Behavioral Ecology Vol. 13 No. 1: 52-58
© 2002 International Society for Behavioral Ecology
The cost of parental care: prey hunting in a digger wasp
a Theodor—Boveri—Institute for Biosciences, Würzburg University, Germany b Zoological Institute, Bonn University, Germany
Address correspondence to E. Strohm, Zoologie III, Biozentrum, Universität Würzburg, Am Hubland, D-97074 Würzburg, Germany. E-mail: strohm{at}biozentrum.uni-wuerzburg.de .
Received 3 August 2000; revised 13 March 2001; accepted 13 March 2001.
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ABSTRACT |
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Trivers's concept of parental investment is an integral part of modern evolutionary biology. "Parental investment" is defined 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.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The concept of parental investment is a fundamental element of sexual selection and investment allocation theories (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 investment" is defined as
any resource that increases the success of current progeny at the expense of a
parent's ability to reproduce in the future
(Trivers, 1972). Thus,
parental investment in a current progeny should ideally be quantified as the
parent's decrease in future reproduction. Because this is usually not
feasible, alternative measures have been used that are thought to be related
to the actual costs. However, this assumption 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 expenditures 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 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 (Hymenoptera, 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
paralyzed on flowers (Rathmayer,
1962; Tinbergen,
1935). Females carry the prey in flight to their nest, which is
constructed in open, sandy soil. Bees are temporarily stored in the main
burrow. The wasp excavates a lateral side burrow with a terminal 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 (depending on the filling
status of the honey stomach). Consequently, flying with a prey is probably the
energetically most costly part of beewolf reproduction. Furthermore, flying
activity has been shown to have negative consequences on subsequent
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 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,
observational data on the intensity of current and future reproduction were
used to assess a possible trade-off (phenotypic correlation). This method has
one major weakness. Because individuals 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 problem 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 experimentally and to determine its effect on future reproduction
(phenotypic manipulation). Finally, negative correlations on the genetic level
can be investigated by selection experiments or sib analysis (genetic
correlation; e.g., Rose and Charlesworth,
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 future reproduction. Additionally, we report
the results of a phenotypic correlation analysis. Costs might manifest
themselves either as a decreased rate of future reproduction (delay of
subsequent reproductive event or lowered reproductive output 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
subsequent hunting trips? Does an experimentally increased (decreased) 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 hunting
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.
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METHODS |
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General
Where possible, we analyzed the hunting success of beewolf females using matched-pairs designs. We matched pairs of experimental and control females with regard to as many relevant factors as possible (size, age, location, and microclimate of nest site). Assignment of a female to experimental or control group was random. Because sample sizes did not allow us to reasonably test for assumptions of parametric tests, we calculated 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 somewhat 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 corrected
(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 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 x 2 x 2 m) where they could nest in a sand
compartment at one narrow side of the cage
(Strohm and Linsenmair, 1997).
Females were observed for their entire daily activity 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 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 durations 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 expenditure for
prey hunting should cause a decrease in the hunting success on the following
day. In the field, the expenditure 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
removed 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 females were pairwise
matched (from the same generation, difference in head width < 0.1 mm, nests
less than 2 m apart from each other with identical exposition and shading).
Ambient temperature differed less than 2° during the experimental period
of 3 days. The experiment was conducted in three different trials (3-day
experimental period) with 6-7 experimental 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 actually bring in more bees than they would have if not manipulated. 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 compared 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 manipulation, 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).
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 pairwise 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 provided
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 generation, difference in head width < 0.1 mm). All
females were individually housed in cages that consisted of a sand-filled
compartment (30 x 20 x 25 cm) and a flight compartment (gauze
cage, 30 x 20 x 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 distributed in the room. Control females were provided
with bees ad libitum (at least one bee was available throughout the activity
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 possible 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
success of experimental females versus control females (experimental/control)
on the first day of unrestricted bee availability.
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 females were kept in a large indoor flight cage (1
x d x h = 4 x 2 x 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 (1
x d x h = 1.2 x 0.8 x 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 confounding variable that obscures a possible
trade-off because hunting success is positively correlated with size
(Strohm and Linsenmair, 1997).
Because life span is a time event variable, it is probably not normally
distributed (Abacus Concepts,
1994). Therefore, we analyzed the data using survival analysis
procedures (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 significantly 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. Females 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.
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RESULTS |
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Hunting of loaded bees
Females needed on average 77% more time to bring in a loaded 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 expenditure 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.
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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 manipulation (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).
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On day 3 (day after manipulation) experimental females 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 success on day 3. Female size had no significant effect on the decrease of hunting success on day 3 relative to day 1 (Spearman 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 control 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 during the observation period. Female size had no significant
effect on the ratio of hunting success of an experimental female 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) experimental
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 control females on the first day of unrestricted bee availability (Spearman
rank correlation: rs =.25, n = 10, p
=.48).
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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).
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DISCUSSION |
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Current and future hunting effort
All experiments that manipulated a female's hunting effort revealed some negative relationship between current and future hunting success. Females delayed subsequent hunting trips after bringing in loaded bees, thus lowering the subsequent 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 success on the following day. In all experiments, the relative increase (decrease) of hunting success was independent of size. These results suggest that hunting is costly in terms of reduced hunting success.
However, the increase of hunting success after caging in the field might have two alternative explanations. First, because experimental female 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. Second, 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 females might have had a strong motivation to bring in bees and oviposit on the day after caging. Both alternative explanations 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 negative effect of
current on future hunting success? Unfortunately, the physiological processes
underlying trade-offs are poorly understood (but see
Nilsson and Svensson, 1996).
Our data suggest that in beewolves the negative effect of decreased hunting
activity is reversible and lasts for about 1 day. Generally, there might be
two nonexclusive explanations. For both there is only little information
available in insects. First, exhaustive 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 reserves (probably glycogen) might be depleted, and replenishing the
stores might take some time (Johnson and
Rowley, 1972; Neukirch,
1982). However, honeybees flown to exhaustion resumed flight about
10 min after feeding on sugar solutions (e.g.,
Crailsheim, 1988;
Loh and Heran, 1970),
suggesting that depletion of energy should not have effects that last for
about 1 day.
The result that females are able to hunt more bees than they would have without manipulation suggests that they usually 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
positive effect of a restricted availability of prey (1 bee per day versus ad
libitum) on life span. We first discuss the nonexistence 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 Sohal,
1986). Because our results are from females kept in the
laboratory, several factors differed from the field. Most important, the
distance flown with the bee was probably considerably 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 laboratory. 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 reproduction and life
span, similar to what we have found in beewolves, were observed in a lace bug.
Brood care (guarding of the eggs and larvae) caused a reduction in the rate of
oviposition but did not reduce life span
(Tallamy and Denno, 1982; see
Roff, 1992, for differing
examples). Why is the future 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 nonrenewable 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 reproduction and on life span suggest
that both factors have to be considered when reproductive trade-offs are being
analyzed.
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 Trivers'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 process
(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 processes might become limiting
(calcium for egg shell production in a bird:
Graveland and Drent, 1997;
oogenesis in parasitoid 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
resource. Similar to energy reserves, it might take some time to refill the
venom reservoir after increased hunting, and females 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 explanation
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 protective chemicals on the day of excessive
hunting (unless 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 number 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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ACKNOWLEDGEMENTS |
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We are grateful to J. Field and U. Grafe for providing valuable comments on an earlier draft of the manuscript. We thank the Institute of Agriculture, Bonn University, and the Department of Animal Physiology and Sociobiology, Würzburg University, and its bee-master Mr. Demmel for allowing us to get honeybees from their stock. We appreciate 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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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Abacus Concepts, 1994. Survival tools for Statview. Berkeley, California: Abacus Concepts Inc.
Bailey RC, 1992. Why we should stop trying to measure the cost of reproduction correctly. Oikos 65: 349-352.[Web of Science]
Bérubé
CH, Festa-Bianchet M, Jorgenson JT, 1996. Reproductive costs of
sons and daughters in Rocky Mountain bighorn sheep. Behav Ecol
7: 60-68.
Bourke AFG, Franks NR, 1995. Social evolution in ants. Princeton, New Jersey: Princeton University Press.
Brockmann HJ, Grafen A, 1992. Sex ratio and life-history patterns of a solitary wasp, Trypoxylon (Trypargilum) politum (Hymenoptera: Sphecidae). Behav Ecol Sociobiol 30: 7-27.[Web of Science]
Cameron EZ, 1998. Is suckling a useful predictor of milk intake? A review. Anim Behav 56: 521-532.[Web of Science][Medline]
Casey TM, 1992. Energetics of locomotion. Adv Comp Environ Physiol 11: 251-275.
Clutton-Brock TH, 1991. The evolution of parental care. Princeton, New Jersey: Princeton University Press.
Collatz KG, Sohal RS (eds), 1986. Insect ageing. Strategies and mechanisms. Heidelberg: Springer Verlag.
Collatz KG, Wilps H, 1986. Ageing of flight mechanism. In: Insect ageing (Collatz KG, Sohal RS, eds). Berlin: Springer Verlag; 55-72.
Collier TR, 1995. Host feeding, egg maturation, resorption, and longevity in the parasitoid Aphytis melinus (Hymenoptera: Aphelinidae). Ann Entomol Soc Am 88: 206-214.[Web of Science]
Crailsheim K, 1988. Intestinal transport of sugars in the honeybee (Apis mellifera). J Insect Physiol 34: 839-845.
Deerenberg C, Pen I, Dijkstra C, Arkies BJ, Visser GH, Daan S, 1995. Parental energy expenditure in relation to manipulated brood size in the European kestrel Falco tinnunculus. Zoology 99: 39-48.
Graveland J, Drent R, 1997. Calcium availability limits breeding success of passerines in poor soils. J Anim Ecol 66: 279-288.
Heimpel G, Mangel M, Rosenheim J, 1998. Effects of time limitation and egg limitation on lifetime reproductive success of a parasitoid in the field. Am Nat 152: 273-289.[Web of Science][Medline]
Hoffmeister H, 1961. Morpholgische Beobachtungen an erschöpften indirekten Flugmuskeln der Wespe. Z Zellforsch 54: 402-420.[Web of Science]
Hoffmeister H, 1962. Beobachtungen an indirekten Flugmuskeln der Wespe nach Erholung von erschöpfendem Dauerflug. Z Zellforsch 56: 809-818.
Johnson BG, Rowley WA, 1972. Ultrastructural changes in Culex tarsalis flight muscle associated with exhaustive flight. J Insect Physiol 18: 2391-2399.[Web of Science][Medline]
Kammer AE, Heinrich B, 1978. Insect flight metabolism. Adv Insect Physiol 13: 133-225.
Kretzmann M, Costa D, Le Boeuf B, 1993. Maternal energy investment in elephant seal pups: evidence for sexual equality? Am Nat 141: 466-480.[Web of Science]
Lenteren J C van, Vianen A van, Gast HF, Kortenhoff A, 1987. The parasite-host relationship between Encarsia formosa Gahan (Hymenoptera: Aphelinidae) and Trialeurodes vaporariorum (Westwood) (Homoptera: Aleyrodidae) XVI. Food effects on oogenesis, oviposition, life-span and fecundity of Encarsia formosa and other hymenopterous parasites. J Appl Entomol 103: 69-84.
Lessells CM, 1991. The evolution of life histories. In: Behavioral ecology (Krebs J, Davies N, ed). Oxford: Blackwell; 32-68.
Loh W, Heran H, 1970. Wie gut können Bienen Saccharose, Glucose, Fructose und Sorbit im Flugstoffwechsel verwerten? Z Vergl Physiol 67: 436-452.
Messina FJ, Slade AF, 1999. Expression of a life history trade-off in a seed beetle depends on environmental context. Physiol Entomol 24: 358-363.
Nalepa CA, 1988. Cost of parental care in the woodroach Cryptocercus punctulatus Scudder (Dictyoptera:Cryptocercidae). Behav Ecol Sociobiol 23: 135-140.[Web of Science]
Neukirch A, 1982. Dependence of the life span of the honeybee (Apis mellifera) upon flight performance and energy consumption. J Comp Physiol 146: 35-40.
Nilsson J-A, Svensson E, 1996. The cost of
reproduction: a new link between current reproductive effort and future
reproductive success. Proc R Soc Lond B
263: 711-714.
Nonacs P, 1986. Ant reproductive strategies and sex allocation theory. Q Rev Biol 61: 1-21.
Partridge L, 1986. Sexual activity and life span. In: Insect aging (Collatz K-G, Sohal RS, ed). Berlin: Springer-Verlag; 45-54.
Rathmayer W, 1962. Paralysis caused by the digger wasp Philanthus. Nature 196: 1149-1151.
Rice W, 1989. Analyzing tables of statistical tests. Evolution 43: 223-225.[Web of Science]
Roff DA, 1992. The evolution of life histories. New York: Chapman and Hall.
Rose M, Charlesworth B, 1981a. Genetics of
life-history in Drosophila melanogaster. I. Sib analysis of adult
females. Genetics 97:
187-196.
Rose M, Charlesworth B, 1981b. Genetics of life-history in Drosophila melanogaster II. Exploratory selection experiments. Genetics 97: 187-196.
Rosenheim J, 1996. An evolutionary argument for egg limitation. Evolution 50: 2089-2094.[Web of Science]
Rosenheim JA, Nonacs P, Mangel M, 1996. Sex ratios and multifaceted investment. Am Nat 148: 501-535.[Web of Science]
Sahragard A, Jervis MA, Kidd NAC, 1991. Influence of
host availability on rates of oviposition and host-feeding, and on longevity
in Dicondylus indianus Olmi (Hym., Dryinidae), a parasitoid of the
rice brown planthopper, Nilaparvata lugens
St
l (Hem., Delphacidae). J Appl
Entomol 112:
153-162.
Sevenster JG, Ellers J, Driessen G, 1998. An evolutionary argument for time limitation. Evol 52: 1241-1244.
Sinervo B, DeNardo DF, 1996. Costs of reproduction in the wild: path analysis of natural selection and experimental tests of causation. Evolution 50: 1299-1313.[Web of Science]
Slansky F, Scriber J, 1985. Food consumption and utilization. In: Comprehensive insect physiology, biochemistry, and pharmacology (Kerkut G, Gilbert L, eds). Oxford: Pergamon Press; 87-161.
Strohm E, 1995. Allokation elterlicher Investitionen beim Europäischen Bienenwolf Philanthus triangulum Fabricius (Hymenoptera: Sphecidae). Berlin: Verlag Dr. Köster.
Strohm E, Lechner K, 2000. Male size does not affect territorial behaviour and life history traits in a sphecid wasp. Anim Behav 59: 183-191.[Web of Science][Medline]
Strohm E, Linsenmair KE, 1997. Female size affects provisioning and sex allocation in a digger wasp. Anim Behav 54: 23-34.[Web of Science][Medline]
Strohm E, Linsenmair KE, 1998. Temperature dependence of provisioning and investment allocation of females in the European beewolf Philanthus triangulum F. (Hymenoptera: Sphecidae). Ecol Entomol 23: 330-339.
Strohm E, Linsenmair KE, 1999. The measurement of parental investment and sex allocation in the European beewolf Philanthus triangulum F. (Hymenoptera: Sphecidae). Behav Ecol Sociobiol 47: 76-88.[Web of Science]
Strohm E, Linsenmair KE, 2000. Allocation of parental investment among individual progeny in the European beewolf Philanthus triangulum F. (Hymenoptera, Sphecidae). Biol J Linn Soc 69: 173-192.
Strohm E, Linsenmair KE, 2001. Females of the European beewolf preserve their honeybee prey against competing fungi. Ecol Entomol. 26: 198-203.
Tallamy DW, Denno RF, 1982. Life history trade-offs in Gargaphia solani (Hemiptera: Tingidae): the cost of reproduction. Ecology 63: 616-620.[Web of Science]
Tallamy DW, Schaefer C, 1997. Maternal care in the Hemiptera: ancestry, alternatives, and adaptive value. In: The evolution of social behavior in insects and arachnids (Choe JC, Crespi BJ eds). Cambridge: Cambridge University Press; 94-115.
Tinbergen N, 1932. Über die Orientierung des Bienenwolfes (Philanthus triangulum Fabr.). Z Vergl Physiol 16: 305-335.
Tinbergen N, 1935. Über die Orientierung des Bienenwolfes II. Die Bienenjagd. Z Vergl Physiol 21: 699-716.
Trillmich F, 1991. Energetic limits to brood care: influences on fertility and longterm fitness consequences. In: Verhandlungen der Deutschen Zoologischen Gesellschaft, 1991 in Tübingen, (Pfannenstiel H-D ed). Stuttgart: Fischer; 79-87.
Trivers RL, 1972. Parental investment and sexual selection. In: Sexual selection and the descent of man, (Campbell B, ed). Chicago: Aldine; 136-179.
Trivers RL, Hare H, 1976. Haplodiploidy and the
evolution of the social insects. Science
191: 249-263.
van Nordwijk AJ, de Jong G, 1986. Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128: 137-142.[Web of Science]
Vass E, Nappi AJ, 1998. Prolonged oviposition decreases the ability of the parasitoid Leptopilina boulardi to suppress the cellular immune response of its host Drososphila melanogaster. Exp Parasitol 89: 86-91.[Web of Science][Medline]
Wegener G, 1996. Flying insects: model systems in exercise physiology. Experientia 52: 404-412.[Web of Science][Medline]
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