ANIMAL BEHAVIOUR, 2008, 75, 809e816

doi:10.1016/j.anbehav.2007.06.018

Available online at www.sciencedirect.com

Production of undersized offspring in a solitary bee

JOR DI B OSC H* †
*Ecologia-CREAF, Universitat Autònoma de Barcelona, Bellaterra
yDepartament de Biologia Animal, Universitat de Barcelona, Barcelona

(Received 18 December 2006; initial acceptance 2 March 2007;

final acceptance 20 June 2007; published online 23 October 2007; MS. number: 9217R)

As predicted by Conditional Sex Allocation Theory, females of the solitary bee Osmia cornuta exposed to
scarce floral resources biased their progeny sex ratio towards males, the least costly sex, and produced
smaller-than-average females. Surprisingly, nesting females also produced a number of ‘tiny’ offspring,
which contrasted with regular-sized offspring within the same nest. Developmental and wintering mortal-
ity are strongly size dependent in O. cornuta, and a high proportion of tiny offspring did not survive. This
result is in disagreement with Optimal Allocation Theory, according to which resources should be allocated
in portions that maximize fitness returns. I ask why did O. cornuta females build tiny provisions and why
did they lay female eggs (with lower survival probability than male eggs) on these provisions. I argue that
egg maturation rates and selective pressure to avoid kleptoparasitism and provision desiccation in cells left
unsealed for long periods may impose a limit to the time available for cell provisioning. Under low food
availability, this limit will be reached before provision sizes resulting in maximum fitness returns are at-
tained. I also argue that the decision to fertilize an egg (and thus produce a female) is made at the begin-
ning of the cell-provisioning process, so that females cannot adjust offspring sex to provision size. At the
same time, altering the femaleemale cell sequence within a nest would result in fratricide because of
protandric emergence. I provide evidence supporting these ecological and physiological constraints on
resource allocation decisions in O. cornuta.

Ó 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Keywords: body size; conditional sex allocation; Megachilidae; optimal allocation theory; Osmia cornuta; parental invest-
ment; sex ratio; solitary bee

In panmictic populations, parental investment should be
equally allocated to male and female progeny (Fisher
1958). Thus, only when sons and daughters are equally
costly is a sex ratio of unity expected. However, subse-
quent elaboration of Fisher’s theory indicates that system-
atic deviations from equal investment in both sexes are to
be expected under certain conditions, notably under low-
resource availability. These deviations would be most
likely if parents were able to respond to resource availabil-
ity by adjusting the sex ratio of their progeny and/or the
amount of parental investment per individual offspring
according to offspring sex. Conditional Sex Allocation
Theory (henceforth, CSAT; Trivers & Willard 1973;
Charnov 1982; Frank & Swingland 1988) predicts that
under poor conditions (e.g. limited food resource
Correspondence: J. Bosch, Ecologia-CREAF, Edifici C, Universitat
Autònoma de Barcelona, 08193 Bellaterra, Spain (email: Jordi.
Bosch@uab.es).
809
0003e 3472/08/$32.00/0 Ó 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
availability) parents should emphasize the production of
the least costly sex. A prerequisite of CSAT is that sons
and daughters differ in the shape or position of their fit-
ness-investment curves (Frank 1987). If so, selection
should favour those parents biasing their investment to-
wards the sex yielding higher fitness returns under low in-
vestment. Failure to do so would result in the production
of offspring with low fitness, a situation which would
conflict with Optimal Allocation Theory (OAT). Optimal
Allocation Theory (OAT) establishes an optimum amount
of investment per offspring at which fitness returns are
maximized, and parents are expected to allocate invest-
ment among their progeny in portions as close as possible
to this optimum (Smith & Fretwell 1974). Optimal Alloca-
tion Theory (OAT) relies on two key assumptions. First,
increased investment per offspring results in increased
offspring fitness. Second, resources for investment in
reproduction are finite, resulting in a trade-off between
offspring number and amount of resources invested in
each offspring (often referred to as brood number versus
810 ANIMAL BEHAVIOUR, 75, 3
size trade-off). A corollary of OAT is that under low-
resource availability parents should be more prone to
reduce their fecundity than the amount of investment
per individual offspring.
The model of Smith & Fretwell (1974) is static in that it
assumes a constant environment and no influence of
offspring number on offspring fitness. In nature, most
environments are heterogeneous, and the shape of the
fitness-investment curve may differ in different environ-
ments (Carriere & Roff 1995). In fact, variation in invest-
ment per offspring (often measured as egg size) is the
norm, not only between populations within a species,
but also between females within a population and even
among offspring produced by a single female (Bernardo
1996; Fox & Csezak 2000). Theoretical models subsequent
to Smith & Fretwell’s have attempted to explain this
variability by accounting for heterogeneity in the proge-
ny’s and/or the parent’s environment. Thus, the optimal
amount of per offspring investment may be dependent
on offspring density and competition among siblings
(Parker & Begon 1986; McGinley et al. 1987), temporal
and spatial heterogeneity in resources available to the
parents (van Noordwijk & de Jong 1986; Lalonde 1991;
Venable 1992), and total reproductive effort per parent
(Winkler & Wallin 1987). For example, larger eggs are usu-
ally produced under adverse conditions, such as crowded
environments (Perrin 1989; Kawecki 1995), or on poor
quality hosts (Fox 2000), and it is under these adverse
environments that fitness differences between large and
small eggs are greatest (Fox & Mousseau 1998). Alterna-
tively, variation in investment per offspring may largely
be nonadaptive (Fox & Czesak 2000). Morphological and
physiological constraints may limit the parent’s ability
to control egg size or amount of resources invested per
offspring (Congdon & Gibbons 1987; Fox 1993; Bernardo
1996).
In species in which offspring survival is investment
dependent, and in which investment-fitness optima differ
for sons and daughters, parents facing a situation of low-
resource availability could adjust their investment strategy
in one of three ways. First, parents could bias the sex ratio
of their progeny towards the least costly sex, as predicted
by CSAT. This would allow these parents to maintain
brood number and investment per offspring. Offspring
survival would not be compromised, but the capacity of
the overproduced sex to sire progeny would decrease if all
parents in the population followed this strategy. Second,
in agreement with OAT, parents could maintain progeny
sex ratio and resource investment per offspring, at the cost
of reducing brood number. Third, parents could maintain
brood number and progeny sex ratio, but then would
have to lower investment per offspring, which would
result in diminished offspring fitness.
Nesting solitary bees and wasps are appropriate systems
for the study of parental investment strategies because
females (males do not participate in nest construction or
provisioning) have a high degree of control over both the
sex and size of their progeny. Most species mass-provision
their nests with discrete amounts of food individually
allocated to each offspring, and therefore food investment
in each sex can be accurately measured and used as an
estimator of parental investment. Females can determine
the sex of their offspring by controlling the release of
sperm from the spermatheca and produce either daugh-
ters (fertilized eggs) or sons (unfertilized eggs; Gerber &
Klostermeyer 1970). Offspring body size has only moder-
ate heritability (Tepedino et al. 1984; Frohlich & Tepedino
1986), but is highly correlated with provision weight
(Klostermeyer et al. 1973; Strohm 2000; Bosch & Vicens
2002).
To my knowledge, CSAT has been tested in three
solitary aculeate Hymenoptera, the beewolf wasp Philantus
triangulum, and two leaf cutting bees, Megachile apicalis
and Megachile rotundata (Strohm & Linsenmair 1997;
Kim 1999; Peterson & Roitberg 2006). In all three species,
female offspring are allocated larger food provisions and
thus grow larger than males. In the first two studies, nest-
ing females were kept in laboratory cages in which food
levels were manipulated. Females responded to decreased
food availability by biasing their progeny sex ratio towards
males, and reducing food investment (and thus body size)
of offspring of one sex (males in P. triangulum, females in
M. apicalis). In the third study, which was conducted in
the open, forage plots were located at various distances
from nesting sites. Females that had to fly longer distances
to forage produced a greater proportion of sons and
smaller offspring of both sexes. Body size reductions in
the two Megachile species were approximately 1.1-fold
(Kim 1999; Peterson & Roitberg 2006). In P. triangulum,
an eight-fold food availability reduction resulted in
a two-fold reduction in investment per male offspring
(Strohm & Linsenmair 1997). In agreement with OAT,
no females were produced under manipulated low or
very low-resource availability in this species (Strohm &
Linsenmair 1997), and in wild populations most female
cells were provisioned with optimal amounts of food
(Strohm & Linsenmair 2000). In this article, I report
a very significant reduction (1.4-fold) in female offspring
body size in a free-flying population of the solitary bee
Osmia cornuta exposed to low-resource availability. I also
report a significant increase in the frequency of offspring
of both sexes that were allocated unusually small amounts
of provision. These results are relevant because, as
reported below, fitness is highly size-dependent in this
species, and thus the results are in strong disagreement
with OAT. Because body size reduction affected mostly
females, female mortality was unusually high and resulted
in a strongly male-biased secondary sex ratio. The objec-
tive of the study is to describe these findings and propose
ecological and physiological constraints that would
explain this seemingly nonoptimal resource allocation.
METHODS
Osmia cornuta is a univoltine, cavity-nesting, spring-flying
solitary bee in the family Megachilidae. Females build
nests consisting of linear series of cells delimited by mud
partitions and containing one pollenenectar provision
and one egg each. Offspring body size is a good estimator
of parental investment in O. cornuta (Bosch & Vicens
2002, 2005). A 2-year field study in which resource
 BOSCH: UNDERSIZED OFFSPRING IN A SOLITARY BEE 811

availability was not manipulated, showed that free-flying
females allocated parental resources in complete agree-
ment with Fisher’s theory (Bosch & Vicens 2005). Sex allo-
cation was 1:1 in both years, regardless of the currency
used to measure parental investment (provision weight or
nesting female foraging time). Offspring sex ratio and body
size of either sex did not vary between years (Bosch &
Vicens 2005).
In 1990e1992, I released three O. cornuta populations
(one per year) in an almond orchard in Mas Bové (Reus,
NE Spain). A detailed account of the methods used is
found in Bosch & Vicens (2006). Females were individu-
ally marked and nesting was monitored daily throughout
the nesting period. In 1990 and 1992, bees were released
in mid-February, at peak bloom of early-flowering almond
cultivars. Conversely, in 1991 bees were released in early
March, at peak bloom of late-flowering cultivars, so that
floral resources in the vicinity of the nesting site became
quickly scarce. The progeny obtained were reared to adult-
hood. To assess the effect of body size on developmental
mortality three offspring weight classes were established:
large (females and males with weights above yearly female
and male average, respectively; see Table 1), small (females
and males below yearly average) and tiny (females
weighing <70 mg, and males weighing <50 mg). Tiny
individuals were unusually small, and contrasted with
regular-sized individuals found in adjacent cells within
the nest.
For each female, I measured the following variables:
nesting period (days between first and last cells produced),
foraging time (proportion of daily time with weather
favourable to O. cornuta activity; Vicens & Bosch 2000),
provisioning rate (progeny weight produced per hour of
foraging activity), fecundity (total number of cells pro-
duced), parental investment (total progeny weight pro-
duced), and mean weight of male and female offspring.
Differences among years in these variables were analysed
with one-way analysis of variance (ANOVA). Data were
not transformed because residuals showed an approxi-
mately even distribution, indicating variance homogene-
ity. I used the Chi-squared test to analyse differences
among years in progeny sex ratio, frequency of tiny off-
spring, and male and female mortality. Developmental
mortality (other than parasitism) was analysed as a func-
tion of year and size class with Logit analysis.
RESULTS
Floral resources other than almond were sparse in Mas
Bové, and thus provisioning rates (progeny weight
produced per hour of foraging activity) were significantly
lower in 1991 (Table 1). By contrast, mean nesting period
(days with nesting activity) and fecundity (number of cells
built per nesting female) were similar across years (Table 1).
In 1991, overall parental investment (progeny weight pro-
duced per nesting female) was 8.3% lower than in 1990,
and 21.1% lower than in 1992, but variability among
females within a year was high (1990: 1435e25 743 mg;
1991: 471e24 874 mg; 1992: 1790e32 129 mg), and
differences across years were not significant (Table 1).
Primary progeny sex ratios (_ produced/\ produced)
were higher in 1991 and 1992 than in 1990 (Table 1). In
1992, the nesting period was punctuated by frequent
spells of bad weather, as reflected in the low foraging
time obtained in that year (Table 1). Male-biased sex ratios

Table 1. Osmia cornuta parental investment and progeny mortality in Mas Bové in 1990, 1991 and 1992
1990 1991 1992 Statistic P

Release date 21 February 8 March 18 February d d

Females established 29 37 29 d d
Nesting period* 11.31.1 13.61.8 15.01.3 F¼1.43 0.2
Foraging timey 0.690.01 0.740.01 0.560.02 F¼37.09 0.0001
Provisioning ratez 16.61.3 12.50.7 16.51.1 F¼5.35 0.006
Cells/female 8.50.9 9.51.1 10.41.1 F¼0.73 0.4
Progeny weightx/female 1195.2121.7 1096.2123.7 1389.5165.3 F¼1.19 0.3
Cells produced 247 352 302 d d
Primary sex ratio (_/\) 1.98 3.46 3.38 c2¼11.34 0.004
Sex allocation (_/\)** 1.13 2.61 1.82 d d
_ Offspring weightx 115.85.5 105.93.0 112.72.5 F¼1.80 0.1
\ Offspring weightx 192.27.8 140.312.0 204.96.7 F¼12.59 0.0001
Tiny offspringyy 5 (2.0%) 33 (9.4%) 5 (1.7%) c2¼60.94 0.0001
Cell-provisioning time*,zz 1.30.6 1.10.6 1.30.7 F¼1.50 0.2
_ Developmental mortality 15 (9.1%) 41 (15.0%) 29 (12.4%) c2¼3.2 0.2
\ Developmental mortality 5 (6.0%) 15 (19.0%) 1 (1.5%) c2¼15.2 0.0005
Parasitism 1 (0.40%) 10 (2.84%) 57 (18.9%) c2¼82.3 0.0001
Secondary sex ratio (_/\) 1.94 4.78 2.77 c2¼12.2 0.002

All means followed by SE.

*In days.
yProportion of daily time with weather favourable to O. cornuta activity (Vicens & Bosch 2000).
zProgeny weight (in mg) produced per hour with weather favourable to O. cornuta activity.
xIn milligrams.
**Total weight of male progeny produced/total weight of female progeny produced.
yyFemales weighing <70 mg and males weighing <50 mg.
zzTime required to provision a cell.
812 ANIMAL BEHAVIOUR, 75, 3
Table 2. Logit analysis on the effect of year and size class on devel-
opmental mortality
Large Small Tiny
Developmental mortality 3.5% 9.4% 44.2%
Logit analysis df Wald c2 P reducing fitness returns of investment in small female off-
Year 2 4.2 >0.1
Size 2 57.7 <0.0000001
Year*size 4 7.5 >0.1
in Osmia are common in years with bad weather (Tepe-
dino & Torchio 1982a). However, climatic conditions
were most favourable in 1991, and thus the strongly
male-biased sex ratio obtained in this year cannot be
attributed to inclement weather. Mean weight of male off-
spring was similar across years, but mean weight of female
offspring was significantly lower in 1991 (Table 1). As a
result, despite similar sex ratios in 1991 and 1992, sex
allocation (total weight of male progeny produced/total
weight of female progeny produced) was 1.4 times higher
in 1991 (Table 1). Tiny offspring were more frequent in
1991 than in the other 2 years (Table 1). Recalculation
of mean male and female offspring weights excluding
tiny progeny still yields significant differences among
years in female offspring weight, with 1991 scoring lowest
(F2,69 ¼ 3.70, P ¼ 0.03) and not in male offspring weight
(F2,83 ¼ 1.38, P > 0.2).
Male developmental failure was similar across years, but
a larger proportion of females died in 1991 compared with
the other 2 years (Table 1). Developmental mortality was
strongly dependent on class size, with as many as 44.2%
of tiny offspring not surviving to adulthood (Table 2). Dif-
ferences in mortality among size classes remained signifi-
cant even when tiny individuals were excluded from the
calculations (Wald c21 ¼ 11.2, P < 0.0009). Parasitism was
very low in 1990 and 1991, but high in 1992 (Table 1).
Most parasitism was due to the chalcid wasp Monodonto-
merus aeneus and occurred during incubation in the labo-
ratory, when nests were removed from the nesting blocks.
Parasitism did not differ among offspring size classes
(c21 ¼ 0.7, P > 0.7; tiny individuals excluded because
most died before cocoon spinning and M. aeneus does
not parasitize noncocooned hosts). Secondary progeny
sex ratio (calculated excluding individuals lost to parasit-
ism or developmental failure) was more male biased
than primary sex ratio only in 1991, when it reached
values as high as 4.5 males per female (Table 1).
DISCUSSION
Osmia cornuta females exposed to low resource availability
expressed low provisioning rates. These females did not
decrease their fecundity and, in agreement with CSAT, em-
phasized the production of the least costly sex. However,
these females also reduced the size of their progeny, which
led to a dramatic increase in developmental mortality.
I did not measure overwintering mortality, but previous
studies show that small O. cornuta individuals are more
likely to die during the winter, and that those surviving
to emergence are less vigorous (Bosch & Kemp 2004),
which would further bias secondary sex ratio in 1991.
Small females are also less likely to establish at their natal
nesting site, and, at least in some years, have lower provi-
sioning rates and produce male-biased progenies com-
pared with large females (Bosch & Vicens 2006), further
spring. Of particular interest is the production of tiny
progeny. It is unclear whether tiny offspring could have
any reproductive success at all. Of the 217 females released
in this study (3 years combined), five were tiny, indicating
that some tiny individuals do not only reach adulthood,
but also survive the winter. However, none of these five fe-
males nested. These results are in strong disagreement
with OAT predictions, and raise two important questions:
(1) Why did females of 1991 not increase provision size?
(2) Even if unable to increase provision size, why did these
females lay female eggs on small provisions, rather than
male eggs, which would have a higher probability of
survival?
Why not Increase Provision Size?
At least theoretically, females under low pollenenectar
availability should be able to build large provisions. It
would just take them longer. I find two possible explana-
tions as to why females would be constrained to lay an egg
(male or female) on an undersized provision.
Risk of mortality
The first explanation relates to increased risk of mortal-
ity when cells are left unsealed for long periods of time.
Large provisions require more time away from the nest,
especially when, as in 1991, provisioning rates are low.
Cells left unsealed for long periods have a higher
likelihood of being parasitized by Cacoxenus indagator. Al-
though not found in this study, C. indagator is a common
kleptoparasite in wild O. cornuta populations throughout
its distribution range (Coutin & Desmier de Chenon
1983; Westrich 1989; Felicioli 2000; Krunic & Stanisavl-
jevic 2006), including the area in which the parental pop-
ulation of this study was obtained (Bosch 1992). In Osmia
pumila, parasitism by another kleptoparasite, Sapyga
centrata, was much higher in cages with sparse bloom
compared with cages with rich bloom (Goodell 2003). In
Osmia rufa, kleptoparasitism by C. indagator and Anthrax
anthrax was positively correlated to cell-provisioning
time, and was interpreted as the main factor determining
provision size reduction in ageing females with low forag-
ing efficiency (Seidelmann 2006). When numerous C. in-
dagator eggs are laid in an Osmia cell, the larvae of the
kleptoparasite break through cell partitions and may end
up parasitizing the entire nest. Thus, selection against
leaving a cell unsealed for long periods is likely to be
strong in O. cornuta.
Partially built provisions in cells unsealed for long
periods are also exposed to increased evaporation, possibly
compromising immature survival. In 1991, the year with
highest developmental mortality, cell-provisioning time

was higher in cells whose offspring failed to develop
(1.59  0.15 days; N ¼ 46) than in cells producing surviv-
ing offspring (1.07  0.06 days; N ¼ 272; ManneWhitney
test: U ¼ 3.40; P < 0.0003). In Osmia lignaria, offspring
mortality increased when young larvae had difficulty bit-
ing through the hard surface of provisions that received
insufficient nectar in a year with sparse floral resources
(Torchio 1985).
Finally, O. cornuta females foraging for long periods are
at increased risk of predation, especially by birds (Felicioli
2000). In bumblebee workers, mortality was correlated to
foraging frequency (Silva-Matos & Garófalo 2000). If this
hypothesis was correct, we would expect slow-working
females to be more likely to be compelled to lay eggs on
tiny provisions. Females that produced one or more tiny
offspring had lower provisioning rates (12.3  0.9 mg/h)
than females not producing tiny offspring (16.0 
0.8 mg/h; one-tailed t test: t93 ¼ 2.76, P ¼ 0.004).
Egg maturation rates
A second explanation for decreased provision size re-
lates to physiological constraints of egg maturation rates.
Osmia females have two ovaries with three ovarioles each
(Maeta & Kurihara 1971). Oocytes mature in succession,
so that at any given time during the nesting period one
of the basal oocytes is mature or close to maturity, and
the remaining oocytes are in different stages of matura-
tion. In natural conditions, females lay no more than
one egg a day on average (Torchio 1989; Bosch & Vicens
2005). Under particularly favourable conditions (e.g. in
greenhouses stocked with abundant floral resources)
females can lay a mean of two eggs per day (Tepedino &
Torchio 1982b; Torchio 1989; J. Bosch & W. P. Kemp,
unpublished data). These results indicate that, in
situations of abundant floral resources, cell production is
limited by provisioning rate, not by egg maturation.
However, females may not be able to hold a mature egg
beyond a certain time without compromising its viability
and/or the timing of maturation of subsequent oocytes in
relation to provision completion. If so, females under low
pollenenectar availability would be constrained to lay
eggs on undersized provisions. In fact, despite provision-
ing rate being lower in 1991, cell-provisioning time
(time between two consecutive ovipositions) did not
vary among years.
If this hypothesis was correct, we would expect to find
more tiny offspring in the first cells within a nest than in
other cells. Upon laying the last egg within a nest, a female
needs to build a cell partition, one or two optional
vestibular partitions (w1.5 to 2 times thicker than regular
partitions; Bosch & Vicens 2005), a mud cap (w4.5 times
thicker than a regular partition), select a new nesting cav-
ity (which may take several hours), usually build a basal
partition (w1.5 times thicker than a regular partition),
and gather a new provision before laying the next egg.
By contrast, upon laying an egg that is not the last one
within a nest, females only need to build a regular parti-
tion and provision a new cell before laying the next egg.
Most (58.1%) of the tiny offspring produced were located
in the first cell of second- or third-constructed nests. If the
BOSCH: UNDERSIZED OFFSPRING IN A SOLITARY BEE 813
hypothesis that, when resources are not abundant, egg
maturation rates, rather than provisioning rates, dictate
the tempo of cell completion was correct, we would also
expect time between two consecutive ovipositions to be
longer when the second egg was laid on a tiny provision,
as females would hold that egg for as long as possible in an
attempt to collect a sufficient amount of pollen and nec-
tar. Cell completion time was longer for cells with tiny
provisions (1.83  0.28 days; N ¼ 29) than for cells with
small (1.25  0.06 days; N ¼ 319) or large provisions
(1.11  0.04 days; N ¼ 413; KruskaleWallis test: H ¼
6.61; P < 0.02). This pattern was also evident when cell
completion times of consecutively built cells within
a nest were compared (tiny provisions: 2.05  0.34 days;
normal (large or small) provisions: 0.82  0.17 days; Wil-
coxon test: T ¼ 2.41, P < 0.02; N ¼ 22). As mentioned,
slow-working females were more likely to produce tiny
offspring, which would also agree with this hypothesis.
The fact that neither O. cornuta, nor P. triangulum, M. api-
calis or O. pumila (Strohm & Linsenmair 1997; Kim 1999;
Goodell 2003) reduced their fecundity (number of eggs
laid per female) in low-resource environments, is a further
indication that, under these circumstances, cell comple-
tion rate may be dictated by egg maturation. However,
M. apicalis forced to fly long distances did reduce their
fecundity (Peterson & Roitberg 2006).
Rosenheim et al. (1996) point out that parental
investment is dependent on more than one resource
(provisions, mature oocytes, nesting sites), and that the
limiting currency may change in a fluctuating environ-
ment. According to their multidimensional model, when
egg maturation rates are slow in relation to food availabil-
ity, nesting females increase food investment per off-
spring, thus maximizing fitness returns per egg.
Conversely, when food resources are low and it takes lon-
ger for nesting females to provision a cell, provision size is
reduced and fitness returns are maximized per unit of pro-
vision. When analysed in light of this model (Rosenheim
et al. 1996), the production of tiny offspring by O. cornuta
appears to be analogous to the starvation of nestlings in
birds (Clutton-Brock 1991). A female O. cornuta laying
an egg on a tiny provision may be sacrificing that egg,
but gaining time to build a regular-sized provision before
overmaturation of the next oocyte. This is supported by
the fact that I only found three series of two consecutively
built cells with tiny provisions, and, in all three cases,
these were cells in different nests (that is, the last cell of
a nest and the first cell of a next-built nest contained
tiny provisions).
Although eggs are costly to produce, there is evidence
that egg production usually does not limit phenotypic
fecundity in Osmia. Osmia females produce w50 oocytes
(Maeta & Kurihara 1971; Maeta 1978), and in greenhouses
with nonlimiting floral resources may lay 30e40 eggs
(Tepedino & Torchio 1982b; Sugiura & Maeta 1989;
J. Bosch & W. P. Kemp, unpublished data). However, under
field conditions fecundity is usually 10e20 eggs per
female (Maeta 1978; Torchio 1985; Bosch 1994; Bosch &
Vicens 2005, 2006). In M. apicalis, females caged with
high levels of floral resources often delayed egg laying
on a completed provision and spent long periods simply
814 ANIMAL BEHAVIOUR, 75, 3
resting, a behaviour not observed in females caged with
scarce floral resources (Kim 1999). Resting periods were
also reported in O. lignaria provided with abundant floral
resources in a greenhouse (Tepedino & Torchio 1982b).
It could be argued against this hypothesis that O. cor-
nuta females of 1992, which were exposed to frequent
spells of bad weather, did not produce tiny progeny. How-
ever, egg maturation rates are highly temperature depen-
dent in Osmia. Thresholds for egg development in four
species of spring-flying Osmia ranged from 10 C to 14 C
(Maeta 1978; Bosch et al., in press), a range that coincides
with the 10e12 C threshold for foraging activity in O. cor-
nuta (Vicens & Bosch 2000). The effect of egg maturation
rates on provision size could be tested by exposing nesting
females to the same diurnal temperature conditions (to
provide similar foraging activity periods) but different
nocturnal temperatures, so that egg maturation would
proceed at different rates in different females.
It could also be argued against this hypothesis that
oocyte resorption has been reported in some Megachili-
dae, including Osmia spp. (Maeta & Kurihara 1971; Sihag
1986). Thus, a female with low provisioning rates could re-
absorb her mature oocyte, build up provision size, and
then lay the following egg in line. However, oocyte resorp-
tion in Osmia takes 8.5 days at 23 C and 15 days at 18 C,
and maturation of the second most mature oocyte is in-
hibited during oocyte resorption (Maeta & Kurihara
1971). Thus, oocyte resorption is too slow a process to
serve as a mechanism to synchronize egg maturation
and provisioning rates. Oocyte resorption in the above-
mentioned studies occurred in situations of total or severe
pollen deprivation. Measurement of unusually low pro-
tein levels in the haemolymph, indicated that oocyte re-
sorption was a mechanism to sequester protein in
protein-starved females (Sihag 1986). These females built
cells, but could not provision them (Maeta & Kurihara
1971; Sihag 1986). Nesting behaviour in solitary bees
and wasps is regarded as a sequence of events (cell build-
ing, cell provisioning, egg laying, cell capping; Evans &
West-Eberhard 1970; von Frisch 1974). Notwithstanding
a certain degree of plasticity (e.g. when a partially provi-
sioned cell breaks and is repaired), the completion of
one operation triggers off the start of the next (von Frisch
1974). Inability to provision a cell may have inhibited egg
laying in pollen-deprived females studied by Maeta &
Kurihara (1971) and Sihag (1986). Despite flower scarcity
in 1991, O. cornuta females of this study were able to
obtain enough floral resources to sustain themselves and
proceed with the complete series of nest building and
nest provisioning behavioural events.
Why Lay Female Eggs on Small Provisions?
Ultimately, it might be advantageous to produce small-
sized female offspring because fitness of male and female
offspring is frequency dependent (Fisher 1958; Charnov
1982). Female offspring surviving the winter of a low-
resource year would find decreased competition for floral
resources and nesting cavities. At the same time, fitness
of male offspring surviving the winter of a low-resource
year would decrease because of competition for scarce
females. However, the increase in female fitness relative
to male fitness would have to be dramatic to compensate
for the disadvantages associated with small female size.
Females of 1991 produced 26 female offspring that were
smaller than an average male (105.9 mg). Developmental
mortality of these females was 30.8%, compared with
11.0% for males in the same size range. Of the 217 females
released (three years combined), 21 were smaller than
105.9 mg. Of these, only two (9.5%) established at the
release site, compared with 93 (47.5%) of the 196 larger-
sized females released (Bosch & Vicens 2006). In contrast,
male mating success in O. rufa was found to be indepen-
dent of body size (Seidelmann 1999).
As mentioned, megachilid females are able to selec-
tively fertilize eggs and therefore control the sex of their
offspring. Contraction of the spermatheca occurs during
oviposition, when the apical end of egg is already visible
at the tip of the female’s abdomen (Gerber & Kloster-
meyer 1970). Thus, even when constrained to build small
provisions, O. cornuta females could decide to lay only
male eggs on them. However, the decision to fertilize
a given egg may be taken at the beginning of cell con-
struction, rather than at the time of oviposition. Two
lines of evidence support this hypothesis. First, in many
bee and wasp species egg laying takes place before provi-
sioning (Stephen et al. 1969; Evans & West-Eberhard
1970). Egg laying in Osmia occurs after provisioning,
however, when starting the construction of a new cell,
females sometimes build a threshold that signals the loca-
tion of the apical cell partition, which will be completed
right after oviposition (Fabre 1916; Torchio 1989). In
other words, cell length, which is greater in female
than in male cells, is established before oviposition. Fail-
ure to alter the femaleemale sequence in nests provi-
sioned by females exposed to sudden changes in food
availability would provide support for an early timing
of the decision to fertilize or not fertilize an egg. Second,
Osmia females lay fertilized eggs in the innermost cells
within a nest, and unfertilized eggs in the outermost
cells. Immatures reach adulthood towards the end of
the summer, and then undergo a winter diapause within
their cocoon (Bosch et al., in press). In spring, emerging
individuals use their mandibles to cut their way out of
the cocoon and through any nest structures found along
the nesting cavity. If they encounter an unemerged indi-
vidual, they chew through it causing its death (Torchio &
Tepedino 1982; Tepedino & Frohlich 1984). Because
males complete diapause and emerge out of the nest
ahead of females (Bosch & Kemp 2004; Kemp et al.
2004), altering the femaleemale sequence within a nest
would result in fratricide.
In the study of progeny size evolution, theoretical
models have largely outpaced empirical data (Fox &
Czesak 2000). The production of undersized progeny in
O. cornuta emphasizes the role of physiological and
ecological constraints in determining parental investment
strategies (Stearns 1992; Fox & Mousseau 1998), and
illustrates the need to account for features of organismal
biology to understand reproductive investment and
resource allocation (Bernardo 1996).

Acknowledgments
I am grateful to the staff at Mas Bové for their support
throughout the study. J. Calzadilla, M.A. Escolano, M.
López, N. Vicens and J. Losarcos generously shared many
hours of field observations and nest dissections. J. Retana
(CREAF e Universitat Autònoma de Barcelona) and V. J.
Tepedino (USDA-ARS, Logan, Utah) reviewed a draft of the
manuscript and made suggestions for its improvement.
The study was supported by a FPI (Formación de Personal
Investigador) scholarship from the Spanish MEC, a DGI-
CYT (Dirección General de Investigación, Ciencia y
Tecnologi) grant (AGR 91-0988-CO3) and an INIA
(Instituto Nacional de Investigaciones Agrarias) grant
(88-8191).
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