Download Quantitative Aspects of Insect Nutrition Division of Entomology

A M . ZOOLOGIST, 8:131-138 (1968).
Quantitative Aspects of Insect Nutrition
HAROLD T. GORDON
Division of Entomology, University of California, Berkeley 94720
SYNOPSIS. The small size of insects, correlated with high food-consumption, growth, and
metabolic rates, makes possible their high efficiency of food-utilization, short life cycles, high
biotic potential, and rapid genetic adaptation and speciation. Most of the qualitative nutritional
requirements are known for many insect species; many essential nutrients are provided by microbial symbiotes. Recent studies in quantitative nutrition make possible more detailed analysis
of the utilization of food, of the kinetics of growth and metabolism in intact animals, and of
the controlling mechanisms in the animal-food interaction.
The classical period of research in insect
nutrition owes much to G. Fraenkel, who
made careful measurements of the relation between growth and composition of
food. He used larvae of beetles and moths
that infest stored foods such as flour and
are easily reared on dry solid diets (Fraenkel, et al., 1941, and many subsequent
papers reviewed by Trager, 1953). Later
investigations extended to orthopterans
such as cockroaches and locusts, which also
require a water supply (Gordon, 1959;
Dadd, 1960). The refinement of axenic
techniques finally made possible the nutritional analysis of many holometabolous
forms that require a semi-liquid diet that
would be quickly spoiled by microorganisms (Sang, 1959; House, 1966; Rock and
King, 1967). These studies evolved not only
in the direction of conquering ever greater
technical difficulties but also of achieving
ever higher quality. Many of the more
recent papers are models of correct experimental design.
1947). Perhaps the most striking discovery
arising from these researches was the key
role of symbiotic microorganisms in providing various nutrients deficient in the
natural diets of many insects (Brooks,
1963).
This paper will necessarily be selective
rather than comprehensive in reviewing
recent quantitative work in insect nutrition. The data illustrate possible developments of the techniques and principles
of nutritional analysis, which may be applicable to work with all animals.
THE LOGIC OF QUANTITATIVE
NUTRITIONAL EXPERIMENTS
The criterion of nutritive value of a
food has always been near-normal growth,
development, and reproduction of the animal (preferably over several consecutive
generations, since body reserves of some
nutrients are large enough to permit normal development during one generation).
Although in much early work it was tacitly
These largely qualitative studies have assumed that poor growth indicated that
been frequently reviewed (House, 1965), one or more essential nutrients were lackand have shown that the dietary require- ing, studies on monophagous species have
ments of insects closely resemble those of shown that they may eat little or none of
other animals, except for the general ar- any food other than that on which they
thropodan requirement for a dietary sterol. feed in nature (Dethier, 1947), and it is
Some specialized species show additional now generally recognized that natural
requirements, such as that for ascorbic foods are not simple mixtures of nutriacid by many phytophagous species (Dadd, ents but also contain a variety of specific
1960; Ito, 1961), for proline by the silk- phagostimulants, phagodeterrents, growth
worm (Ito and Arai, 1965), and for hema- inhibitors and toxicants (Gordon, 1961;
tin by the blood-feeding hemipteran, Tria- Beck, 1965). If an animal fails to grow
toma infestans Klug (Lwoff and Nicolle, well on a certain food, many possible hy131
132
HAROLD T. GORDON
potheses (not mutually exclusive) may
account for this: (1) Food intake is abnormally low because (a) one or more
phagostimulants essential for normal feeding are deficient or (b) one or more phagodeterrents are present and in some way
inhibit the feeding reflexes. (2) Ingested
food is poorly digested because (a) the
animal lacks the requisite lytic enzymes
or (b) normal secretion or action of the
enzymes is inhibited by an antimetabolite.
(3) The absorption of one or more of
the nutrients is blocked by an antimetabolite, acting at any of many possible transfer sites. (4) Absorbed food cannot be
efficiently converted into body substance
because (a) one or more essential nutrients is deficient or (b) one or more antimetabolites are present and somehow interfere with efficient conversion. An excess of a nutrient can act as an antimetabolite in various ways.
Interpretation of the interaction between an animal and a potential food
source, therefore, requires measurement
of food-intake, excretion, and gain in
weight. However, measuring food-intake
and excretion not only augments the labor
of experiments but is often technically
difficult, especially for insects that live in
a liquid medium or require food (such as
plant leaves) that contain over 80% water.
Nevertheless, increasing awareness of the
importance of quantitative studies is driving insect physiologists and ecologists to
attempt complete balance sheets of the
flow of matter through insects. Such
studies are complicated by the fact that
from 60% to 90% of the live weight of
insects is water, of which a large fraction
may be formed by oxidative metabolism
but most of which is usually derived by
intake either with food or from a water
supply. It is possible to ignore such complex water-exchanges by expressing matter-flow on a dry-weight basis. The massbalance during a time interval of T days
can thus be represented by the equation
(1)
AW = AF — AS — AO
where AW is the dry weight gain, AF is
the dry-weight food-intake, AO is the oxi-
dative-metabolic weight-loss, and AS is the
solid excretion-loss. All parameters in the
equation except AO can be directly measured, although AO could be approximately calculated if the intake of oxygen and output of carbon dioxide during the period T were also measured.
Since the difference between AF and AS
is a rough measure of the quantity entering into the body metabolism, it can be
called Al (denoting inflow or input).
DEFINITION AND USE OF MASS-TIME RATES
Absolute values of parameters such as
AF or AW are of limited value in comparisons between experiments, since they
are dependent on the initial and final
body weights (Wi and W() and on the
duration, T, of the experiment. Since the
rate of increase in body weight tends to
be exponential rather than linear, one can
define an "exponential mean live weight"
as
AW
W. =
0.435-AW
(2)
where d is the ratio of dry body weight
to live weight.1 Relative mass-time rates
l The exponential mean weight is not the only
possible growth mean. The arithmetic mean,
(Wi +W f )/2, is very close to We when the increase
in body weight is less than 2-fold; however, when
W f > > W | , the arithmetic mean is approximately
W,/2, so that the early part of the growth interval
is given too little weight and calculated rates are
theoretically unsound. On the other hand, if
growth is linear (so that A W T is constant and G
rapidly declining), the exponential mean will not
yield an average of the successive daily rates over
a long time; but very large changes in weight at
a constant rate will seldom occur in a fast-growing
animal. Waldbauer (1964) and Soo Hoo and
Fraenkel (1966) computed a mean by an approximate integration of the area under the growth
curve (in gram-days) and dividing by the number of days. Their method requires several intermediate weighings between W, and Wf to define
the growth curve, but there is no need to compute a mean if its only function is to permit estimation of the mass-time since the integration step
does this. Calculated values of Waldbauer's "inte-
QUANTITATIVE INSECT NUTRITION
can then be calculated by dividing the
A terms by We • T, or better, by 0.001
We • T, which gives units of mg/g • day
so that numerical values tend to fall in
the convenient range of 1 to 1000. For
example, the rate of intake of food is
defined as
(3)
F = 1000 AF/ (We • T)
and analogous operations define the
growth rate (G, from AW), the rate of
oxidative mass-loss (O, from AO), the
rate of solid excretion (S, from AS), and
the rate of metabolic inflow (/, from Al).
The logic of using live body weight
to calculate We is that it is likely to be
a better measure of metabolically active
substance than the dry weight. Active
tissues usually have a high water content,
while storage or skeletal tissues are much
drier and so make a smaller contribution
to the live body weight.
Equation (1) can be transformed into
the rate equation
(4)
G — F — S — O=I— O
where F measures the impact of the animal on its food supply, I the total level
of metabolism, G the level of anabolism
(incorporation of matter into the organism), and O the level of catabolism. These
rates measure the activity of complex biochemical processes in precisely the same
way as Qo2. In fact, an approximate value
of O can be derived by multiplying the
Qo2 (as mm3/mg live weight/hr) by 18
for glucose or 19.7 for starch-oxidation
(both RQ 1.0), by 26.6 for protein-oxidation (RQ 0.91) or by 48 for oxidation of
fats (RQ 0.71).
A measurement of rate over a short
gral mean" for fourth-instar larvae of the tobacco
hornworm (7-fold increase in weight in 2 days) are
only slightly lower than the arithmetic mean (e.g.,
64.2 instead of 68.1) and much higher than the
exponential mean (53.0). This suggests that the
last phase of growth of some insects is relatively
linear, perhaps because of accumulation of nongrowing reserve material (more than 50% of the
dry weight of last-instar larvae may consist of fat).
Another possibility is that a period of rapid feeding and growth is followed by a period of slow
feeding and growth during a single instar (cyclic
or "staircase" growth-curve); this gives pseudolinearity over the whole instar.
133
interval of time may not hold over a
longer period, although Gordon (1967)
has shown that the rate of intake, F, of
pure sucrose in adult male German cockroaches agrees closely with the value predicted from the Qo2. Many insects show
strong circadian and other rhythms
(Michal, 1931; Harker, 1961), and Qo2
values are often much higher during the
early part of an instar than later (Slama,
1960). Meaningful measurements of rate
should, therefore, cover either a period of
several days or (in fast-growing animals)
weight-gains of several fold, or a complete
instar. Rates are sensitive to temperature
(except near the optimum where one exists), which must be controlled and specified. All these complications make it difficult to measure rates reproducibly.
If one divides one rate by another, the
dimension of time is lost. Such ratios,
often converted to percentages, are encountered in many research papers.
While G/F or G/I are of interest as measures of the efficiency of conversion of ingested or absorbed food into body matter,
such ratios can conceal significant similarities or differences in the actual rates
which are the underlying reality.
The symbols proposed here attempt to
simplify the as yet unstandardized terminology of quantitative nutrition, in the
hope that it may eventually attain the
simplicity and uniformity of the symbolic
notation of physics and chemistry. The
many versions now in use can create confusion. The "feeding efficiency ratio" commonly used in mammalian nutrition is
often denoted by the symbol, E, and is
equivalent to G/(d-F). Waldbauer (1964)
used two efficiency ratios: E.C.I., equivalent to 100 G/F, and E.C.D., equivalent
to 100 G/I. He used the "coefficient of
digestibility," CD., equivalent to 100 I/F,
which was called the "percentage utilization of food" by Hirano and Ishii (1962).
Many excellent quantitative studies deal
primarily with A values and ratios instead
of rates (Hirano, 1964; McGinnis and
Kasting, 1966). Such studies often include
analyses of nitrogen, fat, and carbohydrate
134
HAROLD T .
GORDON
TABLE 1. Rates of utilization of food for several species of insect.
w,
G/F
G
F
S
I
O
156
0.24
0.30
0.36
0.27
0.21
0.20
0.12
92
120
109
109
78
64
46
390
406
304
404
371
324
380
222
155
192
190
167
170
163
192
134
233
226
198
259
168
204
170
171
145
126
121
76
94
71
62
67
62
75
Lycopersicon esculentum
Solanum tuberosum
Taraxacum officinale
Antirrhinum majus
Nicandra physalodes
Prunus serotina
Malus floribnnda
Oryza sativa
57
47
57
58
60
15
21
15
23
151
202
260
170
194
134
108
177
214
44
66
93
68
78
47
37
92
137
117
126
167
102
116
87
71
75
77
60
79
110
44
56
72
50
60
54
0.1
0.37
0.23
0.22
0.34
0.31
0.10
0.20
0.08
0.11
0.13
75
573
245
328
253
Betula verrucosa
0.4
0.13
90
680
535
145
55
100% Y
1
20
0.44
0.34
0.33
0.24
0.28
0.16
0.19
0.11
0.16
0.13
0.11
0.04
0.16
0.03
0.37
0.21
0.26
0.11
42
13
97
38
(0)
(0)
97
38
55
25
41
14
123
59
(0)
(0)
123
59
82
45
35
8
20
124
51
107
55
165
70
303
200
(0)
124
51
107
55
83
35
82
50
97
83
66
39
63
41
89
43
87
49
56
26
49
42
81
81
41
31
47
Pood
Species of insect
1
Protoparce sexta
d = 0.11
(fourth instar)
27°-30° C
Prodenia eridanea2
(d = 0.11 ¥)
(fifth instar)
(W, sa 33 mg)
27° C
Chilo suppressalis"
d = 0.25
(larval life)
28° C
Croesus septentrionalis*
(d = 0.2 t)
(larval life)
21° C
Blattella germanica*
(d = 0.3)
(Y = yeast, S = sucrose, C = cellulose)
30° C
I/ycopersicon esoulentum
Solanum tuberosum
Solanum dulcamara
Taraxacum officinale
Arctwm minus
Verbascum thapsus
Phaseolus lunatus
50% Y, 50% S
1
25
25% Y, 75% S
1
21
1
17
1
16
1
11
12.5% Y, 87.5% S
12% Y, 38% S, 50% C
6% Y, 19% S, 75% C
25% Y, 75% S + 0.05%
cyeloheximide
25% Y, 75% S + 0.2%
cocaine
25% Y, 75% S + 0.05%
veratrine
1
5
1
21
1
18
6
27
9
33
8
16
2
25
8
16
5
97
83
66
39
63
41
(0)
(0)
(0)
82
35
227
150
(0)
(0)
(0)
(0)
(0)
(0)
36
Kef erences:
^Waldbauer
(1964)
2
Soo Hoo and Fraenkel (1966)
8
Hirano and Ishii (1962)
*Janda(1959)
" Gordon, H. T. (in preparation)
composition of the food, insect body, and
excreta. If these were transformed into
rates (e.g., FN, the product of F by the
ratio of nitrogen to total food weight),
our understanding of the trophic process
would be greatly enriched.
EXAMPLES OF RATE-ANALYSIS OF
INSECT NUTRITIONAL DATA
Table 1 presents data for a number of
insect species fed on various foods, all
calculated to fit the basic rate equation
(4). The larval stage of P. sexta feeds ex-
QUANTITATIVE INSECT NUTRITION
clusively on solanaceous plants such as
tomato or tobacco, but removal of the
maxillae of fourth-instar larvae causes
them to feed and grow on many normally
rejected plants (Waldbauer and Fraenkel,
1961). Replicate experiments with tomato
(L. esculentum) give values that can differ
by 25%. Such variability is not unusual
in nutritional data since there are so
many factors (including non-random human errors) that cannot be precisely reproduced. However, it does (or should)
discourage generalization from a single
experiment, even when it yields statistically significant differences. The first 3
listed plants (all in the Solanaceae) give
relatively high values of both I and G; the
3 non-solanaceous plants show decreasing
I values and even more rapidly decreasing
G values (related to the relative constancy
of O for all plants). The classical interpretation of these data would assume that
these values are primarily controlled by
the phagostimulant action of the food (determining F) and its digestibility (determining S) that together determine the
value of /; since part of I is required for
"maintenance" (O), the leftover is all that
is available for G. The very low F and S
for S. tuberosum would then signify low
palatability but high digestibility. It is
equally logical, however, to assume that
there are maximum rates for both G (about
110) and O (about 70), set by the capacity
of the metabolic system, which determine a
maximum / of about 180; when / attains
this rate, a feedback control depresses F
to prevent accumulation of unmetabolized
nutrients. Why, then, is / for A. minus only
126? Here we must invoke either a deficiency of some nutrient or the presence
of an antimetabolite, either or both of
which will depress G below its maximum.
The low value of / may nevertheless represent the highest rate at which the digestive products of A. minus can be metabolized, and this determines the relatively
low value of F. We can consider that
Waldbauer's experiments indicate the
action of antibiotic "nutritional inadequacy" factors, supplementing the anti-
135
phagic factor that would (in non-maxillectomized larvae) depress F to zero.
The much smaller polyphagous larva of
P. eridanea feeds and grows at about half
the rate of P. sexta, but has an O value of
the same magnitude although much more
variable (from 44 on potato to 110 on
tomato, both excellent host plants). This
casts doubt on the characterization of G
as a simple "maintenance metabolic rate."
The tomato plant may contain a large fraction of readily-oxidizable substrates, so
that 110 mg/g-day is a measure of the
capacity of armyworm metabolism to
"burn away" these substrates; this makes
possible a higher / and F. The data for C.
suppressalis on rice (its normal host plant)
show that O can attain very high levels;
this is mostly carbohydrate oxidation made
possible by the very high (31%) carbohydrate content of rice stems and necessary
by their very low (8%) protein content. It is possible that O will eventually
be analyzable into many components: a
basal (starvation?) catabolism, a growthenergy supply-catabolism related to G, an
excess-nutrient removal-catabolism influenced by food-composition, and a neuromuscular activity-catabolism.
The data for the hymenopteran larva,
C. septentrionalis, on beech leaves indicate
an even higher F than that of the three
lepidopterans, but 80% of this is rejected
in S so that / is only 145. The values of
G and O are rendered uncertain by the
fact that d was not given. This paper is
unique in that the author measured the
total O2-consumption during the experiment, from which one can calculate that
O must lie between the extremes of 64
(for carbohydrate oxidation) and 30 (for
fat oxidation). Since the RQ was constantly
0.8, the true value of O probably is in the
range of 40 to 50.
The data for B. germanica reveal the
effects of experimental variation of dietcomposition. Pure yeast contains 50% protein, far above the optimum dietary level,
so that a large fraction of the absorbed
amino acids must be destroyed. This relatively slow metabolism depresses O to 55.
136
HAROLD T. GORDON
In the three yeast-sucrose mixtures there
is little excess protein and O rises to about
85 (largely carbohydrate oxidation). The
limited intake of protein depresses G when
75% or more of the diet consists of sucrose,
because attainment of the maximum rate
of carbohydrate oxidation blocks the necessary rise in F. In these experiments S
was too small to measure and is assumed
to be zero. When 50% or 75% of cellulose
is added to the basal 25% yeast diet, all
the cellulose is excreted and S rises to high
levels; there is a marked depression of J,
most of which is related to the fall in
O. One possible explanation of this effect
is that F is limited by the high cellulose
S, and that a larger fraction of the reduced
I is taken by the "higher-priority" G metabolism; if this is correct, any reduction
of F (such as partial starvation) would
tend to increase the G/I efficiency ratio.
Growth inhibitors added to the 25%
yeast diet have quite different effects on
the rates. Cycloheximide (known to be
a strong inhibitor of protein synthesis) depresses G without much affecting O; the
consequence is a drastic fall in the G/F
ratio. Cocaine greatly depresses O but has
less effect on G, so the G/F ratio is increased. Veratrine strongly depresses both
G and O; this causes a relatively minor
fall in the G/F ratio. From the rate values
alone one cannot single out any one of
the hypotheses of section 2 as the major
determinant. If one also takes into account the data on composition of food,
however, one can infer that excess of either
yeast or of sucrose is acting primarily according to hypothesis 4. Excess cellulose
and also cocaine cause a low / and high
G/I, which is compatible with hypothesis
1-b. Veratrine may be acting both by 1-b
and 4-b, while cycloheximide is almost
surely 4-b.
The data on B. gcrmanica also show the
well-known tendency of all rates to decline
as the insect grows (increasing values of
W;, the initial weight), with G declining
much more rapidly than O. Janda (1959)
reported a gradual fall in Qo2, G, F, and S
during the growth of C. septentrionalis.
This can be considered as heterogonic
growth of metabolic systems, comparable
to the many examples of heterogony discussed by Huxley (1932). It suggests that
there are "growth enzymes" whose activity
declines as G falls. Even in the present
crude state of development, the analysis of
rates enables one to visualize the intact
animal in terms of a fairly small number of
"enzymatic clusters." Within each cluster
there is close meshing of function, so that
slowing of any one activity slows the whole
cluster. The meshing between clusters is
much looser; this permits recognition of
the G and O metabolic subunits. The recent analysis by Sacher (1967) of data on
rate vs. temperature for many insect species suggests that temperature exerts a differential effect on these subunits, especially
during the larval stage. Edwards (1946)
found that even in adults the Qo2 and its
temperature coefficient are higher the
lower the body weight; this supports the
view that complex factors generate the deceptively simple gross metabolic rates.
RATE OF CONVERSION OF FOOD INTO EGGS
There is much scattered information on
the production of insect eggs, since fecundity is a major parameter in population
dynamics. This is not readily convertible
into steady-state production-rates and is
seldom accompanied by data on foodintake. Since eggs are primarily filled with
reserve yolk and their formation is not a
true growth process (Telfer, 1965), the
term P may be used to denote rate of egg
production in mg/g • day. Data for the
milkweed bug, Oncopeltus fasciatus (Dallas), a highly fecund species commonly
reared in laboratories, suggests the order
of magnitude, P. An adult female may in
its lifetime lay about six times its own
weight of eggs, at a relatively constant P
as high as 90 mg/g • day. (Gordon and
Bandal, 1967); this is higher than the G
of about 75 mg/g-day for nymphal
growth, and suggests that conversion of
food into egg yolk is a faster and probably
more efficient process than its conversion
into living substance. The value of P is
137
QUANTITATIVE INSECT NUTRITION
lower when the bugs are fed on almonds
instead of milkweed seed, and lower still
when they are fed on hazelnuts (Johansson, 1958). Food quality, however, is only
one of the many factors involved. P seems
to be directly controlled by the endocrine
activity of the corpus allatum, which is
often cyclic and can be influenced by a
bewildering variety of external factors.
Genetic factors, including long-lasting maternal influences, also play a role (Spiess,
1954).
A trophic life-cycle (dealing with the
fate of all food consumed during the life
of one female) is completed by the growth
of the embryos and their emergence as firstinstar larvae. This is an area sadly neglected by nutritional analysis, although G
and O rates could be calculated from
changes in dry weight. There is much evidence that the food consumed by a female
exerts great influence not merely on her
fecundity but on the survival and growth
of her progeny.
COMPARATIVE SIZES AND METABOLIC RATES
OF INSECTS AND MAMMALS
The adult body weight of most insects
falls in the range of 10 to 10,000,000 micrograms. Terrestrial mammals fall in a range
1,000,000-fold larger. Values of G and O,
however, are not so strikingly different, and
it is primarily the small size of insects that
makes for the relatively short generation
times and high population densities that
underlie their rapid genetic adaptation
and extensive speciation. Every possible
food source (including other insects) is attacked by one or more insect species, often
with high specificity, speed, or efficiency,
although they have not successfully invaded
the sea where the Crustacea play much the
same ecological role.
The fact that terrestrial vertebrates have
successfully competed with insects for hundreds of millions of years proves that there
must be an intrinsic selective advantage in
relatively large body size. This may be
nothing more subtle than the ability of
the growing animal to range over a much
larger territory in the search for food or
to survive severe temporary climatic shocks,
but there may also be nutritional factors
the significance of which has not yet been
realized.
CONCLUSION
The intent of this paper has been to emphasize the value of simple techniques used
with intact animals in revealing some basic
principles of nutrition. Many insect species may serve as ideal experimental animals in this area of biology, just as the
fruit fly, Drosophila melanogaster, served
in the delineation of the principles of genetics. Unfortunately, insect nutrition so
far has dealt primarily with the larval
growth period (often with only a fraction
of this period) instead of the several successive generations required for the analysis of trophic equilibria. Although there
are many research workers, each group
studies one or more different species, so
that knowledge has become extensive but
fragmentary rather than intensive and complete. Therefore, from the increasing accumulation of facts there have not yet emerged
the integrating theories needed for nutrition to play its key role in quantitative
ecology.
In recent years the human technological
and population explosion, in reorienting
terrestrial ecology to increase man's share
of the food supply, has exerted intense
selective pressure on the insects. Those
species that quickly adapted to feeding on
agricultural crops have attained unprecedented population size, distribution, and
economic importance. Use of pesticides on
an enormous scale has selected many highly
resistant strains of these "economic" species and has upset many long-standing dynamic equilibria in the ecosystem. The
outcome of this competition is by no means
certain. Man's recent triumphs have drawn
heavily on the vast but not inexhaustible
material and energy reserves accumulated
in past eons (e.g., petroleum is a major raw
material in the production of pesticides as
well as an energy source for agricultural
technology). It is probable that the adaptive potential of the complex insect bio-
138
HAROLD T. GORDON
chemical-genetic systems has only begun to
respond to the human challenge. It is in
the light of this great conflict that one
must see the possible significance of studies
of both mammalian and insect nutrition.
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Dadd, R. H. 1960. Some effects of dietary ascorbic
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Dcthier, V. G. 1947. Chemical insect attractants
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