. The constant need to replenish dwindling energy resources compels the animal's
dayjto-day attack upon its food supply. Of the energy taken in through its food the animal
loses a large percentage as non-productive energy while only a small fraction goes into the
production of high-energy chemical compounds, some of which are retained as growth and the
remainder discarded back to the environment. The non-productive energy is lost as wastes
eliminated from Che body, as respiration of symbionts and host, and as frictional heat. Energy
flow through the individual organism is represented in a flow diagram which may serve as a
model for relating future investigations. Several methods for evaluating the intake of food in
natural populations are given, and factors which influence food-intake and feeding are discussed.
Energy flow through natural communities presents complex analytical problems because of
the diversity and nutritional flexibility of the consumer species, factors important in maintaining
community stability. For all the complexity, however, there appears to be a common pattern
discernible in the trophic organization of different communities. A new model for representing
energy flow through communities is presented and illustrated with the common pattern of
community trophic organization.
the fate of this energy as it is transformed
into other bonds, captured by animals and
microorganisms, or dissipated into the environment. Energy, like matter, passes
through natural communities by means of
food-chains, and a quarter of a century ago
Lindeman (1952) pointed out that an overview of the community reveals a trophic
pyramid of energy comparable to that of
materials. But if community food-chains
and food-pyramids are poorly understood,
those dealing with the turnover of energy
are at present even less well defined.
The situation is beginning to change,
however. The analysis of primary production (i.e., the conversion of light energy
into chemical potential energy by photosynthetic plants) has now reached a reasonable state of sophistication, and several
techniques have become available for the
analysis of secondary production (i.e., the
transformation of ingested chemical energy
into other forms of high energy chemical
bonds by the consumer organisms). It is
desirable, therefore, to put forth certain
guidelines which, in a sense, summarize the
degree of our present ignorance concerning secondary production, and to suggest
directions whereby some of the gaps may
be filled.
Animals must obtain from their food all
the chemical elements and specific organic
compounds appropriate to their particular
metabolic needs, but it is not the search
for these materials that compels the constant intake of reduced carbon compounds.
Indeed, the course of evolution would have
been much different if this were the case.
Ionic transport and fixation of carbon dioxide would doubtless have been the primary mechanisms of animal survival.
Rather, one must conclude that it is the
need for constant renewal of dwindling reserves of energy that is responsible for the
day-to-day attack on available food resources.
It is a generally accepted fact that all energy involved in fueling biological systems
is derived ultimately from solar radiation
(a minor exception being the energy derived chemosynthetically by certain bacteria). Photopigments of plants capture
about 1% of the incident light energy in
the form of high energy chemical bonds,
and the remaining story of life deals with
Ideas presented in this paper were developed
through discussions with numerous colleagues to
whom the author is deeply indebted. Thinking
time and some of the research reported herein
were supported by NSF grants GB-2224 and GB5255.
83
84
REZNEAT M.
ENERGY FLOW THROUGH THE INDIVIDUAL
ANIMAL
Understanding energy flow through a
community rests, to a large extent, upon
understanding energy flow through the individual organisms comprising the community. Without belaboring here the differences between the thermodynamics of reversible and irreversible systems (Lehninger, 1965) it can be agreed that the energy
input into an organic system (in the form
of food-intake) results in some energy loss
plus the remainder of the energy which is
tied up in production. This relationship
is expressed in the following equation
which is implicit in all studies of energy
flow through biological systems.
Ej = Enp -f- Ep,
where Ej is the energy input or intake
(from any source and by whatever means),
Enp is all energy taken in that does not
wind up as production, and Ep is energy
tied up in production.
Each of the terms of this equation may
be thought of as the summation of energies
associated with several contributing sources
or processes. Energy intake includes the
energy associated with each type of food
ingested or absorbed. Energy of non-production represents energy lost through several pathways, as discussed below. Energy
of production is the energy accumulated
by the body through growth, together with
that energy which is lost as high energy
compounds manufactured by the body and
discarded into the environment. For want
of a better term this may be referred to as
"secretion." This material includes all discarded gametes, shed skin and exoskeletons, albuminous or mucoid materials released by the body surface or lost from the
gut, and the like. It is clear that these
materials represent production in the true
sense, and although this "secretion" energy
has generally been neglected by workers on
secondary production, the loss of energy
involved may represent a substantial fraction of the total productive energy (Le
Cren, 1962). Many of the present estimates
of production are, therefore, far too low.
DARNELL
A large portion of the food ingested is
never absorbed into the body proper. The
rnicrocommunity of gut symbionts takes
some of the energy for its own metabolic
purposes, including that which it utilizes
for its aerobic or anaerobic respiration
(Hungate, I960). Much of the remainder
is eliminated in the fecal material. Of the
energy-rich reduced carbon compounds
which are absorbed into the body proper
a portion may be lost through the respiration of intra- and intercellular parasites.
The host itself loses energy through its own
respiration and through excretion of reduced carbon compounds. Not all of the
energy released through oxidation of organic compounds is available as free energy to run the organism's metabolic machinery or to be stored (or released) as
production, however. For each of the processes discussed above a certain amount of
energy becomes metabolically unavailable
and is lost as frictional heat. This cost of
work is an important item in the energy
budget, and since it can be roughly estimated on the basis of physiological considerations it should be included in the investigator's thinking. To do so, however,
means that the respiratory figure must be
reduced by an equal amount, so that respiration, as listed here, means the free energy available through respiration or total
energy available through respiration minus
the cost of work.
Before attempting to express the relationships in a more inclusive equation it is desirable to collect certain related terms
which, in practice, are often measured together. It will be noted that in the above
discussion there are really four respiratory
factors (stemming from the gut symbionts,
intracellular symbionts, intercellular symbionts, and the host). Measurements of
whole-animal respiration de facto include
the composite measurement of the whole
system, including these four categories as
well as the respiration of any microbes adherent to the external surface of the organism. Respirometer studies thus represent
the respiration of a small community, the
host together with all of its symbionts.
Partial contributions by each source might
85
NUTRITION AND SECONDARY PRODUCTION
RESPIRATORY LOSS
A
gut
inter- and
symbionts introcellular
symbionts
host
organism
accumulation
egestlon
excretion secretion
ORGANIC DETRITUS PRODUCTION
FIG. 1. Model of energy flow through a single
animal, from intake to accumulation, showing progressive pathways of energy loss. As noted in the
be worked out through studies on germfree animals, but since the metabolism of
the host and its symbionts are often so
intimately tied up, it is seriously questionable whether or not the host under such
conditions could be considered a normal
animal. Whether one is studying respiration or nutrition, the whole microcommunity behaves as an ecological unit. Although the investigator must sort out the
variables and keep them in mind, he may,
in practice, be forced to deal with the
heterogeneous system as a unit. We, therefore, lump all respiratory factors into a
single category.
In dealing with all aquatic and some terrestrial animals it is difficult to separate
fecal production from excretion, hence
these two categories may be thought of
simply as waste material eliminated from
the body. It is likewise difficult to sort the
waste from many of the secretions, especially those which are secreted into the gut
and eliminated in the fecal matter. Since
the secretions represent part of the production, however, efforts should be made
to evaluate this loss separately.
Lumping all respiratory factors and considering egestion and excretion as a single
category, we arrive at the second equation:
text, production includes both secretion and accumulation.
(Er
Eh)
-f E,) =
Ea),
where Ej
E, represent energy
contributed by different food sources, Er is
the energy of respiration, Ew is the energy
lost through wastes, Eh is the "friction"
energy lost through heat, Es is production
energy lost through secretion, and Ea is the
production energy accumulated as growth.
From the foregoing discussion it is clear
that whereas the animal removes reduced
carbon from the environment, it also contributes reduced carbon back to the environment, albeit in a lower average energy state. This material (fecal matter,
excretory and secretory products, and eventually its own body after death) contributes to the widespread environmental pool
of organic detritus which may be reused
repeatedly by the same or different species
until the energy is depleted.
Since the quantities on both sides of the
second equation are subject to change in
response to various environmental and
physiological factors, it is of interest to express the relationships in the form of a
flow diagram which may easily be simulated by computers (Fig. 1). Except for
the general decrease from left to right no
86
REZNEAT M. DARNELL
total (labeled plus non-labeled) food consumed.
2. Rate of consumption of natural food
organisms (subject to repeated census) by
natural predators (themselves subject to
repeated census). This method assumes
that reproduction and extraneous mortality
factors of both prey and predator can be
effectively accounted for (Gerking, 1962).
3. Evaluation of stomach contents of
periodically-collected individuals of the
consumer species. If the rate of movement
or digestive disintegration of the food is
known from laboratory experiments, and
the collecting interval represents the time
METHODS FOR EVALUATING THE INTAKE
required for the newly-ingested food to
OF FOOD
reach a recognizable condition or position
Evaluation of the intake of food by ani- in the gut, then the amount of food conmals in the laboratory is a relatively simple sumed during the interval can be determatter. Larger animals may be provided mined fairly accurately in some species.
submaximal rations which are completely Summation of the food ingested during the
consumed, or they may be placed on ad various intervals gives the total daily ration
libitum feeding with the amount consumed (Bajkov, 1935; Darnell and Meierotto,
being obtained by subtraction of the re- 1962; Windell, 1966).
4. Comparison of growth rates of animaining uneaten food from the total provided. Smaller aquatic animals may be mals in the field with those reared in the
provided a food supply in quantity which laboratory on several different levels of
is known through direct count (Edmond- food-intake. One must assume that the
son, 1957) or amount of C14 radioactivity conditions and rations in the laboratory
(Lasker, 1960; Marshall and Orr, 1955). are sufficiently similar to those in the field
The rate of disappearance of the food to provide comparable results. The method
supply provides an indirect measure of the provides an estimate of the total quantity
of food required to produce the rate of
rate of feeding.
growth observed in the field. By further
Evaluation of the intake of food in nacarrying out periodic checks of the types
ture is infinitely more difficult, but several
of food consumed in the field, one can
indirect methods have been proposed
then parcel the total requirement for food
which are of value in particular cases.
into the percentage of each item taken in.
1. Uptake of isotopically-labeled organTechniques for carrying out routine
isms or organic compounds seeded into the analyses of stomach food have been disenvironment. Food-intake may be meas- cussed by many authors including Hynes
ured either in terms of accumulation in the (1950) and Darnell (1958, 1964). Several
consumer animals or as disappearance from have stressed the importance of the "daily
the environment, due consideration being meal" or "daily ration" as the appropriate
given to other potential avenues of loss. If unit of measurement in discussing die foodthe labeled material is the only source of intake of fish. In some cases the intake of
food then the results of the above study food has been expressed as the number of
give the total intake. If not, then a ratio organisms consumed per unit of time
must be established between labeled and (Putter, 1909; Surber, 1935). In other cases
non-labeled food in the environment. De- it has been expressed as percent of body
termination of the quantity of labeled weight ingested per unit of time (Ricker,
material consumed pennits computation of 1946; Gerking, 1955). Each method has its
significance can currently be placed in the
widths of the various arrows. As data become available, however, the width of each
line may be adjusted to represent the relative or absolute rates of energy flow by
each pathway. Each of the arrows may be
thought of as a ribbon or tape of variable
width which continuously feeds through
the system throughout the life of the animal. It is the province of the animal nutritionist to work out the widths of the
tapes, the circumstances under which they
vary, and the mechanisms by which they
are controlled.
NUTRITION AND SECONDARY PRODUCTION
advantages. Whenever possible, the daily
ration should be expressed in terms of
both calories and nitrogen taken in, since
these terms lend themselves to calculations
of energy metabolism and protein accumulated as growth.
FACTORS WHICH INFLUENCE INTAKE OF FOOD
AND FEEDING
A great many factors influence the choice
of food, the rate of feeding, and the amount
consumed per unit of time. The possibility of individual preferences is obvious
(Pearse, 1924), as is the factor of local and
seasonal availability (Harrington and Harrington, 1961; Pillay, 1953; Seaburg and
Moyle, 1964; Wigley and Theroux, 1965).
Temperature, which exerts an over-riding
influence upon metabolism, strongly influences rates of feeding, higher rates being
associated with elevated temperatures and
lower rates with reduced temperatures
(Baldwin, 1926; Hathaway, 1927; Markus,
1932; Rozin and Mayer, 1961). Excessively
high temperatures, however, may inhibit
feeding, and field studies indicate that the
effects of temperature may be over-ridden
by other factors, since the peak intensity
of seasonal feeding in natural populations
often does not coincide with peak environmental temperatures (Wigley and Theroux, 1965). Many species exhibit seasonal
shifts in food habits (Darnell, 1964; Harrington and Harrington, 1961; Wigley and
Theroux, 1965), and these may reflect seasonal availability of food as well as ontogenetic changes in the capacity to handle
potential food items (Darnell, 1958).
Laboratory studies suggest that fishes tend
to feed for calories rather than for bulk
(Rozin and Mayer, 1961) and that individuals deprived of food for a matter of hours
become hungry and take in more food than
those not so deprived (Bitterman, et al.,
1958; Rozin and Mayer, 1964). Fishes continue feeding until they reach satiation
(Brown, 1951; Hunt, 1960; Ivlev, 1961;
Moore, 1941) which is apparently associated with the storage capacity of the stomach (or anterior part of the intestine in
stomachless fishes) (Rozin and Mayer,
1964). Behavioral factors are clearly in-
87
volved, and individuals of some species
will double their consumption if fed in
groups rather than in isolation (Darnell,
unpublished).
The pattern of distribution of the food
may influence the efficiency of the harvest
(Ivlev, 1961), and fatigue from the work
of procuring the food has been suggested
as a factor (Rozin and Mayer, 1964). Ciearcut patterns in the daily chronology of
food-intake have been reported which involve both the time of feeding (Childers
and Shoemaker, 1953; Darnell, 1958; Darnell and Meierotto, 1962) and the sequence
of types of food taken in (Darnell, 1964;
Webster, 1942). Ontogenetic shifts in die
chronology of feeding are often striking.
The feeding factors discussed above operate within a context of conflicting internal
drives and external stimuli. The nature of
these factors and their complex modes of
operation are illustrated in the following
tentative model of the feeding behavior of
young black bullheads, based primarily
upon the work of Bowen (1931), Darnell
(unpublished), Darnell and Meierotto
(1965), and Tugendhat (1960).
Associated internal factors:
A. Hunger drive—enhances feeding behavior.
B. Social appetite—inhibits feeding behavior.
Associated external factors:
A. Absence of light—inhibits both
feeding and social behavior.
B. Dim light—permits feeding behavior but not social behavior.
C. Bright light—inhibits feeding behavior but permits social behavior.
D. Very bright light—inhibits both
feeding and social behavior.
The observed 24-hr behavior of young
bullheads may be analyzed as follows:
Night (darkness)
—Internal drives inhibited, fishes quiescent.
Dawn (dim light)
—Hungry after several hours without
food the fishes are motivated to seek
food.
—Fishes begin search. They test potential food sources and reject items un-
88
REZNEAT M. DARNELL
suitable because of taste, size, shape,
composition, etc.
—Suitable food items are located, and
some are consumed. Reinforcement
takes place and motivation is increased.
—Continued consumption of food
gradually fills the anterior part of
the gut, and the onset of satiation
progressively lowers the motivation
for feeding.
Mid-morning (bright light)
—With the onset of satiation and possibly some fatigue from feeding, and
subject to increased illumination
(and clearer view of companions) the
young fish ceases to feed and responds
to the social drive. Schooling activity begins. (This activity may be
essential to proper digestion and
movement of food in the gut and to
proper aeration of the blood after a
large meal.)
Mid-day (very bright light)
—Subject to the inhibitory influence of
very bright light the fish cease all
activity.
Early afternoon (bright light)
—Schooling activity resumes.
Mid- to late afternoon (moderate to dim
light)
—Subject to several hours of deprivation, becoming fatigued with social
activity, and with decreasing light,
the fishes gradually commence feeding again.
Late evening (diminishing light)
—With social and hunger appetites
satiated and in the absence of the
stimulus of light, the young fish come
to rest and remain quiet throughout
the night.
This entire pattern of feeding and associated behavior is superimposed upon a daynight wave of temperature (of several degrees amplitude) and an internal circadian
rhythm of activity which manifests itself
when food is withheld in a constant, moderately-lighted environment.
Despite considerable work on the factors which influence the rate of digestion
and movement of food within the gut, the
nature of their operation and their modes
of interaction are only partially understood. These factors fall into three general
categories.
1. Environmental factors—temperature,
salinity, crowding, and disturbance
(such as handling and force-feeding).
2. Quality and quantity of the foodsize, composition, hardness, degree of
encapsulation, etc., of the food; composition of the meal, size, and succession (uniform vs. mixed meals, single
vs. multiple meals, etc.).
3. Internal factors—genetic make-up of
individual animals, prehistory (during early life, as well as immediately
prior to experimentation); age, size,
and condition of individual animals.
Although certain generalizations are possible, the student of the field is more impressed with discrepancies than with similarities between the data of different workers, and these discrepancies appear to reflect, in large measure, real differences between species and their handling of diverse
types of food. Unfortunately, no serious
attempt has yet been made to study a single species exhaustively, although Kinne's
(19fi0fl, b; 1963) work represents an excellent beginning. Nor has an effort been
made to draw together and synthesize published information in this field which is
scattered in several languages through a
century of literature. Certain recent or key
references include the following: Barrington, 1942, 1957; Darnell and Meierotto,
1962; Dawes, 1930; Hunt, 1960; Karpevitch
and Bokoff, 1937; Karzinkin, 1935; Kinne,
19606; Markus, 1932; Molnar and Tolg,
1962; Riddle, 1909; Seaburg and Moyle,
1964; and Windell, 1966. It is evident that
many of these factors influence the efficiency of utilization and conversion of food
(Kinne, 19606), and they must be taken
into account in any serious attempt to understand the programming of energy or
materials through the animal body.
ENERGY FLOW THROUGH THE COMMUNITY
The literature supports the view that
within the aquatic community every available source of organic material is subject
NUTRITION AND SECONDARY PRODUCTION
to utilization by one consumer species or
another (Darnell, 1958, 1961; Edmondson,
1957). Some species tend to specialize
whereas others, as a matter of course, are
quite euryphagic, but most display considerable flexibility in meeting their energyintake requirements. Many fishes and invertebrates consume high-energy foods (living plants and animals) by preference, but
will take in low-energy foods, such as decomposing organic material with its associated microfauna, when their preferred
diets are in low supply or are unavailable.
For other species organic detritus is the
chief or sole source of nourishment. It is
now becoming clear that in all benthic and
other near-shore aquatic environments organic detritus is a major, if not the chief,
source of nourishment for the consumer
species (Darnell, 1967a, b; Darnell and
Meierotto, 1962; Edmondson, 1957; Menzies, 1962; Minshall, 1967; Nelson and
Scott, 1962). Coprophagy is surely involved
(Frankenburg and Smith, 1967; Johannes
and Satomi, 1966; and Newell, 1965), and
the possibility of utilization of dissolved
organic matter as a nutritional source,
originally suggested by Putter (1909) and
discounted by Krogh (1931), has now been
resurrected as a distinct major possibility
for many marine invertebrates (McWhinnie and Johanneck, 1966; Stephens, 1967;
Stephens and Schinske, 1961), if not for
fishes (Darnell, unpublished).
It was pointed out earlier that, as a background for understanding the energy flow
through natural communities, it is desirable to work out budgets for the flow of
energy through individual organisms and
species. Because of the dynamic and flexible
nature of these relations at the individual
level and the diversity of nutritional alternatives in nature, however, achievement
of real understanding of energy flow
through natural communities is, in prospect, a task of some magnitude. In dealing with communities one is faced with
overlapping and parallel lines of energy
flow involving different species, each with
its own built-in flexibilities. Such redundancy in a system automatically leads to
stability, and it is probably true generally
89
that in terms of rates of energy flow the
community as a whole is more stable than
are populations of the component species.
On the other hand, there appears to be a
feed-back, and stable communities, in turn,
tend to stabilize the rates, levels, and cyclic
changes in these parameters at the population level. Much of this stability is mediated through nutritional exchange, and it
is of interest to point out the nutritional
phenomena which lead to stability of
aquatic communities.
1. For their day-to-day existence many
species tend to specialize upon a given
category of food items.
2. Within a given community at any nutritional level several species tend to
overlap, so that a given resource is exploited by more than one consumer
species.
3. Each of the "specialists" is flexible
enough to exploit certain temporary
or unusual food opportunities which
may from time to time become available.
4. Certain species within the community
exhibit extreme nutritional flexibility
most of the time and are quick to
seize upon special opportunities. Such
highly multivorous species are generally quite successful, and they are
clearly the primary day-to-day regulators of the community.
5. Faced with the scarcity or absence of
their primary foods, many species can
apparently subsist for prolonged periods upon a diet consisting partially
or wholly of the ever-present, lowenergy, organic detritus.
6. Most aquatic animals can survive prolonged periods of semi- or complete
starvation. Metabolic adjustments in
the internal allocation of energy reserves place highest priority on survival, lower priorities being given to
growth and reproduction.
7. Most aquatic consumers can allocate
their above-survival energy reserves
between growth and reproduction, so
that some offspring can be produced
in lean years by the stunted individuals.
90
REZNEAT M. DARNELL
8. Most aquatic consumers can adjust
their growth rates to the energy resources available, exhibiting spurts of
growth in response to short-term,
highly-available, nutrient sources, and
they may store energy against lean
periods ahead.
9. Long-term association of particular
species with a given ecological situation permits genetic adjustment to
particular environmental idiosyncrasies. Thus, the organism's seasonal
and ontogenetic demands and the degree of their flexibility become attuned to the predictable environmental variables. The genetic adjustments tend to maximize the organism's efficiency of utilization of environmental resources for growth and
reproduction while doing least damage to the underlying resource.
If an investigator wishes to treat the entire
ecosystem as a "black box" and limit his
attentions to the inputs and outflows, he
may, of course, do so, and for some purposes this is certainly worth doing. But if
he seeks to understand the working machinery of the ecosystem within the box,
he must take account of the above factors.
"To ignore the inherent diversity and the
system of alternatives would seem to be
overlooking the very essence of trophic integration involved in community balance."
(Darnell, 1961).
Careful examination of the literature reveals that, although differing in details, the
trophic structure of different aquatic communities follows a common pattern of organization. This pattern appears to reflect
a commonness in the nutritional offerings
of different environments, as well as a general workable pattern of survival for consumer species within a community, and the
survival pattern itself apparently relates
energy resources and energy flow to stable
systems-organization. If the observations
and line of reasoning are correct it should
be possible to work out this pattern of
energy flow in great detail for certain relatively simple ecosystems and to use such
models as standards for understanding
more complex ecosystems.
As it stands, the trophic pyramid conceived by Elton (1927) and modified by
Lindeman (1942) is a remarkable device
for visualizing a very simple ecosystem in
which the successive components dwindle
in size as a result of progressive loss of energy. However, this model fails in several
respects to meet the criteria for a model
which adequately describes the functional
relations of the ecosystem, and, at the same
time, provides a useful tool for working
with the ecosystem. The Lindemanian
model is based upon the concept of discrete trophic levels which are presently
somewhat indefinable. It does not allow
for species which are multivores, and it
makes no provision for decomposers or recycling of energy through consumer circles which must occur, even though a certain amount of energy is lost at each transformation. A perfectly adequate functional
model would be one in which all the species
in the community were connected by pipelines which could be shut off or partially
opened as the situation demanded. Such a
model would be entirely too cumbersome
for practical use.
A currently reasonable compromise is
shown in Figure 2, which combines the
trophic level of Lindeman (1942) with the
trophic spectrum of Darnell (1961, 1964).
The trophic levels are listed along the left
in sections of equal height from the lowest
at the bottom to the highest at the top. On
the right are horizontal bands whose
heights correspond to the percent of the intake energy of a given species which may
be allocated to a particular trophic level.
The sum of the heights of all the bands
within a given spectrum equals 100%,
which is also the standard height of each
category of trophic level. The width of
each band corresponds to the rate of turnover of energy by the species population.
Since the rates of turnover vary widely
among species within the community it is
desirable that they be expressed as log
rates. Implicit in the model is the notion
that a given consumer species draws its
energy from one or more trophic levels and
pumps a certain fraction of this energy
(5-10%) to the next higher level or levels.
91
NUTRITION AND SECONDARY PRODUCTION
Consumer
Trophic
level
B
Species
D
A.
A.
—n!
A,
A.
A,
FIG. 2. Model of the ecosystem showing sources of
energy for the various consumer species in relation
to trophic levels. Category A includes various microorganisms which, for convenience, have been
lumped into three groups (those which derive
energy entirely from breakdown of vegetation, those
which receive their energy by attacking certain
chemical bonds common to both plants and animals, and those which specialize on certain compounds present mostly in animal matter). Category
A should probably equal the widths of all the
remaining categories combined. Category B in-
Unused materials are returned as wastes
to the levels from which they came, and a
large portion of the energy is dissipated
through respiration and loss of frictional
heat.
In preparing the model, an effort has
been made to illustrate the common pattern of organization of the nutritional community referred to above, as discerned by
the present writer. The illustration incorporates the following facts: Certain
species tend to specialize, others to generalize. For each type of consumer there are
approximate equivalents. On the whole,
the most successful species are those which
obtain energy from the lowest levels and
those which generalize, and these two cate-
cludes mostly zooplankton (and a few benthic)
species which harvest the phytoplankton, but which
also take in a certain quantity of other microorganisms. Category C includes detritus feeders
(which are presumed to derive more nourishment
from the microbes than from the substrate) as well
as certain browsers on the zooplankton. Category
D includes the higher predators repesenting both
the broad multivores and the specialists, but for all
of which the energy sources must be allocated to
the proper trophic levels.
gories likewise contain the largest numbers
of species. The highest predators are represented by the lowest rates of energy flow
(and the smallest populations), as well as
the lowest diversity of species.
The difficulty with this or any other
trophic model lies in the allocation of intake energies to specific trophic levels. This
can be accomplished only through a painstaking series of food studies carried out by
methods suggested earlier, and building up
the community relations from the lower
levels on up. In the meanwhile the model,
as proposed, is available for computermanipulation, and it is specifically desirable that various combinations of species
be tested for maximum community stabil-
92
REZNEAT M. DARNELL
ity. This must be the goal toward which
the evolution of the community tends.
REFERENCES
Bajkov, A. D. 1935. How to estimate the daily food
consumption of fish under natural conditions.
Trans. Am. Fisheries Soc. 65:288-289.
Baldwin, N. S. 1956. Food consumption and growth
of brook trout at different temperatures. Trans.
Am. Fisheries Soc. 86:323-328.
Barrington, E. J. W. 1942. Gastric digestion in the
lower vertebrates. Biol. Rev. 17:1-27.
Barrington, E. J. W. 1957. The alimentary canal
and digestion, p. 109-161. In M. E. Brown, [ed.],
The physiology of fishes, vol. 1. Academic 1'ress,
Inc., New York.
Bitterman, M. E., J. Wodinsky, and D. Candland.
1958. Some comparative psychology. Am. J.
Psychol. 71:94-110.
Bowen, E. S. 1931. The role of the sense organs in
aggregations of Ameiurus melas. Ecol. Monographs 1:1-35.
Brown, M. E. 1951. The growth oE brown trout
{Salmo trutta Linn.). J. Exptl. Biol. 28:473-491.
Childers, W., and H. H. Shoemaker. 1953. Time of
feeding of the black crappie and the white crappie. Trans. Illinois Acad. Sci. 46:227-230.
Darnell, R. M. 1958. Food habits of fishes and
larger invertebrates o£ Lake Pontchartrain, Louisiana, an estuarine community. Publ. Inst. Marine Sci., Univ. Texas 5:353-416.
Darnell, R. M. 1961. Trophic spectrum of an
estuarine community, based on studies o£ Lake
Pontchartrain, Louisiana. Ecology 42553-568.
Darnell, R. M. 1964. Organic detritus in relation
to secondary production in aquatic communities.
Verh. Intern. Verein. Limnol. 15:462-470.
Darnell, R. M. 1967a. The organic detritus problem. Estuaries, AAAS Publ. 83:374-375.
Darnell, R. M. 1967b. Organic detritus in relation
to the estuarine ecosystem. Estuaries, AAAS Publ.
83:376-382.
Darnell, R. M., and R. R. Meierotto. 1962. Determination oE feeding chronology in fishes. Trans.
Am. Fisheries Soc. 91:313-320.
Darnell, R. M., and R. R. Meierotto. 1965. Diurnal
periodicity in the black bullhead, Ictalurus melas
(Rafinesque). Trans. Am. Fisheries Soc. 94:1-8.
Dawes, B. 1930. The absorption oE fats and lipids
in the plaice. J. Marine Biol. Assoc. U.K. 17:
75-102.
Edmondson, W. T. 1957- Trophic relations of the
zooplankton. Trans. Am. Microscop. Soc. 76:
225-245.
Elton, C. 1927. Animal ecology. Sidgwick and
Jackson, London. 207 p.
Frankenberg, D., and K. L. Smith, Jr. 1967. Coprophagy in marine animals. Limnol. Oceanog.
12:443-450.
Gerking, S. D. 1955. Influence of rate of feeding
on body composition and protein metabolism of
bluegill sunfish. Physiol. Zool. 28:267-282.
Ccrking, S. D. 1962. Production and food utilization in a population of bluegill sunfish. Ecol.
Monograph 32:31-78.
Harrington, R. W., and E. S. Harrington. 1961.
Food selection among fishes invading a high subtropical salt marsh; from onset of flooding
through the progress of a mosquito brood. Ecology 42:646-666.
Hathaway, E. S. 1927. The relation of temperature
to the quantity of food consumed by fishes.
Ecology 8:428-433.
Hungate, R. E. 1960. Microbial ecology of the
rumen. Bact. Rev. 24:353-364.
Hunt, B. P. 1960. Digestion rate and food consumption of Florida gar, warmouth, and largemouth bass. Trans. Am. Fisheries Soc. 89:206-211.
Hynes, H. B. N. 1950. The food of fresh-water
sticklebacks (Gasterosteus aculeatus and Pygosteus
pungitius), with a review of methods used in
studies of the food of fishes. J. Animal Ecol.
19:36-58.
Ivlev, V. S. 1961. Experimental ecology o£ the
feeding of fishes. Yale Univ. Press, New Haven.
302 p.
Johannes, R. E., and M. Satomi. 1966. Composition and nutritive value of fecal pellets of a
marine crustacean. Limnol. Oceanog. 11:191-197.
Karpevitch, A., and E. Bokoff. 1937. The rate of
digestion in marine fishes. Zool. Zhur. 16:28-44
(Russian; English summary.)
Karzinkin, G. S. 1935. Toward knowledge of the
fish productivity of waters. II. Report. Investigation of the nutritional physiology of the mirror
carps. Kossino Limnol. Sta. 19:21-66. (Russian;
German summary.)
Kinne, O. 1960a. Die Wirkung verschiedener Urnweltfaktoren auf die Nahrungskonversion bei
einem Knochenfisch. Naturwissenschaften 22:
525-526.
Kinne, O. 1960b. Growth, food intake, and food
conversion in a euryplastic fish exposed to different temperatures and salinities. Physiol. Zool.
33:288-317.
Kinne, O. 1963. t)ber den Einfluss des Salzgehaltes
auf verschiedene Lebensprozesse des Knochenfisches Cyprinodon macularius. Veroff. Inst.
Meeresforsch. Bremerhaven, Sonderbd. Drittes
mecresbiol. Symposium 49-66.
Krogh, A. 1931. Dissolved substances as food of
aquatic animals. Biol. Rev. 6:412-442.
Lasker, R. 1960. Utilization of organic carbon by
a marine crustacean: analysis with carbon-14.
Science 131:1098-1100.
Le Cren, E. D. 1962. The efficiency of reproduction
and recruitment in freshwater fish, p. 283-296.
In E. D. Le Cren and M. W. Holdgate, [ed.], The
exploitation of natural animal populations.
Blackwell Sci. Publisher, Oxford. 399 p.
Lehninger, A. L. 1965. Bioenergetics. W. A. Benjamin, Inc., New York. 285 p.
Lindeman, R. L. 1942. The trophic-dynamic aspect
of ecology. Ecology 23:399-418.
NUTRITION AND SECONDARY PRODUCTION
Markus, H. C. 1932. The extent to which temperature changes influence food consumption in the
largemouth bass (Jiuro floridand). Trans. Am.
Fisheries Soc. 62:202-210.
Marshall, S. M., and A. P. Orr. 1955. On the biology of Calanus finmarchicus. VIII. Food uptake,
assimilation, and excretion in adult and stage V.
Calanus. J. Marine Biol. Assoc. U.K. 34:495-529.
McWhinnie, M. A., and R. Johanneck. 1966. Utilization of inorganic and organic carbon compounds by Antarctic zooplankton. Antarctic J.
of the U.S. 1:210.
Menzies, R. J. 1962. On the food and feeding
habits of abyssal organisms as exemplified by the
Isopoda. Intern. Rev. Ges. Hydrobiol. 47:339358.
Minshall, G. W. 1967. Role of allochthonous detritus in the trophic structure of a woodland
springbrook community. Ecology 48:139-149.
Molnar, G., and I. Tolg. 1962. Relation between
water temperature and gastric digestion of largemouth bass (Micropterus salmoules Lacepede).
J. Fisheries Res. Board Canada 19.1005-1012.
Moore, W. G. 1941. Studies on the feeding habits
of fishes. Ecology 22:91-96.
Nelson, D. J., and D. C. Scott. 1962. Role of detritus in the productivity of a rock-outcrop community in a piedmont stream. Limnol. Oceanog.
7:396-413.
Newell, R. 1965. The role of detritus in the nutrition of two marine deposit feeders, the prosobranch Hydrobia ulvae and the bivalve Macoma
balthica. Proc. Zool. Soc. London 144:25-45.
Nordenskiold, E. 1942. The history of biology.
Tudor Publ. Co., New York. 629 p.
Pearse, A. S. 1924. Amount of food eaten by four
species of freshwater fishes. Ecology 5:254-258.
Pillay, T. V. R. 1953. Studies on the food, feeding
habits, and alimentary tract of the grey mullet,
Mugil lade Forskal. 1'roc. Nail. Inst. Sci. India
19:777-827.
93
Piilter, A. 1909. Die Eniiihrung der Fische. Zeit.
Allgem. Physiol. 19:147-242.
Ricker, W. E. 1946. Production and utilization of
fish populations. Ecol. Monographs 16:373-391.
Riddle, O. 1909. The rate of digestion in coldblooded vertebrates—the influence of season and
temperature. Am. J. Physiol. 24:447.
Rozin, P., and J. Mayer. 1961. Regulation of food
intake in the goldfish. Am. J. Physiol. 201:968.
Rozin, P., and J. Mayer. 1964. Some factors influencing short-term food intake of the goldfish.
Am. J. Physiol. 206:1430-1436.
Scott, D. 1965. The determination and use of
thermodynamics data in ecology. Ecology 46:
673-680.
Seaburg, K. G., and J. B. Moyle. 1964. Feeding
habits, digestive rates, and growth of some Minnesota warmwater fishes. Trans. Am. Fisheries Soc.
93:269-285.
Stephens, G. C. 1967. Dissolved organic material
as a nutritional source for marine and estuarine
invertebrates. Estuaries, AAAS Publ. 83:367-373.
Stephens, G. C, and R. A. Schinske. 1961. Uptake
of amino acids by marine invertebrates. Limnol.
Oceanog. 6:175-181.
Surlier, E. W. 1935. Trout feeding experiment with
natural food {Gammarus jasciatus). Trans. Am.
Fisheries Soc. 65:300-304.
Tugendhat, B. I960. The normal feeding behavior
of the three-spined stickleback (Gasterosteus aculealus L.). Behavior 15:285-318.
Webster, D. A. 1942. Food progression in young
white perch (Morone americana (Gmelin)) from
Bantam Lake, Connecticut. Trans. Am. Fisheries
Soc. 72:136-144.
Wigley, R. L., and R. B. Theroux. 1965. Seasonal
food habits of highlands ground haddock. Trans.
Am. Fisheries Soc. 94:243-251.
Windell, J. T. 1966. Rate of digestion in the bluegill sunfish. Invest. Indiana Lakes and Streams
7:185-214.