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AM. ZOOLOGIST, 8:53-59 (1968).
Secondary Productivity in Terrestrial Communities
FRANK B. GOLLEV
Institute of Ecology and Department of Zoology, University of Georgia,
Athens, Georgia 30601
SYNOPSIS. Secondary productivity is one portion of energy flow in a community, which includes
the ingestion and assimilation of energy, and the expenditure of energy in metabolism by consumer organisms. The purpose of this paper is to describe the ecological significance of energy
flow in consumers and to discuss methods of measuring its components. Data pertaining to 20
terrestrial animal populations are presented. About 20% of the energy assimilated by invertebrates is manifested as net production, while only about 2% of the assimilated energy is represented by net production in populations of birds and mammals. The relationship between production and metabolism appears to depend on the capacity for homeothermy. For a given
amount of assimilated energy, homeotherms produce less than heterotherms.
The ecologist defines secondary productivity as the net quantity of food or energy
ingested that is transferred to the tissue of.
heterotrophs over a period of time. It is
one component of the energy flow process
diagramed in Figure 1. Secondary productivity is expressed as an increase in biomass,
e.g., as growth, deposition of fat, or birth of
young. The ecologist is interested in this
parameter because it is an index to the significance of a population in terms of food
resources made available to other predatory
populations in the food-chain. Applied
fields, such as animal husbandry and wildlife management, seek to increase the total
output and the extent of utilization of
secondary productivity by man.
The concepts of food-chain and food-web
are central to the study of secondary production. The energy flow diagram in Figure 1 need only be expanded to illustrate
SECONDARY PRODUCTION
ASSIMILATED ENERGY
ING
^WA
METABOLISM
•uiINASSIMILATED
ENERGY
FJG. 1.
the food-chain: with herbivores eating
plants, and carnivores feeding upon herbivores. But the food-chain is a simplification of the actual trophic relationships
found in most natural communities.
Heterotrophic populations feed on the net
primary productivity of plants and on the
secondary production of other consumer
populations in a complex web. The full
skein of feeding relationships has never yet
been described for any terrestrial community, but we know from the diversity of
communities that food-webs may be extremely complicated.
The diagram of energy flow makes it
clear that secondary production is but one
of a series of interrelated processes. For this
reason secondary production cannot be considered alone. Within a population we
must consider the energy cost of metabolism because this expenditure competes
with secondary productivity. The assimilated energy represents the total energy
budget of the population, and it is conventional to consider that all of this energy is
utilized either in metabolism or expressed
in some form of production. In some studies it may be useful to consider the amount
of energy which is ingested but not assimilated. Although this energy may be changed
in state, it does not enter the energy budget
of the consumer and is merely hastened to
eventual exploitation by decay organisms.
For the study of energy flow and secondary productivity we require two kinds of
information: (1) a census of the energetically significant members of the population of
species over an appropriate period of time,
and (2) an estimate of the separate energy
components for each single population. We
consider methods of obtaining these kinds
of information below.
CENSUS OF THE POPULATION
Methods of censusing animals are almost
53
54
FRANK B.
TABLE 1. Caloric values and ash content of various
stages of the meadow spittlebug (Philaenus spumarius). Data from Wiegert (1965).
Ash
Stage
cal/ash-free gram
% dry weight
6503
4976
5674
5801
5780
5902
5625-6116
3.1
8.1
7.0
6.1
4.3
3.2
Eggs
1st Instar
2nd "
3rd "
4th "
5th "
Adults
0.1-2.1
as varied as the species of animals themselves. Unfortunately, few techniques give
absolute estimates of abundance in a unit
area. The most successful of these utilize
some peculiarity of the species which permits a count of all the animals over successive time periods. Sessile, slow-moving, or
social animals, and those large or conspicuous enough to be recognized visually may
all be censused fairly completely. In studies of energy flow, we are specifically interested in the dynamics of components of
the population which are energetically significant. The age structure of the population is often of great importance. For example, Wiegert (1965) has shown that the
different stages in the life history of the
meadow spittlebug have different caloric
values (Table 1). In this species the ontogenetic range in caloric content was as
great as that observed in 17 different species
of animals (Slobodkin and Richman, 1961).
Different age groups may vary in their capacity for assimilation. Phillipson (1960)
showed that, in the phalangid Mitopus, the
energy assimilated from ingested material
was 74% for instar II but only 44% for
instar VI (Table 2). Because the early instars could not tear up the hard parts of
their prey, the food entering their guts was
TABLE 2. Assimilation of collembolan food by instars of the phalangid, Mitopus mono. Data from
Phillipson (1960).
Instar
Pood Intake
( m g)
II
III
IV
V
"VT
VII
0.129
0.229
0.357
1.069
1.539
—
%
Feces (mg) Assimilation
0.035
0.095
0.162
0.484
0.862
74
59
55
55
44
47
GOLLEY
made up largely of highly digestible fat and
muscle. In both of the foregoing examples
a gross census of numbers would have concealed important variability in the energetically significant portions of the population.
In addition to an enumeration of total
numbers, we usually need the weight distribution of the population. This is because energy flow is usually described in
terms of body weight (i.e., as cal/g). The
distribution of ages and weights varies during the year, so a series of censuses is usually required.
INTAKE OF ENERGY
Intake of energy may be determined directly by field observations or by measuring food consumption in the laboratory.
In laboratory experiments ecologists have
devised ingenious techniques to provide
organisms with suitable conditions and
foods. In these investigations, the food is
simply weighed before eating commences
and after feeding has been completed. The
difference in weight indicates the amount
of food consumed. Of course, there are
problems of waste and change in weight of
food due to evaporation of water. As
Odum, et al. (1962) have suggested, an advantage of the feeding technique is that
the food can be concentrated in a small
area while the animal is allowed to roam
throughout a large cage. Thus, patterns of
activity may be more natural.
There are also indirect ways to determine intake of food. F'or example, the
ratio of a natural or introduced tag in the
food to that appearing in the animal or
in its feces may be used to estimate intake.
An interesting experiment illustrating this
approach with a beetle (Chrysomela knabi)
was reported by Crossley (1966). The tag
used was the radioactive isotope Cs137,
which occurred in both plants and beetles
in a contaminated area. The amount of
tag in the food and beetles was determined
by conventional counting techniques, and
the elimination of Cs137 from the beetles
was determined in the laboratory. These
measurements permitted Crossley to estimate the intake of food (Table 3), with
TERRESTRIAL SECONDARY PRODUCTIVITY
55
TABLE 3. Determination of food consumption by third instar leaf beetles (Chrysomela knabi).
Data from Crossley (1966).
Statistics
Mean Valne
Elimination constant (fc)
Concentration in larvae in the field (§)
Larval rate of intake of Cs (r)
Concentration in plant in the field
Larval feeding rate on plant
Mean weight of larvae
Larval feeding rate on plants
Feeding rate determined in laboratory
the formula:
where r is the rate of feeding, k is the fraction of radioactivity eliminated per day,
and Qa is the concentration of radioisotope
in the organic material at equilibrium concentration. The rate calculated by this
method was 9.2 mg plant/larva/day.
Crossley also measured intake of food in
the laboratory using conventional weighing
techniques and found that the consumption was about 9 mg plant/larva/day.
Other ratio-techniques use naturally occurring, non-radioactive chemical indicators.
ASSIMILATION OF ENERGY
Not all the energy that is ingested is
assimilated by the animal; some of the food
is indigestible, and this portion is egested.
For practical purposes the difference between the energy ingested and that defecated is assimilated energy. But there may
be problems—especially in measuring excretions. Wastes excreted through the kidneys have been assimilated and should not
be subtracted from food-intake, yet often
kidney excretions cannot be separated from
egestions from the digestive tract. Not all
of the feces are undigested material;
glandular secretions, cells from the gut wall
and microorganisms also occur in the feces.
These problems are best handled by an independent description of what excreta do
and do not include for each species studied. It should also be recalled that these
wastes form a source of food for other organisms in the community.
METABOLISM
The investigation of the energy expendi-
2.08 per
day
62 pe1"mCs/g larva
129 pe Cs/g larva/day
43.3 pcOT Cs/g plant
2.98 g plant/g larva/day
3.1 mg
9.2 mg plant /larva/day
~ 9 mg plant/larva/day
ture of individual organisms under laboratory conditions has been highly developed,
and there is a large volume of information
available for animals of various sizes and
physiological conditions. While these data
are of use to the ecologist, we seldom know
the extent of the energy metabolism of freeliving animals. Hence, we must extrapolate
from laboratory to field conditions. This
is not a particularly serious problem with
small organisms because the natural environment of these species can be simulated
reasonably well in the laboratory. Estimating the metabolism of large animals is more
difficult because we must often greatly restrict their activity.
Investigators may measure consumption
of O2 in the laboratory, convert this value
to energy using standard values, and then
extrapolate to the field from the laboratory
conditions. Grodzinski and Gorecki (1967)
suggest that this is an accurate way to determine the utilization of energy by small
mammals. They found that small mammals are active for only 20-25% of the day,
and that energy metabolism in nature is
significantly influenced by environmental
temperatures, pregnancy and lactation,
huddling, etc. These phenomena can be
measured in the laboratory.
Other workers have suggested that activity has a more important influence on metabolism, and have initiated studies to estimate metabolism in the field. Some investigators have attempted to calculate rate
of metabolism from the rate of excretion
of a radioisotope (Odum and Golley, 1963;
Reichle, 1967). The use of D2O18 to measure CO2-output and energy metabolism
may be a useful way to measure respiration
directly in the field. In the most successful
56
FRANK B. GOLLEY
application of this technique, LeFebvre
(1964) determined that the energy cost of
flight in homing pigeons flying several hundred miles was about seven times that at
rest. Other investigators who have studied
the energy expense of flight argue that such
a high output of energy would not permit
migration over long distances. Therefore,
the factor of 7 cannot be extended to birds
generally. Further data are obviously
needed.
SECONDARY PRODUCTION
Secondary production is simply expressed
as the growth (increase in biomass) of the
population if both prenatal and postnatal
growth are considered. If only postnatal
growth is measured, then the biomass of
newborn animals must be added to the
total. If the population is in equilibrium,
secondary production is also equivalent to
the caloric equivalent of all individuals
dying (yield) during a selected interval of
time. In other words, whatever increase in
biomass is realized by growth will also
eventually show up in the weight of animals removed from the population, whether by predation or natural death. A more
general expression of secondary production,
applicable to non-equilibrium situations is:
net production rr yield ± caloric equivalent of change in standing crop
Thus, if the standing crop declines during
the period of investigation the second term
is negative; if there is an increase in standing crop the second term is positive. This
formulation was used by Teal (1957), although he did not state it explicitly.
Secondary production is one of the more
easily measured components of energy flow.
It only requires successive weighing of individuals or cohorts from the time of conception or birth to adulthood or death. It
organisms can be marked and recaptured,
secondary production can be measured directly in the field. If age groups can be
identified, it is also possible to follow
change in weight of these groups over time.
In this way the growth of an entire cohort
can be determined. Secondary production
is also one of the energy parameters most
TABLE 4. Annual growth in one age group of the
terrestrial isopocl, Ligidium japoiiica. Data from
Saito (1965).
Date
Xumber of
Individuals
Mean Body
Weight (mg)
Growth
(mg/nr)
Aug.
Sept.
Oct.
Xov.
JJec.
Jan.
Feb.
March
April
May
.Tune
July
Aug.
1380
3 050
800
610
460
360
275
235
165
130
100
76
0.8
1.4
3.7
3.9
1.9
3.9
3.9
3.9
2.0
2.2
7.6
12.5
14.0
828
364
185
0
0
0
0
25
38
797
564
132
responsive to changes in the environment
or in the structure of populations. For this
reason secondary production may be highly
variable from one season or year to the
next. An interesting example of seasonal
change in secondary production was given
by Saito (1965) for a terrestrial isopod
(Table 4). Growth was maximal after
hatching and also vigorous almost a year
later in the summer. There was no growth
during winter. Saito added the growth of
the age group shown in Table 4 to that oC
other age cohorts and the new isopods born
to obtain the total production of the population.
COMPARISONS OF FIliLO POPULATIONS
Over the past few years a number of investigators have examined the energy flow
in natural populations. A comparison of
their findings may reveal general relationships between species, which will in turn
stimulate and direct further examination of
other populations. In evaluating the energ)' dynamics of diverse populations we
can compare parameters of energy flow directly, or we can examine ratios between
the components. Selected data for natural
terrestrial and estuarine populations are
given in Table 5. The standing crop is a
crude measure of the population since it
represents only the average quantity of energy stored in the population over a year.
The range in standing crops shown in
Table 5 is great. The planthopper (Prokelisia) and the snail (Littorina) in a
57
TERRESTRIAL SECONDARY PRODUCTIVITY
TABLE 5. Selected 2data on cntrgy floic from natural population* of terrestrial and cstuarine
animals (Kcal/m /ycar). Data from Wiegrrt and Evans (1967) and Engchnann (1966).
BERBIVOSES
Spittlebugs
Grasshoppers
Grasshoppers
Orthoptera
Harvester aiit
Plaiithoppers
Savannah sparrow
Sparrows
Deermice
Old field mouse
Ground squirrels
Meadow vole
Elephant
CARNIVORES
Marsh wren
Weasel
DETRITIVOBES
Oribatid mites
Isopod
Mussel
Nonia.todes
Snail
Standing Crop
Metabolism
0.14
0.16
0.80
0.86
19.0
21.6
30.9
205.0
3.8
0.40
0.22
24.1
0.03
0.05
0.003
0.02
0.05
0.19
7.10
0.002
0.011
.—
3.80
18.41
—
3.6
2.29
0.62
6.6
3.69
17.0
23.0
88.3
0.54
1.58
16.0
39.0
64.0
249.4
Georgia salt marsh exhibited extremely
large standing crops and high levels of assimilation, metabolism, and production.
Generally, secondary production is greater
in the invertebrate herbivores and decomposers than in vertebrate herbivores and
carnivores.
Two related ratios which may be derived
from Table 5 are of special interest. These
are (1) the ratio of metabolism to assimilation, and (2) the ratio of production to
metabolism. An average of about 90% of
assimilated energy is used in metabolism,
but vertebrates use proportionally more of
their available energy in metabolism (ca.
98%) than do invertebrates (ca. 79%). As
Engelmann (1966) has pointed out, this
difference also implies that invertebrates
invest a greater proportion of their assimilated energy in production of new biomass.
A plot of the data in Table 5 (Fig. 2) illustrates this distinction more clearly (see also
Engelmann, 1966, p. 105). The one point
which seems to be inconsistent with the
general pattern is for the ant, Pogonomyrmex hadius (see Golley and Gentry, 1964).
If this species is omitted, a comparison of
the slopes of lines drawn through the data
Secondary
Productivity
0.08
0.51
11.0
4.0
0.09
70.0
0.04
0.05
0.01
0.12
0.11
0.52
0.34
0.4
0.013
0.43
3.5
16.7
21.0
40.6
Assimilated Productivity X
100/Assiniilation
Energy
0.88
1.37
30.0
25.6
31.0
275.0
3.6
9.1
37.2
36.6
15.6
0.3
25.5
3.S0
17.52
23.3
1.1
2.1
1.6
1.8
2.9
3.0
1.5
8S.7
0.55
0.5
2.4
2.01
19.5
56.0
21.4
17.9
29.8
24.7
14.0
2.34
0.63
6.7
85
290
points for vertebrates and invertebrates
yields a £-value of 1.328, with 15 degrees of
freedom. This value is significant at the
90% level but not at the 95% level. However, the data in Figure 2 exhibit a curvilinear (rather than linear) relationship,
and the pattern merits further analysis.
The data in Table 5 have been discussed in
terms of vertebrates vs. invertebrates, but
as Engelmann (1966) pointed out, a more
meaningful distinction is probably homeothermy 7/5. heterothermy. Recent work by
Turner (personal communication) indicates that the ratio of production to assimilation in the lizard, Uta stansburiana, is
about 80-85%, a proportion generally similar to that exhibited by invertebrates.
SECONDARY PRODUCTION IN TERRESTRIAL
LABORATORY POPULATIONS
There have been several studies of the
dynamics of confined populations in the
laboratory and, with knowledge of the body
weight of the animals, the data from these
studies may be converted to production of
biomass. Petrusewicz (1963) adopted this
approach in his study of confined populations of protozoans, insects, and mammals.
58
FRANK B. GOLLEY
total increase in biomass. The weight of
individuals dying in the population may
also be considered an estimate of secondary
production; however, this statistic does not
account for losses of weight during the life
of the individual. The difference between
total increase in weight and total weight at
o
0
0
death is due to the fact that total increase
0
in weight is the sum of all positive increases
in weight measured at intervals of one
month (including gain of weight after
weight-loss). Secondary production in this
study was the total increase in weight minus
weight-losses, and it ranged from 86.1 to
88.8% of the total increase in weight. While
FIG. 2. The relationship between metabolism and
secondary production varied greatly besecondary production (Kcal/m2/year) for populatween populations, on a per capita basis it
tions of vertebrates (open circles) and invertebrates
was essentially constant between popula(solid circles). The invertebrate point at upper left
is for the harvester ant (Pogonomyrmex badius).
tions (6.5 to 7.3 grams per individual).
He concluded that decrease in production
As far as I know there has been but one
is directly associated with increase in the study of the energy flow in a confined popusize of the medium or habitat. Later, Wal- lation of a terrestrial animal. Brown (1963)
kowa and Petrusewicz (1967) evaluated sec- studied two populations of laboratory mice,
ondary production directly in confined one during the phase of early growth and
populations of laboratory mice (Table 6). the second after growth had ceased. MeFour populations, each started with 10 tabolism was measured by confining indimales and 10 females, were observed for viduals removed from the population in
182 weeks. These populations lived in respirometers for a period of about one
cages 6.15 m2 in extent. These investigators hour. Secondary production was measured
measured loss of body weight of individ- by weighing the mice daily. The growing
ual mice, weight of mice dying in the popu- population exhibited some secondary prolations, and increase in body weight, so duction, while the denser population acproduction can be considered from several tually lost energy through loss of weight
points of view. The sum of all increases (Table 7). In the growing population the
in weight is an overestimate of secondary ratio of production to assimilation was
production because it assumes that produc- 3.1%, a value only slightly greater than
tion is always positive. Loss of weight, at that determined for free-living populations
least in mammalian populations, seems to of mammals. Brown also examined the
be important since the animals may use partitioning of energy flow by sex and age
body tissue when environmental conditions group and the influence of behavior. In
are suboptimal. In the populations studied the growing population, 24% of the enby Walkowa and Petrusewicz, loss of body ergy flow went to immature mice. In the
weight ranged from 11.2 to 13.8% of the dense population all energy was used by
TABLE 6. Secondary production (g) in confined mouse populations. Data from Walkowa and
Petrusewicz (1967).
Population
Original
Weight
Loss of Weight
Weight of
Dead Mice
Total Increase
in Weight
Secondary
Production
1
2
3
4
346
367
368
357
1,017
1,963
2,098
3,147
7,303
11,593
14,872
22,998
8,162
14,169
16,910
28,087
7,145
12,206
14,812
24,941
59
TERRESTRIAL SECONDARY PRODUCTIVITY
TABLE 7. Summary of energy flow (Kcal/day) in a confined house mouse population. Data from
Brown (196S).
Number of Mice Assimilation
Growing population
Dense population
26
110
323.6
2262.8
adults because no new mice were added to
the population. In the growing population,
32% of the energy budget was directly related to territoriality and status-maintaining behavior, while in the dense population 45% of the energy was used in this
manner. Brown concluded that, as density
increased, intensification of social interactions exacted an ever-increasing toll of the
total energy flow until none was available
for recruitment.
CONCLUSIONS
Secondary production can be measured
directly in many field populations and is
responsive to environmental influences as
well as to changes in structure of the population and behavior. The available data
strongly suggest that the ratio of secondary
production to metabolism is greater among
invertebrates than among birds and mammals. This difference is not unexpected
because homeotherms under laboratory
conditions exhibit a higher metabolic rate
per gram of body weight than do heterotherms. The ratio of secondary production
to metabolism is an important ecological
parameter because it influences the amount
of energy available to other trophic levels
of the community.
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Brown, R. Z. 1963. Patterns of energy flow in populations of the house mouse (Aftw musculus). Bull.
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Engelmann, M. D. 1966. Energetics, terrestrial field
studies, and animal productivity, p. 73-115. In
J. B. Cragg, [ed.], Advances in ecological research.
Academic Press, London and New York.
Metabolism
Secondary
Production
Production
Assimilation
%
312.8
2268.3
+ 10.8
— 5.5
3.1
0.0
Golley, F. B., and j . B. Gentry. 1964. Bioenergetics
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