Adult rhinoceros beetles use a sweeping pattern to ingest high-viscosity fluid.

More than half of all insect species utilize various natural liquids as primary diet. The concentrated liquids with energy-dense nutrition can provide highly favorable rewards, however, their high-viscosity poses challenges to the insect for ingesting. Here we show that rhinoceros beetles, Trypoxylus dichotomus (Coleoptera: Scarabaeidae), are capable of ingesting sugar solutions with viscosities spanning four orders of magnitude, exhibiting extraordinary adaptability to diverse natural liquid sources. We discovered a previously unidentified maxillae-sweeping motion that beetles preferentially adopt to consume highly viscous liquids, achieving a higher feeding rate than the more common direct sucking. By utilizing morphological characterizations, flow visualization, and fluid-structure coupling simulation, we revealed the underlying mechanisms of how this maxillary movement facilitates the transportation of viscous liquid. Our findings not only shed light on the multi-functionality of beetle mouthparts but also provide insights into the adaptability of generalized mouthparts to a broad range of fluid sources.

Honey bees switch mechanisms to drink deep nectar efficiently.

The feeding mechanisms of animals constrain the spectrum of resources that they can exploit profitably. For floral nectar eaters, both corolla depth and nectar properties have marked influence on foraging choices. We report the multiple strategies used by honey bees to efficiently extract nectar at the range of sugar concentrations and corolla depths they face in nature. Honey bees can collect nectar by dipping their hairy tongues or capillary loading when lapping it, or they can attach the tongue to the wall of long corollas and directly suck the nectar along the tongue sides. The honey bee feeding apparatus is unveiled as a multifunctional tool that can switch between lapping and sucking nectar according to the instantaneous ingesting efficiency, which is determined by the interplay of nectar-mouth distance and sugar concentration. These versatile feeding mechanisms allow honey bees to extract nectar efficiently from a wider range of floral resources than previously appreciated and endow them with remarkable adaptability to diverse foraging environments.

Trade-off mechanism of honey bee sucking and lapping.

Animals have developed various drinking strategies in capturing liquid to feed or to stay hydrated. In contrast with most animals, honey bees Apis mellifera that capture nectar with their tongue, can deliberately switch between sucking and lapping methods. They preferentially suck diluted nectar whereas they are prone to lap concentrated nectar. In vivo observations have shown that bees select the feeding method yielding the highest efficiency at a given sugar concentration. In this combined experimental and theoretical investigation, we propose two physical models for suction and lapping mode of capture that explain the transition between these two feeding strategy. The critical viscosity, µ*, at which the transition occurs, is derived from these models, and agrees well with in vivo measurements. The trade-off mechanism of honey bee sucking and lapping may further inspire microfluidics devices with higher capability of transporting liquids across a large range of viscosities.

Enhanced Flexibility of the Segmented Honey Bee Tongue with Hydrophobic Tongue Hairs.

Fibrous surfaces in nature have already exhibited excellent functions that are normally ascribed to the synergistic effects of special structures and material properties. The honey bee tongue, foraging liquid food in nature, has a unique segmented surface covered with dense hairs. Since honey bees are capable of using their tongue to adapt to possibly the broadest range of feeding environments to exploit every possible source of liquids, the surface properties of the tongue, especially the covering hairs, would likely represent an evolutionary optimization. In this paper, we show that their tongue hairs are stiff and hydrophobic, the latter of which is highly unexpected as the structure is designed for liquid capturing. We found that such hydrophobicity can prevent those stiff hairs from being adhered to the soft tongue surface, which could significantly enhance the deformability of the tongue when honey bees feed at various surfaces and promote their adaptability to different environments. These findings bridge the relationship between surface wettability and structural characteristics, which may shed new light on designing flexible microstructured fiber systems to transport viscous liquids.

Hydrophilic and opened canals in honey bee tongue rods endow elastic structures with multiple functions.

The honey bee (Apis mellifera L.) tongue is a sophisticated and dexterous probing device that can bend and twist, adapting to various surfaces for liquid imbibition and/or gustatory sensing. The tongue exhibits remarkable extendibility, flexibility, and durability, which may be essentially ascribed to the internal elastic rod that supports the entire tongue. However, neither the material composition nor the structural features of the rod, especially a peculiar inner canal that facilitates feeding, have been studied in relation to their function. Herein, by combining a set of imaging techniques, including optical microscopy, high-speed videography, scanning electron microscopy, micro-computed tomography (micro-CT), and confocal laser scanning microscopy, we characterize the spatial morphology, surface wettability and material composition of honey bee tongue rods. By performing mechanical testing, including atomic force microscopy, fracture testing, and finite element analysis, we provide the first evidence that the internal canal of the rod may represent a specialized structure for water retention due to the specific chemistry of resilin, which is an elastomeric protein that dominates the entire rod and renders it highly elastic, compliant and robust. Numerical simulations also suggest that the opening of the canal may facilitate larger deformations in twisting, extending the flexibility of the rod. STATEMENT OF SIGNIFICANCE: The honey bee is one of the most important pollinators around the world and is capable of foraging a wide spectrum of liquid sources by dipping into them with a miniature hairy tongue. However, there are no direct muscles distributed inside the tongue, instead, there is a conspicuous elastic rod with a hollow core. The rod extends for its full length and, according to our study, structurally reinforces the entire tongue to achieve functional versatility, and suggests a water containing function of the rod canal for maintaining the elasticity of the protein (resilin) that constitutes the rod. Our results broaden understandings of the relationship among morphology, materials science, and function of a honey bee tongue.

Sucking or lapping: facultative feeding mechanisms in honeybees (Apis mellifera).

Nectarivorous insects generally adopt suction or lapping to extract nectar from flowers and it is believed that each species exhibits one specific feeding pattern. In recent literature, large groups of nectarivores are classified as either 'suction feeders', imbibing nectar through their proboscis, or 'lappers', using viscous dipping. Honeybees (Apis mellifera) are the well-known lappers by virtue of their hairy tongues. Surprisingly, we found that honeybees also employ active suction when feeding on nectar with low viscosity, defying their classification as lappers. Further experiments showed that suction yielded higher uptake rates when ingesting low-concentration nectar, while lapping resulted in faster uptake when ingesting nectar with higher sugar content. We found that the optimal concentration of suction mode in honeybees coincided with the one calculated for other typical suction feeders. Moreover, we found behavioural flexibility in the drinking mode: a bee is able to switch between lapping and suction when offered different nectar concentrations. Such volitional switching in bees can enhance their feeding capabilities, allowing them to efficiently exploit the variety of concentrations presented in floral nectars, enhancing their adaptability to a wide range of energy sources.