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.