Microrheology of haemolymph plasma of the bumblebee Bombus terrestris.

Viscosity, which impacts the rate of haemolymph circulation and heat transfer, is one of the transport properties that affects the performance of an insect. Measuring the viscosity of insect fluids is challenging because of the small amount available per specimen. Using particle tracking microrheology, which is well suited to characterise the rheology of the fluid part of the haemolymph, we studied the plasma viscosity in the bumblebee Bombus terrestris. In a sealed geometry, the viscosity exhibits an Arrhenius dependence with temperature, with an activation energy comparable to that previously estimated in hornworm larvae. In an open to air geometry, it increases by 4-5 orders of magnitude during evaporation. Evaporation times are temperature dependent and longer than typical insect haemolymph coagulation times. Unlike standard bulk rheology, microrheology can be applied to even smaller insects, paving the way to characterise biological fluids such as pheromones, pad secretions or cuticular layers.

Essential role of papillae flexibility in nectar capture by bees.

Many bees possess a tongue resembling a brush composed of a central rod (glossa) covered by elongated papillae, which is dipped periodically into nectar to collect this primary source of energy. In vivo measurements show that the amount of nectar collected per lap remains essentially constant for sugar concentrations lower than 50% but drops significantly for a concentration around 70%. To understand this variation of the ingestion rate with the sugar content of nectar, we investigate the dynamics of fluid capture by Bombus terrestris as a model system. During the dipping process, the papillae, which initially adhere to the glossa, unfold when immersed in the nectar. Combining in vivo investigations, macroscopic experiments with flexible rods, and an elastoviscous theoretical model, we show that the capture mechanism is governed by the relaxation dynamics of the bent papillae, driven by their elastic recoil slowed down through viscous dissipation. At low sugar concentrations, the papillae completely open before the tongue retracts out of nectar and thus, fully contribute to the fluid capture. In contrast, at larger concentrations corresponding to the drop of the ingestion rate, the viscous dissipation strongly hinders the papillae opening, reducing considerably the amount of nectar captured. This study shows the crucial role of flexible papillae, whose aspect ratio determines the optimal nectar concentration, to understand quantitatively the capture of nectar by bees and how physics can shed some light on the degree of adaptation of a specific morphological trait.

Collection of nectar by bumblebees: how the physics of fluid demonstrates the prominent role of the tongue's morphology.

Bumblebees and some other tiny animals feed on nectar by visiting flowers in their neighborhood. Some bee species appear to be highly specialized, their tongue being adapted to specific flowers. Bombus terrestris in contrast is able to feed on a wide variety of flowers and can thus be considered as a kind of universal nectar catcher. Since plant nectars show highly variable sugar content, Bombus terrestris have developed a capture mechanism that works for almost any fluid viscosity. Their tongues are decorated with very elongated papillae forming a hairy coating surrounding a rod-like main stalk. When settled on a flower, Bombus rapidly dip their tongue into the inflorescence to catch the highly sought-after nectar. To determine the physical mechanism at the origin of this outstanding ability, the capture dynamics was followed from videos recorded during viscous fluid ingestion. Surprisingly, the volume per lap and the lapping frequency are independent of the fluid viscosity over three orders of magnitude. To explain this observation, we designed a physical model of viscous dipping with structured rods. Predictions of the model compared to observations for bees showed that the nectar is not captured with the help of viscous drag, as proposed in the Landau-Levich-Derjaguin model, but thanks to the hairy structure that traps the viscous fluid, capillary forces drastically limiting the drainage. Our approach can be transposed to others nectar foragers such as bats and hummingbirds.