1. STOR ®
E ffect of Ration on Energy Allocation in a Carabid Beetle
Author(s): P. C. De R uiter and G. Ernsting
Source: Functional Ecology, Vol. 1, No. 2, (1987), pp. 109-116
Published by: B ritish Ecological Society
Stable URL: http://www.jstor.org/stable/2389713
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2. : Effect of ration on energy allocation in a carabid
i,109-116 beetle
109
P. C. DE RUITER* and G. ERNSTING
Department ofBiology, Vrije Universiteit, de
Boelelaan 1087, 1081 HV Amsterdam, The
Netherlands
Abstract. The energy budget of the predatory
beetle Notiophilus biguttatus F. has been estab-
lished at three rations. Rates of egg production,
respiration and defecation and the energy valué of
the faeces increase with an increase in ration.
From these parameters we have estimated the
amounts of energy that are allocated to reproduc-
tion and maintenance.
Key-words: Carabidae, energy budget, cost of repro-
duction
Introduction
Predators frequently face temporal and spatial
fluctuations in food availability. The predator may
respond to these fluctuations by altering its search
effort to maintain a sufficient amount of energy
input. In spite of such behavioural responses,
fluctuations in the rate of ingestión might be
inevitable and then physiological responses, such
as altering the energy budget, are required. The
relationship between the energy budget of a preda­
tor and the rate of ingestión shows how fluc­
tuations in food availability affect the allocation of
energy to reproduction and survival, and may
reveal compromises between these demands
(Calow, 1977).
In this paper we examine the effects of food
supply on the energy budget of Notiophilus bigut­
tatus F. This carabid beetle is a predator of
springtails (Schaller, 1949; Ernsting, 1978). Natu­
ral populations of springtails fluctuate consider-
ably in number (Van Straalen, 1985). Schaller
(1949) noted that N. biguttatus responds
numerically to fluctuations in the density of
springtails. This was supported by data from a
pitfall experiment which showed that the activity-
Correspondence: Dr P. C. De Ruiter, Department of
Population and Evolutionary Biology, Rijksuniversiteit
Utrecht, Padualaan 8, 3508 TB Utrecht, The Netherlands.
density of N. biguttatus was positively correlated
with the activity-density of the springtails (Ern­
sting, 1978). The individual consumption of the
beetle also responds to fluctuations in springtail
density (De Ruiter, 1987).
We defined the energy budget of N. biguttatus
from measurements of egg production (P), respi­
ration (R) and defecation rate (F) at different rates
of ingestión (I). From these quantities we esti­
mated the energy allocated to reproductive effort
(REP: energy expended on reproduction) and to
maintenance (M). We also measured, under ad
libitum feeding conditions, the food requirements
of females with different rates of egg production.
From this we deduced the maintenance energy
required by non-reproductive females. Finally, we
examined if energy is allocated to reproduction at
the cost of other aspects of metabolism.
Materials and methods
Subjects
Notiophilus biguttatus is a common species which
may occur in densities of up to c 10 m-2 in
woodlands. It is a small (5-7mg), diurnally active,
visually hunting predator. Gut contents of beetles
collected in the field consisted of mites, springtails
and pollen (Davies, 1959). Ernsting &Joosse (1974)
showed that N. biguttatus is one of the most
important predators of springtails. The beetle may
have one (Lindroth, 1949; Davies, 1959; Luff, 1976;
Turin, Haeck &Hengeveld, 1977) or two (Burmeis-
ter, 1939; Den Boer, 1977; Loreau, 1985) gener-
ations per year and Larsson (1939) reported that
adults live for one year.
The beetles used in the present study were
collected in November from a pine plantation on
the Dutch Wadden Island of Schiermonnikoog. In
the laboratory they were stored at 8°C under short
day conditions (Light:Dark [L:D] —8:16) and were
fed with springtails of the species Orchesella
cincta (Linné). The latter is one of the commonest
surface dwelling springtails; it is especially abun-
dant in pinewoods where it can be found in
densities > 1000 m-2 (Van Straalen, 1985).
Because of its abundance, habitat choice and

3. 110 relatively high locomotor activity this species is
P. C. De Ruiter probably an important prey for N. biguttatus
& G. Ernsting (Ernsting, 1978). Weights of O. cincta range from
0-02 mg as hatchling to 2*0mg as adult. The
springtails used in the experiment were collected
from a mass culture in the laboratory; only
specimens within the range 0*45-0*55mg were
used.
Experimental design and statistics
The experiments were carried out in a controlled
climate room with long day conditions (L:D —
16:8) and a fluctuating temperature regime
20°C:10°C — 16:8). The female beetles were kept
individually in small jars (diameter 5cm; height
3*5 cm). The jars had a transparent lid and a moist,
plaster bottom 2cm thick topped by a layer of
moist fine-grained sand (3mm) and a few broken
pine needles. Three weeks before each experiment
the beetles were transferred to the experimental
room to acclimatize to the experimental condi­
tions. The beetles were transferred to a new jar
weekly, on which occasion a male beetle was
added to join each female for c 2 hours.
Experiment 1: Reproduction (P). In experiment
la, 30 females were assigned to five groups of six
beetles and were supplied 2, 4, 6, 8 and 10 prey per
day (corresponding to 1, 2, 3, 4 and 5mg). Egg
production was measured weekly by washing the
sand through a mesh that retained the eggs. Exper­
iment la lasted 3 weeks. In experiment Ib, 30
females were assigned to three groups of 10 beetles
and were supplied with 1,1*5 (one/two springtails,
alternately) or 2 springtails each day (correspond­
ing to 0*5, 0*75 and lmg). Experiment Ib lasted 2
weeks.
Experiment 2: Respiration (R). Twelve female
beetles were assigned to three groups of four
beetles. They were supplied with 1, 3 or 5 prey per
day. Oxygen consumption at 20°C was measured
with a Cartesian Diver micro-respirometer with 10
diving chambers (Zeuthen, 1964) containing gas
volumes ranging from 949 to 992 jjlI . Readings were
made for 3h at 20min intervals. In experiment 2b,
the oxygen consumption of the same beetles was
measured once after they had been deprived of
food for 24h.
Experiment 3: Defecation (F). Thirty female
beetles were assigned to three groups of 10 beetles
and were supplied with 1, 3 or 5 prey per day. At
the beginning of the experiment the beetles were
transferred to small glass jars (diameter 2cm,
height 5cm) supplied with a layer of moist fine-
grained sand (0*5 cm). Defecation was estimatedby
subtracting the initial weight of the jars, with sand,
from their weight after 4 days, with sand and
faeces (eggs were removed). Before the jars were
weighed they were dried in an oven. We assumed
that the springtails produced only a negligible
amount of faeces since they were deprived of food
for one day before being supplied to the beetles. A
control group of jars, without beetles and
springtails, showed a slight increase in weight
during the experimental period. The mean valué of
these increments was subtracted from the weight
increment of each experimental jar before the data
were submitted to a regression analysis.
Experiment 4: Food requirements and respi­
ration at ad libitum feeding conditions. Twenty-
five female beetles were collected in the field at the
end of March during the reproductive period. In
the laboratory these beetles were offered excess
prey. Consumption was measured each day, egg
production and respiration after one week. For
comparison we also measured the rates of inges­
tión and respiration of 25 males kept under ad
libitum feeding conditions.
Energy equivalents. The energy equivalents of
prey, faeces and eggs were measured using a
microbomb calorimeter (Phillipson, 1964).
Statistics. Prior to each analysis of variance
(a n o v a ), we verified the homogeneity of variances
by means of Bartlett’s test (Sokal & Rohlf, 1981)
and the normality of the data using the test of Wilk
&Shapiro (1968). Regression equations were com­
pared by means of an analysis of covariance
(a n c o v a ) (Sokal & Rohlf, 1981).
Results
Ingestión (I). Ingestión was considered to equal the
amount of food supplied. Only when the ration
exceeded six springtails per day was the consump­
tion of the beetles less than the food supplied
(experiment la) and these data were excluded
from the analysis.
Experiment 1: Production (P). The pre-treatment
(3 weeks under experimental conditions) brought
the female beetles to a steady state with zero
growth and a more or less constant egg production.
Therefore, production here is considered to con-
sist of egg production only. Egg production
increased linearly with food ration for both exper­
iments (Fig. 1) and the slopes and adjusted means
of the two regression lines were not significantly
different (a n c o v a , slopes: 0*25 < P < 0*50; adjusted
means: 0*75 < P < 1). The regression equations of

4. 111
Energy
aliocatión in a
carabid beetle
Production
(Eggs.d’13
0.27 0.5 0.75
Food ration Cmg.d"1]
Fig. 1. The effect of food ration on egg production. Open
dots: experiment la. Solid dots: experiment Ib. Vertical
bars denote 95% CL. Regression equations: P = T53^FR
—0-64 (Experiment la); P = 1-18*FR —0-32 (Experiment
Ib). Slopes differ significantly (a n o v a , P < 0-001) from
zero.
experiment la and Ib predict that egg production
will stop at a daily ration of 0-42 and 0-27mg
respectively. (The results of a control experiment
have shown that beetles indeed stop reproducing
when supplied with one prey [0-25 mg.day-1]).
The regression equation of experiment la was
used to construct the energy budget; this choice
was based on the observation that in experiment
Ib, at a ration of 0-5 mg.day-1, two beetles had not
produced eggs.
Experiment 2: Respiration (R). Oxygen con­
sumption increased linearly with ration (Fig. 2)
and the slopes of the two regression lines were not
significantly different (a n c o v a , 0-25 < P < 0-50),
whereas the adjusted means were (a n c o v a , P <
0*001). The fact that the slopes were not signifi­
cantly different implies that the increase of respi­
ration with ration is independent of gut contents.
This increase in oxygen consumption is presuma-
bly an effect of the increase in egg production with
ration. The fact that the adjusted means were
different suggests that gut emptying reduces
oxygen consumption hut it is also possible that the
food deprivation for one day reduced the rate of
reproduction, which in turn reduced the respi­
ration.
Experiment 3: Defecation (F). Defecation
(mg.day-1) increased linearly with ration (Fig. 3).
Energy-equivalents. Table 1 shows the energy-
equivalents of prey, eggs and faeces. The dry
weight (Wd) of one springtail is 0-11 mg. The
energy valué of O. cincta was found to be 18-81
Joule (J).mg-1 (Wd), i.e. 2-07 J.prey-1. The regres­
sion equations (given in Figs 1, 2 and 3) have been
transformed in order to relate energy expenditure
(J.day-1) on egg production, respiration and defe­
cation to ration (FR in mg wet weight (Ww).day-1).
The energy valué of eggs was estimated to be
22-84 J.mg-1 (Wd). The dry weight of one egg is
0-053mg which corresponds to 1-21J. The regres­
sion equation in terms of J. day-1 therefore
becomes:
P = 1-85*FR —0-77 Equation 1
Respiration
Food ration (mg.d 13
Fig. 2. The effect of food ration on respiration. Solid dots:
experiment 2a. Open dots: experiment 2b (empty guts).
Vertical bars denote 95% CL. Regression equations: R =
1-38^FR + 1-65 (Experiment 2a); R = 1-ll^FR + 1-21
(Experiment 2b). Slopes differ significantly (a n o v a , P <
0-001) from zero.
Defecation
Food ration (mg.d 1]
Fig. 3. The effect of food ration on defecation. Vertical
bars denote 95% CL. Regression equation: F = 0-28^FR +
0-05. Slope differs significantly (a n o v a , P < 0-001) from
zero.

5. 112
P. C. De Ruiter
& G. Ernsting
Table 1. Average energy equivalents (in J.mg 1 [Wd]) of prey, eggs and faeces; the three valúes for faeces refer to the food
rations of 1, 3 and 5 springtails per day. SE and numbers of measured pellets are given in parentheses.
Prey Eggs Faeces
FR: 1 FR: 3 FR: 5
18-81 22-84 12-05 13-67 14-60
(±0*22 ;3) (±0-25;3) (±0-30;2) (±0-93;3) (±0-14;2)
Table 2. Energy budgets, absorption efficiencies (A/I) and production efficiencies (P/A) at rations of 1, 3 and 5
springtails (0-5mg each) per day. I: ingestión; P: production; R: respiration; F: defecation; 8: I-P-R-F. all valúes are
expressed (except A/I, P/A and 8/1) in J. day-1 .
I P R F 8 A/I P/A 8/1
FR 1: 2-07 = 0-155 + 0-965 + 0-555 + 0-395 0-731 0-102 0-191
FR 3: 6-21 = 2-005 + 1-535 + 1-665 + 1-005 0-731 0-441 0-162
FR 5: 10-35 = 3-855 + 2-105 + 2-775 + 1-615 0-731 0-509 0-156
Oxygen consumption valúes were converted to
energy valúes using the oxy-Joule equivalent of
20-0 J.ml-1 of oxygen consumed (Engelman, 1966).
However, respiration was measured at 2 0°C,
whereas beetles were kept at 20°C during the day
(16h) and 10°C during the night (8h). Oxygen
consumption at 10°C amounts to 58-6% of oxygen
consumption at 2 0 °C and this percentage is
independent of food level (Ernsting, in prepar-
ation). Henee, respiratory rates were multiplied by
24(h)*-0-02(J.|uil_1) and subsequently reduced by
13-8% (i.e. [100—58-6]^8/24) to give:
R = 0-57*FR + 0-68 Equation 2
Experiment 4: Food requirements and respi­
ration under ad libitum feeding conditions. Con­
sumption and egg production by the female beetles
were positively correlated (Fig. 5a) and the rela-
tion between them is represented by the ‘principal
axis’ estimated in the correlation analysis (Sokal &
Rohlf, 1981):
P = 2-74t*Co - 4-71 (Co: consumption in mg.day-1)
Extrapolation of this axis to zero-reproduction
indicates that non-reproductive females require
1-72 mg.day-1 under ad libitum feeding condi­
tions. This rate of consumption deviates markedly
The energy valué of the faeces appeared to
depend on the amounts ingested (Table 1). There-
fore, we performed a sepárate regression analysis
on the data expressed in J.day-1. This analysis
yielded a regression equation with a zero-value for
the y-intercept and a slope that was significantly
different from zero (a n o v a , P < 0-001):
Output CJ.d")
F = l-ll*F R Equation 3
The energy budget. Table 2 shows the energy
budgets for beetles with food rations of 1, 3 and 5
springtails per day, together with valúes for pro­
duction efficiency (P/A, where A = I-F ) and
absorption efficiency (A/I). Production efficiency
increased with food ration. Since total energy
expenditure measured was less than energy intake
the budgets were balanced using a term 8. The
input-output diagram (Fig. 4) was constructed by
summing the regression equations 1, 2 and 3 on a
continuous ration scale.
Fig. 4. The energy budget constructed from the regression
equations of experiment la, 2a and 3. (P: Production; R:
Repiration; F: Faecal production; 8 :1-P-R-F).

6. 113
Energy
allocation in a
carabid beetle
(a)
Production
(Eggs.cf1)
0.5 1 2 3 4
Consumption (mg.d-1)
Cb)
Respiration
(¡u02.h"1)
i i i i i i
1 2 3 4 5 6
Production (Eggs.d-1)
Fig. 5. Consumption, respiration and egg production at
ad libitum food supply. Solid lines represent the prin­
cipal axes. Open symbols with bars denote mean and
standard error of male data (O: not corrected for
bodyweight; □: corrected for body weight). Correlation
coefficients (r) are calculated with body weight held
constant. (a) The relation between egg production and
consumption. r: 0-83. Broken line: experiment la. (b) The
relation between respiration and egg production. r: 0-76.
from that obtained by the extrapolation of the
regression line established in experiment la. The
latter predicts that egg production will not stop
until consumption is below 0*42 mg.day-1. Respi­
ration was also positively correlated with egg
production (Fig. 5b) and extrapolation of the
principal axis to zero-production predicted a
respiration rate for non-reproductive females of
2-94 |jLl02.h-1 (1*22 J.day-1). Rates of consumption
and respiration of non-reproductive females are
compared with the rates of consumption and
respiration of males in Fig. 5a and b. However, the
average body weight of males (Wm) was less than
the average body weight of females (Wf) and both
consumption and respiration depended on body
weight. Therefore, for males we give both the
observed rates of consumption and respiration and
the deduced rates that are corrected for the lower
body weight. This correction consisted of a multi-
plication by Wf/Wm, since, within the range of
4-6 mg, respiration and consumption were
observed to increase approximately propor-
tionally with body weight.
Discussion
The energy budget
In energy budget studies intake rarely equals
expenditure (Wightman, 1981; McEvoy, 1985). In
our study the imbalance (8) appears to be a
constant fraction (16-19%) of ingestión. It might
be due to (1) underestimation of respiration since
locomotor activity in the respirometer is very low
and (2) overestimation of consumption, since the
energy contení of a prey decreases during the
period between weighing the prey and consump­
tion by the predator, due to respiration by the prey
(McEvoy, 1985). The respiratory rate of a 0-5-mg
springtail is equivalent to an energy expenditure of
0*097 J.day-1 (Testerink, 1981). If we assume that
the average period from weighing until capture is
6h, the energy valué of a 0*5-mg springtail (2*07 J)
will be reduced by 0*025J (1*2%). This could
account for ±7% of the imbalance.
Absorption efficiency (A/I) in N. biguttatus is
within the range previously reported for terrestrial
carnivores (Lawton, 1970; Brafield & Llewellyn,
1982). Absorption efficiency often decreases with
increased ration, since the retention time offood in
the gut decreases under these conditions (Hassall
&Jennings, 1975). In the present study the energy
valúes of the faeces agree with this expectation but
the producís of these energy valúes and the dry

7. 114 weight of the faeces revealed a ration-independent
P. C. De Ruiter absorption efficiency.
& G. Ernsting
Reproductive effort (REP) and maintenance (M)
It is generally assumed that energy partitioning
between reproductive effort and maintenance is
adjusted by natural selection so as to maximize the
number of offspring. This adjustment may entail a
trade-off between current and future reproductive
success (Hirshfield & Tinkle, 1975; Calow, 1979;
Tuomi, Hakala & Haukioja, 1983). The cost of
reproduction (CI) then refers to the reduction in
future reproduction due to investing energy on
current reproduction instead of on the mainten­
ance of the parent.
The data in Table 2 cannot be related unambi-
guously to REP and M, since respiration (R) is
partly due to processes related to REP (Rr) and
partly to somatic processes related to M (Rm).
Consequently, the energy contení of eggs accounts
for only part of REP. The energy budget of the
beetle thus becomes:
I = REP + M + F + 8
Rm (Table 3) can be estimated by extrapolating
the regression line of respiration on ration (exper­
iment 2a) to the ration of 0-42 mg (the ration at
which egg production will stop; experiment la).
The respiration above Rm (due to the increase in
food ration) can be assumed to reflect Rr. This way
of estimating Rr implies that any increase in
respiration is allocated to REP, but it is also
possible that beyond a ration of 0-42 mg.day-1
beetles allocate more respiration energy to non-
reproductive demands. However, this is not likely
to be a large amount since the estimated valué for
Rm (0-917 J.day-1) is not far below the estimated
respiration rate ofnon-reproductive females under
ad libitum feeding conditions (1-22 J.day-1).
Here we define the cost of reproduction as being
the extent to which energy is allocated to repro­
duction at the cost of maintenance. An index ofthe
cost ofreproduction can be calculated according to
Calow (1979) using:
CI = 1-([I-REP]/REST)
REST stands for the amount of energy needed by a
non-reproductive fem In the case of N. bigutta­
tus, REST is estimated by multiplying the absorp­
tion efficiency (i.e. 0-731) by the rate of ingestión at
zero reproduction (i.e. 1-72 mg.day-1 = 7-12
J.day-1) leading to 5-20 J.day-1. This rate of inges­
tión differs from the results of experiment la,
which predict that reproductive females will not
stop egg production until the food ration is below
0-42 mg.day-1 (1-74 J.day-1). The difference
between the two predicted consumption rates for
non-reproductive females illustrates that during
reproduction poor feeding conditions lead to a
drain of resources from non-reproductive to repro­
ductive demands.
There are two possible ways of calculating CI.
First we might assume that I—REP corresponds to
the ration-independent estímate for Rm. This
method implies that REP also includes 8. Second,
we may assume that 8 is used (at least in part) for
non-reproductive processes, e.g. locomotor act-
ivity. Then I—REP includes Rm and (part of) 8. In
Table 3 we give valúes of CI with I—REP = Rm and
of CI* with I—REP = Rm + 8. CI appears to be
independent of ration, whereas CI* decreases as
ration increases.
Positive valúes of CI imply that energy is being
diverted from somatic maintenance to reproduc­
tion and point to the possible existence of some
sort of somatic stress during reproduction, parti-
cularly when food is limited. Notiophilus bigutta­
tus is presumably faced with such periods of food
shortage during its reproductive period (Van
Straalen, 1985). Favouring reproduction at the
expense of maintenance is a strategy that is to be
found especially in species that breed only once
(semelparous species; Stearns, 1976; Woollhead &
Calow, 1979). However, it is not clear if N. bigutta­
tus is a semelparous species but the data are
suggestive. For example, a high post-reproductive
Table 3. Estimation of the reproductive effort at rations of 1, 3 and 5 springtails (0-5 mg each) per day. Rm: respiration
due to somatic processes; Rr: respiration due to reproductive processes; REP: reproductive effort (P + Rr); REP%:
(REP/I)-*100; CI: index for the cost of reproduction (with I-REP = Rm), CH: idem (with I-R EP = Rm + 8). All valúes
(except Rep%, CI and CH) are expressed in J.day-1 .
I Rm Rr REP REP% CI CI*
FR 1: 2-07 0-917 0-048 0-203 9-81 0-824 0-748
FR 3: 6-21 0-917 0-618 2-623 42-24 0-824 0-630
FR 5: 10-35 0-917 1-188 5-043 48-72 0-824 0-513

8. 115
Energy
allocation in a
carabid beetle
mortality has been found by Ernsting & Huyer
(1984) in an experiment on the fecundity of the
beetle. Eight out of 10 females died after one
reproductive period (lasting a máximum of 24
weeks) and two died after 36 weeks following a
second period of (low) reproductive activity. N.
biguttatus breeds predominantly in spring and
reports on reproductive activity in autumn
(Burmeister, 1939; Den Boer, 1977; Loreau, 1985)
may concern either a few survivors of the spring-
breeding generation or females that emerged early
in autumn. Certainly, females that are cultured in
the laboratory can produce eggs c 3 weeks after
emergence. In conclusión, the data so far suggest
that female beetles invest a large effort in repro­
duction at the cost of their own metabolism and
this predicts a semelparous pattern. More field
data are needed to test this prediction further.
Acknowledgments
The experiments were carried out with the help of
G. van Overbeeke, J. A. Isaaks and F. A. Huyer. P.
Calow and S. M. McNab made valuable comments
on an earlier versión ofthe manuscript. The figures
were prepared by the Department of Image Pro­
cessing and Design (Faculty of Biology, University
of Utrecht). The investigations were supported by
the Foundation of Fundamental Biological
Research (BION), which is subsidized by the
Netherlands Organization for the Advancement of
Puré Research (ZWO).
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