Behavioral Ecology Vol. 13 No.

1: 52–58

The cost of parental care: prey hunting in a

digger wasp
Erhard Strohma and André Marlianib
Theodor–Boveri–Institute for Biosciences, Würzburg University, Germany, and bZoological Institute,
a

Bonn University, Germany

Trivers’s concept of parental investment is an integral part of modern evolutionary biology. ‘‘Parental investment’’ is defined

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as any parental expenditure that benefits a current progeny at the expense of a parent’s ability to reproduce in the future.
Because future costs are hard to quantify, other currencies were used that were thought to be related to the actual costs.
However, the validity of these alternative measures has rarely been established, at least in insects. Specifically, these measures
were not shown to represent costs at all. We investigated provisioning behavior in a sphecid wasp, the European beewolf,
Philanthus triangulum F., and tested whether prey hunting entails future costs to the female wasp and thus represents parental
investment. We increased as well as decreased the females’ hunting effort experimentally and determined their hunting success
on the following day. Furthermore, we analyzed the correlation between hunting rate of unrestricted females and their life span
and assessed the effect of an experimentally decreased hunting effort on life span. The future rate of bee hunting decreased
when hunting expenditure was increased (in the field) and vice versa (both in the field and in the laboratory). In contrast,
there was no trade-off between hunting rate and life span, and life span was not affected by an experimentally decreased hunting
effort (in the laboratory). Because prey hunting entails costs in terms of a reduced rate of prey hunting in the future, it meets
Trivers’ definition of parental investment. Key words: cost of reproduction, European beewolf, parental investment, Philanthus
triangulum F., Sphecidae, Trivers. [Behav Ecol 13:52–58 (2002)]

T he concept of parental investment is a fundamental ele-

ment of sexual selection and investment allocation the-
ories (Clutton-Brock, 1991; Trivers, 1972). However, empirical
studies have notoriously suffered from problems to quantify
parental investment (e.g., Bérubé et al., 1996; Brockmann and
Grafen, 1992; Strohm and Linsenmair, 1999). ‘‘Parental in-
vestment’’ is defined as any resource that increases the success
of current progeny at the expense of a parent’s ability to re-
produce in the future (Trivers, 1972). Thus, parental invest-
ment in a current progeny should ideally be quantified as the
parent’s decrease in future reproduction. Because this is usu-
ally not feasible, alternative measures have been used that are
thought to be related to the actual costs. However, this as-
sumption has not been adequately tested (Clutton-Brock,
1991; Rosenheim et al., 1996; Strohm and Linsenmair, 1999),
so the validity of these measures is hard to judge.
Parental investment is particularly difficult to quantify if
parents provide substantial parental care because these ex-
penditures are more difficult to measure than, for example,
the amount of nutrients in an egg. Recently, for example,
suckling time, which was often used as a measure of parental
investment in mammals, has been shown to be a questionable
estimate of milk intake (Cameron, 1998). Nevertheless, there
is some information on the future cost of parental care for
mammals and birds (Clutton-Brock, 1991). However, little is
known about costs of parental investment in insects (Nalepa,
1988; Tallamy and Denno, 1982; Tallamy and Schaefer, 1997),
particularly in solitary as well as social aculeate Hymenoptera.
This is in contrast with the prominent role that brood care in
general and the concept of parental investment in particular
Address correspondence to E. Strohm, Zoologie III, Biozentrum,
Universität Würzburg, Am Hubland, D-97074 Würzburg, Germany. E-
mail: strohm@biozentrum.uni-wuerzburg.de.
Received 3 August 2000; revised 13 March 2001; accepted 13 March
2001.

2002 International Society for Behavioral Ecology
has for studies of Hymenoptera (Nonacs, 1986; Trivers and
Hare, 1976). In this study, we investigated a solitary digger
wasp, the European beewolf, Philanthus triangulum (Hyme-
noptera, Sphecidae), and asked whether parental behavior
entails a cost to females.
Female European beewolves hunt exclusively on honeybees,
Apis mellifera (Strohm, 1995; Tinbergen, 1932). Bees are par-
alyzed on flowers (Rathmayer, 1962; Tinbergen, 1935). Fe-
males carry the prey in flight to their nest, which is construct-
ed in open, sandy soil. Bees are temporarily stored in the main
burrow. The wasp excavates a lateral side burrow with a ter-
minal brood cell, places the bees into the brood cell, oviposits
on one of them, and finally closes the brood cell by refilling
the side burrow very carefully. Larvae hatch 2–3 days later and
feed on the bees for about 6–7 days. Then they spin into a
cocoon and either emerge as a second generation the same
year or hibernate and emerge the next summer. Male progeny
are provisioned with 2.2 ⫾ 0.8 bees (mean ⫾ SD, range: 1–
5), whereas female progeny receive 3.8 ⫾ 0.5 bees (range: 3–
5; Strohm and Linsenmair, 2000).
Beewolf females spend time, energy, and material on four
main aspects of reproduction: prey hunting, nest excavation,
preservation of the prey, and egg production (Strohm, 1995;
Strohm and Linsenmair, 2001). Prey hunting comprises
searching, stinging, and the transportation of prey in flight.
Flying per se, and particularly flying with a load, is extremely
costly energetically (Casey, 1992; Kammer and Heinrich, 1978;
Wegener, 1996). A beewolf female weighs 110 ⫾ 20 mg (mean
⫾ SD) and carries a honeybee that weighs 80–160 mg (de-
pending on the filling status of the honey stomach). Conse-
quently, flying with a prey is probably the energetically most
costly part of beewolf reproduction. Furthermore, flying activ-
ity has been shown to have negative consequences on subse-
quent reproduction in other insect species (Collatz and Wilps,
1986; Slansky and Scriber, 1985). Therefore, we focused on
the question of whether hunting bees generates future costs
for a beewolf female.
One of the reasons for the paucity of information on the
Strohm and Marliani • Cost of parental care
cost of parental care (i.e., the negative relationship between
current and future reproduction), is a general difficulty of
investigating trade-offs (e.g., Lessells, 1991; Roff, 1992; van
Nordwijk and de Jong, 1986; see also Bailey, 1992; Sinervo and
DeNardo, 1996). Three different approaches have been used
(Lessells, 1991; Partridge, 1986; Roff, 1992). First, observa-
tional data on the intensity of current and future reproduc-
tion were used to assess a possible trade-off (phenotypic cor-
relation). This method has one major weakness. Because in-
dividuals might differ considerably in their total reproductive
potential, superior individuals might produce more progeny
both now and in the future. The result would be a positive
rather than a negative correlation between current and future
reproduction (van Nordwijk and de Jong, 1986). This prob-
lem might be solved if the confounding variable that accounts
for the differences in reproductive potential (e.g., size) is
known and its effect is controlled (Roff, 1992). The second
method is to increase (or decrease) parental expenditure ex-
perimentally and to determine its effect on future reproduc-
tion (phenotypic manipulation). Finally, negative correlations
on the genetic level can be investigated by selection experi-
ments or sib analysis (genetic correlation; e.g., Rose and Char-
lesworth, 1981a,b).
In this study we mainly used a phenotypic manipulation
approach. We assessed the effects of both an experimentally
increased and decreased expenditure for parental care on fu-
ture reproduction. Additionally, we report the results of a phe-
notypic correlation analysis. Costs might manifest themselves
either as a decreased rate of future reproduction (delay of
subsequent reproductive event or lowered reproductive out-
put per unit time) or as reduced life span. We investigated
both aspects and addressed the following questions. Does an
increased effort for the transportation of a bee delay subse-
quent hunting trips? Does an experimentally increased (de-
creased) hunting effort on one day have negative (positive)
consequences for the hunting success on the following day?
Is life span negatively correlated with the rate of hunting of
unrestricted females? Do females live longer when their hunt-
ing effort is experimentally decreased? Because female size is
known to affect hunting success (Strohm and Linsenmair,
1997), we also analyzed whether a possible cost depends on
female size.
METHODS
General
Where possible, we analyzed the hunting success of beewolf
females using matched-pairs designs. We matched pairs of ex-
perimental and control females with regard to as many rele-
vant factors as possible (size, age, location, and microclimate
of nest site). Assignment of a female to experimental or con-
trol group was random. Because sample sizes did not allow us
to reasonably test for assumptions of parametric tests, we cal-
culated p values by use of Monte Carlo simulations for paired
data (or independent data when indicated; in each case
100,000 iterations; SPSS 10.0.7). Sample sizes differed some-
what among tests because the conditions for the inclusion of
the data from one female might have differed (e.g., there
might have been no female of similar size to be compared in
a paired design; however, a comparison of data of this female
before and after a treatment is possible). In cases of multiple
tests based on the same data, the significance level ␣ was cor-
rected (sequential Bonferroni correction; Rice, 1989).
Hunting of loaded bees
If flying with prey is costly, flying with a larger load should be
more costly. Females were simultaneously provided with bees
53
with experimentally increased weight and unmanipulated
control bees. We predicted that females need longer to bring
in manipulated bees and make longer pauses before starting
on a new hunting trip. Females were caught at a field site
near Würzburg, Germany. They were kept in an outdoor flight
cage (4 ⫻ 2 ⫻ 2 m) where they could nest in a sand com-
partment at one narrow side of the cage (Strohm and Linsen-
mair, 1997). Females were observed for their entire daily ac-
tivity period. Bees were provided ad libitum. The weight of
half of the bees was increased by 20 mg (an increase of about
20%) by bending a piece of lead solder around each hindleg
(bees were not conspicuously affected by this treatment). We
recorded the duration of foraging trips procuring control and
experimental bees as well as the duration of the pause until
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the next hunting trip. If a female stayed for longer than 2 h
in her nest after bringing in a bee, she probably provisioned
a brood cell (Strohm and Linsenmair, 1997, 1998). Thus,
pauses longer than 2 h were regarded to belong to different
brood cell cycles and were not included. We compared du-
rations of hunting trips and pauses of individual females using
Monte Carlo simulations for paired data. Only females with
at least five flights with each kind of bee were considered in
the analysis.
Increased hunting effort in the field
If prey hunting is costly, an experimental increase of the ex-
penditure for prey hunting should cause a decrease in the
hunting success on the following day. In the field, the expen-
diture for bringing in bees was increased by removing some
of the bees before a female entered the nest. Females were
observed for their entire daily activity period for several days,
and the number of bees they brought in was recorded at a
field site near the Biocenter of the University of Würzburg.
On day 1 of a trial, females were not disturbed. On day 2,
every second bee that a female of the experimental group
brought to the nest (starting with the second prey) was re-
moved just before the female could enter the nest. Control
females were disturbed when trying to enter their nest in a
way similar to the removal of bees from experimental females,
but bees were not removed. On day 3, all females could hunt
undisturbed. The number of bees the females brought to the
nest was recorded on each day. Experimental and control fe-
males were pairwise matched (from the same generation, dif-
ference in head width ⬍ 0.1 mm, nests less than 2 m apart
from each other with identical exposition and shading). Am-
bient temperature differed less than 2⬚ during the experi-
mental period of 3 days. The experiment was conducted in
three different trials (3-day experimental period) with 6–7 ex-
perimental and control females in each trial. Because there
were no differences between these three trials and because we
used a matched-pairs design, the results of the different trials
were pooled.
The desired effect of the manipulation, an increase in the
females’ expenditure, requires that experimental females ac-
tually bring in more bees than they would have if not manip-
ulated. Therefore, we tested whether the number of bees
brought to the nest on day 2 was higher for experimental than
for control females. To test whether there was a decrease in
hunting success of experimental females on day 3, we com-
pared their change in hunting success between day 1 and day
3 (day1/day3) with the respective values of control females.
Because female size might influence the impact of the manip-
ulation, we tested for a correlation between size and the
change in hunting success of experimental females on day 2
relative to day 1 (number of bees on day 2/number of bees
on day 1) as well as day 3 relative to day 1 (day 3/day 1).
54
Decreased hunting effort in the field
We predicted that the future hunting success of females could
be enhanced when their current expenditure for hunting was
decreased. This experiment was conducted at a field site near
Bonn, Germany (Wahnerheide; see Strohm and Lechner,
2000 for details). Experimental and control females were pair-
wise matched (from the same generation, difference in head
width ⬍ 0.1 mm, nests ⬍ 2 m apart from each other with
identical exposition and shading). Experimental females were
prevented from hunting by covering their nest entrances with
small gauze cages (250 cm3 volume) before they became active
in the morning. Because females were also prevented from
nectar feeding, they were provided with water and honey.
When necessary the cages were shaded to avoid overheating.
Control females were not manipulated in any way. On the
next day, experimental and control females were allowed to
hunt freely, and we recorded their success for the whole daily
activity period. Because the weather was very unstable during
the whole season, it was only possible to analyze the data for
the day after caging. Thus, the hunting success of pairs of
experimental and control females was compared by Monte
Carlo simulations. The effect of female size on the impact of
the treatment was assessed by testing for a correlation between
size (if not identical for a pair of females, the mean was used)
and hunting success of an experimental female relative to the
respective control female (experimental/control) on the day
after caging.
Limited bee availability in the laboratory
Again, we predicted that an experimentally decreased hunting
effort on 1 day should result in increased hunting success in
the future. In contrast to the previous caging experiment in
the field where experimental females were not allowed to
hunt at all, in the laboratory experiment females were provid-
ed with one bee per day for a period of several days. Beewolves
were caught at the field site near Bonn. Experimental and
control females were pairwise matched (from the same gen-
eration, difference in head width ⬍ 0.1 mm). All females were
individually housed in cages that consisted of a sand-filled
compartment (30 ⫻ 20 ⫻ 25 cm) and a flight compartment
(gauze cage, 30 ⫻ 20 ⫻ 20 cm). The cages were placed in a
room with a light/dark cycle of 14/10 h. Temperature ranged
from 23⬚ to 28⬚C at day and 20⬚ to 23⬚C at night. The cages
of experimental and control females were randomly distrib-
uted in the room. Control females were provided with bees
ad libitum (at least one bee was available throughout the ac-
tivity period). Experimental females were provided with only
one bee per day for 5–10 (mean ⫾ SD ⫽ 7.7 ⫾ 1.7) days.
Subsequently, they were provided with bees ad libitum. Bees
were caught at the same hive throughout the experiment. The
number of bees a female hunted per day was recorded. We
compared the hunting success of pairs of experimental and
control females by Monte Carlo simulations. To assess a pos-
sible effect of female size on the impact of the treatment, we
tested for a correlation between size (if not identical for a
pair of females the mean was used) and relative hunting suc-
cess of experimental females versus control females (experi-
mental/control) on the first day of unrestricted bee availabil-
ity.
Correlation between rate of bee hunting and life span
We predicted that the rate of bee hunting and life span should
be negatively correlated. This trade-off might, however, be
masked by differences in female quality (see introduction).
Cocoons were hibernated in the laboratory. After emergence
Behavioral Ecology Vol. 13 No. 1
females were kept in a large indoor flight cage (l ⫻ d ⫻ h ⫽
4 ⫻ 2 ⫻ 2 m) with males for about 7 days to allow mating
(males do not show territorial behavior when kept in small
cages; Strohm, 1995). During this time females had access to
prey and could nest in a large sand filled box (l ⫻ d ⫻ h ⫽
1.2 ⫻ 0.8 ⫻ 0.5 m). Subsequently, females (n ⫽ 42) were
individually housed in smaller cages (cage size and abiotic
conditions as above). Bees were provided ad libitum, and the
number of bees a female brought in per day as well as its life
span were recorded. Female body size might be a confound-
ing variable that obscures a possible trade-off because hunting
success is positively correlated with size (Strohm and Linsen-
mair, 1997). Because life span is a time event variable, it is
probably not normally distributed (Abacus Concepts, 1994).
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Therefore, we analyzed the data using survival analysis pro-
cedures (program Statview; Abacus Concepts 1994). A Weibull
equation provided an adequate fit to the life-span data. We
tested whether the inclusion of the covariates mean rate of
bee hunting (bees/day) and female weight at emergence sig-
nificantly improved the fit.
Limited bee availability and life span
An experimentally reduced hunting effort should extend life
span. After the mating period of about 7 days females were
individually kept in the laboratory as described above. Fe-
males of the experimental group were provided with one bee
per day, whereas the control group received bees ad libitum.
The number of bees actually hunted by a female and life span
were recorded. We analyzed the data using survival analysis
procedures (program Statview, Abacus Concepts, 1994). The
two treatment groups were compared by a Mantel-Cox test.
To test for the effect of female size on life span, we chose a
Weibull equation that provided an adequate fit to the survival
data and assessed the effect of female size as a covariate.
RESULTS
Hunting of loaded bees
Females needed on average 77% more time to bring in a load-
ed bee compared with control bees (Figure 1; Monte Carlo
simulation: n ⫽ 12, p ⫽ .017). The pause until the next trip
increased by 48% after flying with a loaded bee (Monte Carlo
simulation: n ⫽ 10, p ⫽ .01). Thus, flying with a bee that was
20% heavier than the average bee increased the time expen-
diture for a hunting trip by about 64% (control: 30.1 min,
loaded: 49.5 min). Consequently, after flying with a loaded
bee, subsequent hunting trips were delayed, and the rate of
hunting decreased.
Increased hunting effort in the field
Because females sometimes entered the burrow very rapidly,
only 42% of the bees (on average 2.1 bees per female) could
be removed from experimental females on the day of manip-
ulation (day 2). After removal, females flew around in the
vicinity of their nests for about 0.5–2 min, possibly searching
for the lost bee. Usually females then entered the burrow for
several minutes before starting on a new hunting trip (56 of
84 cases). Less often (28 cases) females immediately left to
hunt anew. The manipulation on day 2 caused a significant
increase in the hunting effort of experimental females. They
brought about 1.5 more bees to the nest than control females
(Figure 2, Monte Carlo simulation: n ⫽ 21, p ⫽ .001). There
was no significant effect of size of experimental females on
the hunting success on day 2 relative to day 1 (Spearman rank
correlation: rs ⫽ .25, n ⫽ 21, p ⫽ .27).
Strohm and Marliani • Cost of parental care 55

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Figure 1
Mean (⫾ SD) duration of hunting trips and of pauses until the Figure 2
next trip of beewolf females bringing in a control bee or a loaded Hunting success of beewolf females in the field (mean ⫾ SD
bee (mean of means of individual wasps with at least 5 flights with number of bees per day, N ⫽ number of females). On day 1 and
each kind of bee, N ⫽ number of females). day 3 both the control and experimental group were not
manipulated. On day 2 every second bee that an experimental
female brought to the nest was removed, and control females were
On day 3 (day after manipulation) experimental females disturbed in a similar way but the bee was not removed.
brought about 37% fewer bees to the nest compared with day
1 (Figure 2). There was no correspondingly strong decrease
in hunting success of control females. As a consequence, the
difference in hunting success between day 1 and day 3 was
significantly larger in experimental (-1.3 ⫾ 1) than in control
females (-0.3 ⫾ 1.5; Monte Carlo simulation: n ⫽ 21, p ⫽
.015). Thus, the increased effort of experimental females on
day 2 probably caused the significant decrease in hunting suc-
cess on day 3. Female size had no significant effect on the
decrease of hunting success on day 3 relative to day 1 (Spear-
man rank correlation: rs ⫽ .2, n ⫽ 21, p ⫽ .38).

Decreased hunting effort in the field

All females that had been prevented from foraging to reduce
their hunting effort brought in bees on the following day.
They brought in significantly more bees (1.3 ⫾ 1) than con-
trol females (0.55 ⫾ 1, Monte Carlo simulation: n ⫽ 15, p ⫽
.005). Overall hunting success was low because of low bee
availability at this site and suboptimal weather conditions dur-
ing the observation period. Female size had no significant
effect on the ratio of hunting success of an experimental fe-
male relative to the respective control female (Spearman rank
correlation: rs ⫽ .45, n ⫽ 12, p ⫽ .14).

Limited bee availability in the laboratory

During the period of limited bee availability (1 bee/day) ex-
perimental females brought in significantly fewer bees per day
than control females (Figure 3, Monte Carlo simulation: n ⫽
12, p ⫽ .004). On the first day of ad libitum bee availability,
experimental females brought in significantly more bees than
control females (Figure 3; Monte Carlo simulation: n ⫽ 12, p
⫽ .027). On the second day (and the following days), the
difference was no longer significant (Monte Carlo simulation:
n ⫽ 12, p ⫽ .12). Female size was not significantly correlated
with hunting success of experimental females relative to con-
Figure 3
Hunting success of beewolf females in the laboratory (mean ⫾ SD
number of bees per day, N ⫽ number of females). During the
treatment phase (5–10 days) females of the experimental group
received only 1 bee per day, whereas control females were provided
with bees ad libitum. In the test phase (day 1 and 2) both groups
received bees ad libitum.
56
trol females on the first day of unrestricted bee availability
(Spearman rank correlation: rs ⫽ .25, n ⫽ 10, p ⫽ .48).
Rate of bee hunting and life span
Mean (⫾ SD) female life span was 40.1 ⫾ 17.5 days. There
was no significant effect of the rate of bee hunting (␹2 ⫽ 0.74,
df ⫽ 1, p ⫽ .78) or female weight (␹2 ⫽ 0.01, df ⫽ 1, p ⫽
.90) on life span.
Limited bee availability and life span
Treatment groups differed in the number of bees hunted per
day (experimental group ⫽ 1 bee/day: 0.88 ⫾ 0.01, n ⫽ 20;
control group ⫽ ad libitum: 2.5 ⫾ 0.24, n ⫽ 19; Monte Carlo
simulation: n ⫽ 19, p ⬍ .001). Females that were provided
with 1 bee per day had a life span of 35 ⫾ 11 days and those
that received bees ad libitum lived for 43 ⫾ 12 days. The effect
was thus opposite to the prediction and nearly significant
(Mantel-Cox test: ␹2 ⫽ 3.49, df ⫽ 1, p ⫽ .062). The low p
value suggests that there might actually be some effect that
was not detected in this experiment. There was no significant
effect of female size as a covariate on life span (␹2 ⫽ 0.31, df
⫽ 1, p ⫽ .57).
DISCUSSION
Current and future hunting effort
All experiments that manipulated a female’s hunting effort
revealed some negative relationship between current and fu-
ture hunting success. Females delayed subsequent hunting
trips after bringing in loaded bees, thus lowering the subse-
quent rate of bee hunting. When bees were removed from
homing females, they increased their hunting effort with the
consequence of a decreased success on the following day. In
the field and in the laboratory, an experimental reduction of
hunting effort was associated with an increased hunting suc-
cess on the following day. In all experiments, the relative in-
crease (decrease) of hunting success was independent of size.
These results suggest that hunting is costly in terms of re-
duced hunting success.
However, the increase of hunting success after caging in the
field might have two alternative explanations. First, because
experimental females were provided with honey, this food
supplementation might have improved their hunting ability
on the following day. Beewolf females preferentially feed on
the content of the honey stomach of the prey bees as well as
on flowers. Because control females had unlimited access to
both bees and flowers, their food supply might not have been
considerably restricted compared with the caged females. Sec-
ond, because experimental females could not hunt, they
could not oviposit, although they might have had mature eggs.
If success of overmatured eggs is reduced, experimental fe-
males might have had a strong motivation to bring in bees
and oviposit on the day after caging. Both alternative expla-
nations are not relevant in the laboratory experiment because
both treatment groups were provided with honey ad libitum,
and experimental females were able to oviposit because they
had one bee available each day. The result of the laboratory
experiment is consistent with the field data. This suggests that
in both experiments the increase in hunting success is due to
the decreased hunting effort on the previous day and not
(only) the result of artifacts.
What are the physiological mechanisms mediating the neg-
ative effect of current on future hunting success? Unfortu-
nately, the physiological processes underlying trade-offs are
poorly understood (but see Nilsson and Svensson, 1996). Our
Behavioral Ecology Vol. 13 No. 1
data suggest that in beewolves the negative effect of decreased
hunting activity is reversible and lasts for about 1 day. Gen-
erally, there might be two nonexclusive explanations. For both
there is only little information available in insects. First, ex-
haustive flight might cause ultrastructural changes in flight
muscles (e.g., disruption of mitochondria; Hoffmeister, 1961,
1962; Johnson and Rowley, 1972) that negatively affect muscle
function, and recovery takes some time. Second, energy re-
serves (probably glycogen) might be depleted, and replenish-
ing the stores might take some time ( Johnson and Rowley,
1972; Neukirch, 1982). However, honeybees flown to exhaus-
tion resumed flight about 10 min after feeding on sugar so-
lutions (e.g., Crailsheim, 1988; Loh and Heran, 1970), sug-
gesting that depletion of energy should not have effects that
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last for about 1 day.
The result that females are able to hunt more bees than
they would have without manipulation suggests that they usu-
ally do not completely exhaust their capacity. One explanation
for this is that excessive hunting effort would decrease future
hunting success as indicated by this study. Second, hunting
effort might be adjusted to the rate of egg maturation. Finally,
females might have to save some energy (or other relevant
resource) to produce an egg or to excavate and provision a
brood cell.
Hunting effort and life span
There was no correlative evidence for a trade-off between the
rate of bee hunting and life span, and no effect of size as a
potentially confounding variable. Though an experimentally
decreased hunting effort increased hunting success on the
following day, there possibly was a negative rather than a pos-
itive effect of a restricted availability of prey (1 bee per day
versus ad libitum) on life span. We first discuss the nonexis-
tence of a positive effect of restricted hunting opportunity on
life span, second the possible negative effect of restricted
hunting, and third the conflicting results that a decreased
hunting effort had a negative effect on the following day but
not on life span.
In contrast to our results, a positive effect of experimentally
induced low rates of reproductive activity on life span has
been found in several insect species (e.g., in a bruchid beetle;
Messina and Slade, 1999), though not in all (Collatz and So-
hal, 1986). Because our results are from females kept in the
laboratory, several factors differed from the field. Most im-
portant, the distance flown with the bee was probably consid-
erably smaller than in the field (though it was larger than
might be expected from the size of the cage because females
mostly flew around for some time with a prey before entering
the nest). Increased predation is a potentially important cost
of increased hunting activity in the field but not in the labo-
ratory. However, we do not have any indication of predation
on foraging females (very few females were missing in action;
most died in their nest). Thus, overall predation risk might
be rather low in the field, too.
A negative effect of a low rate of reproduction (limited host
availability) on life span has been reported for parasitoid
wasps (Sahragard et al., 1991; van Lenteren et al., 1987). This
is probably caused by limited opportunity of host feeding
(Collier, 1995; Sahragard et al., 1991; van Lenteren et al.,
1987). Beewolf females also feed on their prey’s hemolymph
(Rathmayer, 1962; E. Strohm, unpublished observations), and
with only one bee per day hemolymph might not be available
in sufficient amounts. Alternatively, when provided with only
one bee per day, beewolf females might continuously search
for prey and spend even more resources on flying than do
nonrestricted females.
Differing effects of brood care on the future rate of repro-
Strohm and Marliani • Cost of parental care
duction and life span, similar to what we have found in bee-
wolves, were observed in a lace bug. Brood care (guarding of
the eggs and larvae) caused a reduction in the rate of ovi-
position but did not reduce life span (Tallamy and Denno,
1982; see Roff, 1992, for differing examples). Why is the fu-
ture rate of reproduction affected but not life span? Possibly,
the rate of reproduction and the duration of the reproductive
period depend on different resource pools or processes and
thus might be more or less independent of each other. For
example, the rate of bee hunting might depend on energy
reserves that can be fully replenished, and a female is able to
regain its maximum hunting capacity. Life span, however,
might be influenced by the eventual depletion of nonrenew-
able reserves or a constant rate of attrition (for a review, see
Collatz and Sohal, 1986). Anyhow, the different results of a
manipulated level of reproduction on the future rate of re-
production and on life span suggest that both factors have to
be considered when reproductive trade-offs are being ana-
lyzed.
Is the number of bees hunted a good measure of parental
investment in European beewolves?
Increased (decreased) hunting effort had negative (positive)
consequences for future reproduction and thus meets Triv-
ers’s definition of parental investment. However, the existence
of such a trade-off is a necessary but, unfortunately, not a
sufficient precondition for a valid measurement of parental
investment. In fact, one had to know the resource or process
that actually limits reproduction because natural selection
works only on the allocation of this limiting resource or pro-
cess (Rosenheim et al., 1996). Most often, the limiting factor
is assumed to be either time (see references in Heimpel et
al., 1998; Sevenster et al., 1998) or energy (e.g., Bourke and
Franks, 1995; Deerenberg et al., 1995; Kretzmann et al., 1993;
Trillmich, 1991). However, at least under certain conditions
the availability of particular substances or the rate of key pro-
cesses might become limiting (calcium for egg shell produc-
tion in a bird: Graveland and Drent, 1997; oogenesis in par-
asitoid wasps: Heimpel et al., 1998; Rosenheim, 1996; amount
of substances that suppress the host defense in parasitoid
wasps: Vass and Nappi, 1998).
The results of this study support the view that the ability to
hunt for bees is a promising candidate for a limiting process
in the European beewolf. However, other possibilities cannot
be ruled out. For example, our results could also be explained
if the venom of the wasp is assumed to be the limiting re-
source. Similar to energy reserves, it might take some time to
refill the venom reservoir after increased hunting, and fe-
males might have an excess of venom after a period of limited
bee availability. However, in the laboratory females paralyzed
on average 8.2 ⫾ 4.6 bees per day (mean ⫾ SD, range: 2–18,
n ⫽ 16) when bees were removed immediately after stinging
(Strohm and Linsenmair, 1999; E. Strohm, unpublished data).
Furthermore, Rathmayer (1962) reports that beewolf females
are able to paralyze four bees within 30 min. Thus, females
should have enough venom to paralyze more bees than they
actually did in either experiment of this study. Consequently,
it seems unlikely that the amount of venom limits hunting
success of beewolf females.
Oogenesis or the availability of chemicals that protect the
bees against fungus infestation (Strohm and Linsenmair,
2001) might be the limiting factors. However, neither expla-
nation is consistent with the decrease in hunting success after
an experimental increase of hunting effort because females
should not have had higher expenditures for eggs or for pro-
tective chemicals on the day of excessive hunting (unless
57
hunting and oogenesis or synthesis of protective chemicals
share certain resource pools, see Slansky and Scriber, 1985).
In conclusion, based on our current knowledge, the num-
ber of bees hunted provides a reasonable measure of parental
investment in the European beewolf (Strohm and Linsenmair,
1999), though some doubt remains. Ideally, the most limiting
resource or process should be identified. However, species
might differ vastly in this respect, making the identification
of the limiting factor extremely difficult (Rosenheim et al.,
1996; Strohm and Linsenmair, 1999). Nevertheless, future
studies that quantify parental investment should characterize
the measure used and at least test whether it represents costs
at all.
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We are grateful to J. Field and U. Grafe for providing valuable com-
ments on an earlier draft of the manuscript. We thank the Institute
of Agriculture, Bonn University, and the Department of Animal Phys-
iology and Sociobiology, Würzburg University, and its bee-master Mr.
Demmel for allowing us to get honeybees from their stock. We ap-
preciate the permission to investigate beewolves in the training area
and nature reserve Wahner Heide granted by the Bundesforstamt
Wahnerheide, the Belgian Army, as well as the Rhein-Sieg-Kreis.
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