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The extensive biodiversification of butterflies and moths (Lepidoptera) is partly attributed to their unique mouthparts (proboscis [Pr]) that can span in length from less than 1 mm to over 280 mm in Darwin's sphinx moths. Lepidoptera, similar to other insects, are believed to inhale and exhale respiratory gases only through valve-like spiracles on their thorax and abdomen, making gas exchange through the narrow tracheae (Tr) challenging for the elongated Pr. How Lepidoptera overcome distance effects for gas transport to the Pr is an open question that is important to understanding how the Pr elongated over evolutionary time. Here, we show with scanning electron microscopy and X-ray imaging that distance effects on gas exchange are overcome by previously unreported micropores on the Pr surface and by superhydrophobic Tr that prevent water loss and entry. We find that the density of micropores decreases monotonically along the Pr length with the maxima proportional to the Pr length and that micropore diameters produce a Knudsen number at the boundary between the slip and transition flow regimes. By numerical estimation, we further show that the respiratory gas exchange for the Pr predominantly occurs via diffusion through the micropores. These adaptations are key innovations vital to Pr elongation, which likely facilitated lepidopteran biodiversification and the radiation of angiosperms by coevolutionary processes., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2023 Elsevier Inc. All rights reserved.)

Adult cicadas pierce woody stems with their mouthparts to feed on xylem, suggesting the presence of cuticular adaptations that could increase hardness and elastic modulus. We tested the following hypotheses: (a) the mouthpart cuticle includes inorganic elements, which augment the mechanical properties; (b) these elements are abundant in specific mouthpart structures and regions responsible for piercing wood; (c) there are correlations among elements, which could provide insights into patterns of element colocalization. We used scanning electron microscopy (SEM) and energy dispersive X-ray spectroscopy (EDS) to investigate mouthpart morphology and quantify the elemental composition of the cuticle among four cicada species, including periodical cicadas ( Magicicada sp.). Nanoindentation was used to quantify hardness and elastic modulus of the mandibles. We found 12 inorganic elements, including colocalized manganese and zinc in the distal regions of the mandible, the structure most responsible for piercing through wood; nanoindentation determined that these regions were also significantly harder and had higher elastic modulus than other regions. Manganese and zinc abundance relates to increased hardness and stiffness as in the cuticle of other invertebrates; however, this is one of the first reports of cuticular metals among insects with piercing-sucking mouthparts (>100,000 described species). The present investigation provides insight into the feeding mechanism of cicadas, an important but understudied component of their life traits.

Antlion larvae are fluid-feeding ambush predators that feed on arthropods trapped in their funnel-shaped pits built in sandy habitats; however, details are lacking about their feeding mechanism. Here, we tested the hypothesis that the antlion, Myrmeleon crudelis, has adaptations that facilitate fluid feeding in sandy habitats. We measured contact angles of water droplets and used the capillary-rise technique to assess mouthpart wettability. A structural organization was discovered that provides a hydrophobic-hydrophilic wetting dichotomy that simultaneously supports self-cleaning and fluid uptake and is enabled by antiparallel movements of the maxillae. The mouthparts also are augmented by their mechanical properties, including maxillae and mandible tips that might be heavily sclerotized, as determined by confocal microscopy, which likely facilitates piercing prey. Our findings provide insight into how antlion larvae have overcome the challenges of fluid feeding in sandy habitats, which probably contributed to their success and widespread distribution., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2022. Published by The Company of Biologists Ltd.)

Prestomal teeth are cuticular projections on the mouthparts of some fly species that rasp surfaces when feeding. Although prestomal teeth morphology has been reported for several fly species, their material properties have not been investigated. Here we report the morphology, elemental composition, extent of sclerotization, hardness, and elastic modulus of prestomal teeth and relate these findings to feeding habits. Scanning electron microscopy revealed that species categorized as flower visitors have a large labellum with numerous pseudotracheae and lack prestomal teeth, generalist species have these same features but with prestomal teeth, and specialist species that feed on blood or other insects have a smaller labellum with few or no pseudotracheae and relatively large prestomal teeth. Confocal microscopy revealed that prestomal teeth are heavily sclerotized and the labellum contains resilin, an elastomeric protein. Hardness and elastic modulus were explored with nanoindentation and showed that the insectivorous Scathophaga stercoraria had the hardest prestomal teeth and the highest modulus. Energy dispersive x-ray spectroscopy revealed that prestomal teeth had low concentrations of inorganic elements, suggesting that hardness might be partially supplemented by inorganic elements. Our findings indicate that prestomal teeth morphology and material properties relate more to feeding habits than to phylogeny.

Few insect species are as popular as periodical cicadas (Magicicada spp.). Despite representing an enormous biomass and numbers that exceed 370/m 2 during mass emergences, the extended time period of the underground nymphal stages (up to 17 years) complicates investigations of their life history traits and ecology. Upon emergence, female cicadas mate and then use their ovipositors to cut through wood to lay their eggs. Given the ability to penetrate into wood, we hypothesized that the ovipositor cuticle is augmented with inorganic elements, which could increase hardness and reduce ovipositor fracturing. We used scanning electron microscopy and energy dispersive x-ray spectroscopy to evaluate the material properties of ovipositors of four cicada species, including three species of periodical cicadas. We found 14 inorganic elements of the cuticle, of which P, Ca, Si, Mg, Na, Fe, Zn, Mn, Cl, K, and S show the highest concentrations (%wt) near the apex of the ovipositor, where other structural modifications for penetrating wood are present. To the best of our knowledge, this is the first report of metal deposits in the cuticle of true bugs (Hemiptera, >80,000 described species).

The western honey bee, Apis mellifera L. (Hymenoptera), is arguably the most important pollinator worldwide. While feeding, A. mellifera uses a rapid back-and-forth motion with its brush-like mouthparts to probe pools and films of nectar. Because of the physical forces experienced by the mouthparts during the feeding process, we hypothesized that the mouthparts acquire wear or damage over time, which is paradoxical, because it is the older worker bees that are tasked with foraging for nectar and pollen. Here, we show that the average length of the setae (brush-like structures) on the glossa decreases with honey bee age, particularly when feeding on high-viscosity sucrose solutions. The nectar intake rate, however, remains nearly constant regardless of age or setae length (0.39±0.03 μg s -1 for honey bees fed a 45% sucrose solution and 0.48±0.05 μg s -1 for those fed a 35% sucrose solution). Observations of the feeding process with high-speed video recording revealed that the older honey bees with shorter setae dip nectar at a higher frequency. We propose a liquid transport model to calculate the nectar intake rate, energy intake rate and the power to overcome viscous drag. Theoretical analysis indicates that A. mellifera with shorter glossal setae can compensate both nectar and energy intake rates by increasing dipping frequency. The altered feeding behavior provides insight into how A. mellifera , and perhaps other insects with similar feeding mechanisms, can maintain a consistent fluid uptake rate, despite having damaged mouthparts., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2019. Published by The Company of Biologists Ltd.)

The Homerus swallowtail, Papilio ( Pterourus ) homerus Fabricius, is listed as an endangered species and is endemic to the Caribbean island of Jamaica. The largest butterfly in the Western Hemisphere, P. homerus once inhabited seven of Jamaica's 14 parishes and consisted of at least three populations; however, now only two stronghold populations remain, a western population in the rugged Cockpit Country and an eastern population in the Blue and John Crow Mountains. Despite numerous studies of its life history, much about the population biology, including estimates of total numbers of individuals in each population, remains unknown. In addition, a breeding program is needed to establish an experimental population, which could be used to augment wild populations and ensure the continued survival of the species. Here, we present a review of the biology of P. homerus and recommendations for a conservation plan., Competing Interests: The authors declare no conflict of interest.

Fluid-feeding insects, such as butterflies, moths and flies (20% of all animal species), are faced with the common selection pressure of having to remove and feed on trace amounts of fluids from porous surfaces. Insects able to acquire fluids that are confined to pores during drought conditions would have an adaptive advantage and increased fitness over other individuals. Here, we performed feeding trials using solutions with magnetic nanoparticles to show that butterflies and flies have mouthparts adapted to pull liquids from porous surfaces using capillary action as the governing principle. In addition, the ability to feed on the liquids collected from pores depends on a relationship between the diameter of the mouthpart conduits and substrate pore size diameter; insects with mouthpart conduit diameters larger than the pores cannot successfully feed, thus there is a limiting substrate pore size from which each species can acquire liquids for fluid uptake. Given that natural selection independently favoured mouthpart architectures that support these methods of fluid uptake (Diptera and Lepidoptera share a common ancestor 280 Ma that had chewing mouthparts), we suggest that the convergence of this mechanism advocates this as an optimal strategy for pulling trace amounts of fluids from porous surfaces., (© 2017 The Author(s).)

Mouthparts of fluid-feeding insects have unique material properties with no human-engineered analogue: the feeding devices acquire sticky and viscous liquids while remaining clean. We discovered that the external surface of the butterfly proboscis has a sharp boundary separating a hydrophilic drinking region and a hydrophobic non-drinking region. The structural arrangement of the proboscis provides the basis for the wetting dichotomy. Theoretical and experimental analyses show that fluid uptake is associated with enlargement of hydrophilic cuticular structures, the legulae, which link the two halves of the proboscis together. We also show that an elliptical proboscis produces a higher external meniscus than does a cylindrical proboscis of the same circumference. Fluid uptake is additionally facilitated in sap-feeding butterflies that have a proboscis with enlarged chemosensory structures forming a brush near the tip. This structural modification of the proboscis enables sap feeders to exploit films of liquid more efficiently. Structural changes along the proboscis, including increased legular width and presence of a brush-like tip, occur in a wide range of species, suggesting that a wetting dichotomy is widespread in the Lepidoptera.

The ability of Lepidoptera, or butterflies and moths, to drink liquids from rotting fruit and wet soil, as well as nectar from floral tubes, raises the question of whether the conventional view of the proboscis as a drinking straw can account for the withdrawal of fluids from porous substrates or of films and droplets from floral tubes. We discovered that the proboscis promotes capillary pull of liquids from diverse sources owing to a hierarchical pore structure spanning nano- and microscales. X-ray phase-contrast imaging reveals that Plateau instability causes liquid bridges to form in the food canal, which are transported to the gut by the muscular sucking pump in the head. The dual functionality of the proboscis represents a key innovation for exploiting a vast range of nutritional sources. We suggest that future studies of the adaptive radiation of the Lepidoptera take into account the role played by the structural organization of the proboscis. A transformative two-step model of capillary intake and suctioning can be applied not only to butterflies and moths but also potentially to vast numbers of other insects such as bees and flies.