Discussion
Group living fundamentally alters an organism’s microclimatic niche
[31–35]. The group niche can offer refuge from stressful
environmental conditions, particularly under climate change. Here, we
demonstrated that social conditions facilitate water conservation in
typically solitary bees. When exposed to low humidity, paired bees
retained more water than bees kept alone, with no differences in
activity level. These advantages of social living offer insights into
the ecological conditions that can give rise to incipient communal
societies.
Several mechanisms have been proposed to account for social water
conservation advantages. These benefits have been described across
arthropod taxa, including beetles [36–38], cockroaches [4], bed
bugs [2], woodlice [39,40], and larval Lepidoptera [3,41].
These animals aggregate in the tens to thousands of individuals, greatly
reducing their collective surface-area-to-volume ratio and thereby
reducing evaporative water loss. Interestingly, we found similar
benefits for groups of just two individuals. Paired bees in our study
generally stood adjacent to one another rather than forming a tight
huddle, indicating that their effective surface-area-to-volume ratios
were not substantially changed in the social treatment. Instead, it may
be that groups benefitted from altered microclimates, perhaps through
the creation of a humidified boundary layer via mutual transpiration
[2]. Simultaneously, paired bees may benefit from reduced
respiratory water loss if metabolic rate decreases with increasing group
size, as in other insects [38,42]. Metabolic studies of paired and
single solitary or communal bees have the potential to clarify the
mechanisms underlying this social advantage.
Bees in the social treatment experienced a modest but significant
reduction in water loss relative to singletons (~2% of
average body water content) in just three hours at 0% humidity. Over
longer time periods in natural contexts, accumulated differences in
water loss could account for differential mortality and/or fitness
outcomes for solitary vs. social individuals. Similarly, we found no
effect of body size on water loss in our study, though longer exposures
to low-humidity stress could reveal size effects on water balance, as in
other systems [1,43]. Importantly, our study design allowed for
non-destructive sampling with minimal observed harm to study subjects.
Bees were rehydrated and returned to their nest sites within five hours
of capture, and observed foraging on subsequent days. Many common insect
physiological stress assays are lethal or inflict severe sublethal
injuries, limiting their usefulness for large-scale studies of non-model
insect systems. Our study provides a template for future studies aimed
at expanding our understanding of physiological stress responses in rare
and declining bee species while minimizing impacts on source
populations.
Under climate change, increasing drought will restrict soil moisture in
many regions, with unknown consequences for the behavior and
distributions of ground-nesting bees, many of which exhibit preferences
for particular soil abiotic conditions [44,45]. Our study population
of M. tepidus timberlakei nests in water-saturated soil,
suggesting a possible preference for moisture-rich soils. Species-level
data on bees’ soil moisture preferences are scarce, and the nesting
preferences of M. tepidus are largely unknown. More data on soil
conditions at M. tepidus nesting aggregations could shed light on
the breadth of soil moisture conditions they tolerate. Under unfavorable
conditions, joining a nest with other females could increase humidity in
nesting tunnels and help mitigate challenges of maintaining water
homeostasis in dry soils.
Combined, our behavioral and physiological data suggest both a capacity
for group living as well as a physiological advantage of grouping in dry
conditions. Water loss increased significantly with active time, in line
with previous studies [1,46], yet paired bees were no more active
than singleton bees, suggesting that proximity to another bee did not
stimulate activity (e.g., avoidance). Furthermore, we did not observe
any instances of aggression in pairs. The lack of aggressive or avoidant
behaviors observed in our study mirrors observations of other communal
and solitary bees [47,48], and indicates a capacity for mutual
tolerance of unrelated conspecifics, an important pre-adaptation to the
formation of stable communal groups. Contexts like these that combine
behavioral plasticity with selective advantages for social individuals
may broadly resemble conditions at the evolutionary origins of group
living.