Discussion
The timing of resource abundance relative to colony development
profoundly impacted colony growth and reproduction of B.
vosnesenskii . Colonies that received supplemental resources earlier in
development achieved greater peak weights and also produced more queens
– on average over 10 times more – than those colonies that received
supplemental food later. Greater peak weights of early-pulse colonies
were not driven by greater growth during a simulated resource pulse.
Instead, early-pulse colonies had higher growth rates during the period
that followed, in which they had access to ambient resources only. The
increase in growth rate is consistent with expectations based on
transient dynamics. Past studies have shown that higher food resources
increase bumble bee body size (Sutcliffe & Plowright 1988; Persson &
Smith 2011; Malfi et al. 2019), and that larger bumble bees bring
back more resources (Goulson et al. 2002; Spaethe & Weidenmüller
2002; Klein et al. 2017; Kerr et al. 2019) which would
lead to higher colony growth rates after the pulse ended. Our
early-pulse colonies had higher foraging rates compared to late-pulse
colonies during their off-pulse periods, even when controlling for
colony size, suggesting there was a more effective foraging workforce
during the post-pulse period in early-pulse colonies (Fig S4). It is
also possible that elevated resources may have led to additional
carry-over effects beyond the change in body size structure per
se . For example, Malfi et al. (2019) found that elevated resources
increase bumble bee worker longevity, as well as body size. Conversely,
captive workers deprived of pollen died earlier than those allowed to
feed ad libitum on pollen (Smeets & Duchateau 2003). Further
investigation of these mechanisms would be an interesting avenue for
future research.
In contrast to persistent pulse effects in early-pulse colonies, we did
not see a corresponding negative carryover effect of the off-pulse
period in the late-pulse colonies, in that their growth rates were not
different from those of early-pulse colonies during the pulse itself.
One hypothesis for similar responses to the pulse is that early-pulse
and late-pulse colonies had the same distribution of worker sizes at the
start of the pulse; in other words, all colonies had similar body-size
distributions when placed in the field regardless of treatment, and
late-pulse colonies might have retained this distribution during the
off-pulse period. Another possibility is that, because supplemental
resources were added by hand to colonies, size-based foraging ability
did not strongly affect resource gain during the period of
supplementation; in other words, worker size distribution did not
matter. Foraging levels were equally low during pulses for early-pulse
and late-pulse colonies (Fig S4). By supplementing colonies at the nest,
we also likely affected other aspects of colony dynamics, e.g.,
mortality associated with foraging (Rodd et al. 1980; Cresswell
2017; Malfi et al. 2018). A third hypothesis is that, during the
pulse, colonies were limited by factors other than resource return. For
certain Hymenoptera in particular, fecundity is sometimes limited by the
rate of egg maturation (Zhang et al. 2014; Yadav & Borges 2018),
rather than resource return, particularly under high resource scenarios
(Heimpel & Rosenheim 1998; Neff 2008).
Despite the strong carryover effect of resource pulses on off-pulse
growth rate, the timing of resource pulses did not significantly affect
the switch point (τ). Optimality models of bumble bee colonies (Macevicz
& Oster 1976; Beekman et al. 1998) predict the timing of
reproduction for bumble bee colonies should be earlier in high-resource
environments. In these models, the key effect of resource abundance is
on whether colonies are limited by queen egg production (presumably,
high resource environments), which leads to earlier switches to
reproduction, or limited by worker resource return (presumably, low
resource environments), which leads to later switches to reproduction.
Consistent with these models, Bowers (1986) observed that B.
flavifrons colonies in high-resource meadows switched to reproduction
sooner than those in low-resource meadows. It may be that bumble bee
colonies respond differently to fluctuations in resource limitation (our
experimental pulse treatments) than to chronically high or low resource
conditions. It may also be that B. vosnesenskii life histories
were resource limited (not egg limited) in both food resource
treatments, and so timing of the switch from growth to reproduction was
cued by end-of-season environmental conditions in both cases.
The availability of floral resources within landscapes varies throughout
the season with pulses and dearth occurring at different times (Reader
1984; Liz & Ruiz-Herrera 2016). In our study region, the Central Valley
of California, there is a steady decline of flowers from the onset of
the growing season to the dry season in natural areas, with
mass-flowering crops producing late season resource pulses in some
agriculturally dominated areas (Williams et al. 2012). In a
European agricultural system, late season forage from mass-flowering
clover increased queen abundance, but early season mass-flowering did
not elevate queen numbers (Rundlöf et al. 2014) or colony-level
queen production in similar landscapes (Westphal et al. 2009). It
is tempting to speculate that persistent effects of the early-season
pulse in our system reflected dynamics of ambient resources,
specifically elevated late season resources in some landscapes. Indeed,
new queen production was highest in four colonies that both received
early supplements and encountered a natural increase in late-season
ambient forage. However, analyses of growth rates across all colonies
suggest that ambient resources are not the primary driving factor behind
carry-over effects of the early-season pulse (Supporting
Information, Appendix 2 ).
More generally, our work emphasizes the need to understand the temporal
distribution of available flowering resources and its influence on
population dynamics of bees. Pollinator conservation efforts are often
based on planting floral resources to achieve greater abundance of
forage resources but must also recognize the importance of resource
continuity and timing (Schellhorn et al. 2015; Scheper et
al. 2015; Williams et al. 2015). Our study strongly indicates
the importance of resource timing for bumble bee colony and population
health and supports targeted efforts to boost resources during the early
season in areas where they are lacking, such as the agricultural lands
in our study system (Williams et al. 2012). At its simplest, our
study indicates that the timing of resources affects both the phenology
of colony growth and the ultimate reproductive output, so season-long
estimates of floral resources are not an adequate metric of habitat
quality.
In closing, our results emphasize the importance of the timing of
resources for colony growth, reproduction, and phenology. Carry-over
effects have been widely demonstrated in plant and animal populations,
but only rarely linked to population dynamics (Beckerman et al.2002). For the particular case of transient dynamics, effects of changes
in size structure have mostly been evaluated using models (McDonaldet al. 2016), not field experiments where populations are
confronted both with large perturbations and ordinary environmental
fluctuations. Numerous landscape studies of bees focus on the spatial
context of land use and resource availability, whereas extremely few
have investigated temporal dynamics within sites. Conservation planning
for bumble bee populations will need to emphasize not only overall
quality habitats but the temporal pattern of resources they contain. Our
results also demonstrate the general importance of temporal variation
for population dynamics, and the utility of bumble bee colony growth as
a model system for understanding population dynamics in temporally
varying environments.