Seasonality of pollinators in montane habitats: Cool-blooded bees for early-blooming plants

Understanding the factors that drive community-wide assembly of plant-pollinator systems along environmental gradients has considerable evolutionary, ecological, and applied significance. Variation in thermal environments combined with intrinsic differences among pollinators in thermal biology have been proposed as drivers of community-wide pollinator gradients, but this suggestion remains largely speculative. We test the hypothesis that seasonality in bee pollinator composition in Mediterranean montane habitats of southeastern Spain, which largely reflects the prevalence during the early flowering season of mining bees (Andrena), is a consequence of the latter's thermal biology. Quantitative information on seasonality of Andrena bees in the whole plant community (275 plant species) and their thermal microenvironment was combined with field and laboratory data on key aspects of the thermal biology of 30 species of Andrena (endothermic ability, warming constant, relationships of body temperature with ambient and operative temperatures). Andrena bees were a conspicuous, albeit strongly seasonal component of the pollinator assemblage of the regional plant community, visiting flowers of 153 different plant species (57% of total). The proportion of Andrena relative to all bees reached a maximum among plant species which flowered in late winter and early spring, and declined precipitously from May onward. Andrena were recorded only during the cooler segment of the annual range of air temperatures experienced at flowers by the whole bee assemblage. These patterns can be explained by features of Andrena's thermal biology: null to weak endothermy; ability to forage at much lower body temperature than strongly endothermic bees (difference ~ 10°C); low upper tolerable limit of body temperature, beyond which thermal stress presumably precluded foraging at the warmest period of year; weak thermoregulatory capacity; and high warming constant enhancing ectothermic warming. Our results demonstrate the importance of lineage-specific pollinator traits as drivers of seasonality in community-wide pollinator composition; show that exploitation of cooler microclimates by bees does not require strong endothermy; and suggest that intense endothermy and precise thermoregulation probably apply to a minority of bees. Medium- and large-sized bees with low upper thermal limits and weak thermoregulatory ability can actually be more adversely affected by climate warming than large, hot-blooded, extremely endothermic species.