Hierarchical Microstructures and Functions of the Lepidopteran Proboscis Cuticle

Lehnert, Matthew S.; Wei, Qi‐Huo

doi:10.1007/978-3-030-29654-4_9

Cited by 7 publications

(7 citation statements)

References 65 publications

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“…Fluid-feeding insects (e.g. butterflies and moths, bees, and flies), for example, use numerous mouthpart adaptations for fluid uptake, such as cuticle wettability and structures that enable capillary action (Krenn et al, 2005;Lehnert & Wei, 2019;Wu et al, 2015). Butterflies and moths (Lepidoptera), the most diverse group of fluid-feeding insects (approximately 16% of all insect species; Adler & Foottit, 2009), use their modified mouthparts, the proboscis, to feed on a variety of nutritive fluids, including nectar, sap, wetted soil, and liquids on rotting fruit and carrion (Krenn, 2010;Monaenkova et al, 2012;Ômura et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Physical adaptations of butterfly proboscises enable feeding from narrow floral tubes

Lehnert

Johnson

Wu³

et al. 2021

Functional Ecology

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1. Butterflies use a proboscis, a microfluidic probe engineered by natural selection, to feed on nutritive fluids. The structural configuration of proboscises relates to feeding habits; however, the adaptations that enable proboscis entry into narrow floral corollas lack experimental evidence.2. Here, we investigated proboscis adaptations that enable entry into corollas using funnel-shaped glass capillary tubes and performed feeding trials with six butterfly species of different feeding habits. Proboscises were either guided (natural treatment) or forced (forced treatment) into the capillary tubes that were filled with a 20% sucrose solution. The treatments were video-recorded to determine the depth the proboscises reached into the tube and how long they remained there.The results were interpreted in terms of proboscis morphology, friction forces and the material properties of the cuticle.3. In the natural treatment, butterflies classified as flower visitors were more efficient at feeding from the tubes, reaching an average 1.83× deeper into the tubes than the other species and never getting their proboscises stuck. The non-flowervisiting species, in contrast, had their proboscises remain in the tube 17× longer than the flower-visiting species, with 90% of them getting their proboscises at least partially stuck. The butterfly species with generalist feeding habits fed more efficiently than the non-flower visitors, but less than the flower visitors. A similar pattern was observed in the forced treatment. 4. Flower-visiting butterflies had smoother and more tapered proboscises, lower friction forces and a semi-circular cross-section that would reduce bendability and was augmented by a more sclerotized cuticle. Proboscises of flower-visiting butterflies, therefore, have a suite of adaptations that operate synergistically to optimize their feeding habits.

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Section: Introductionmentioning

confidence: 99%

Physical adaptations of butterfly proboscises enable feeding from narrow floral tubes

Lehnert

Johnson

Wu³

et al. 2021

Functional Ecology

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“…Zone 1 with a closed interlocking structure is considered to be a hydrophobic non-drinking region, whereas Zones 2 and 3 are regarded as hydrophilic drinking regions [22]. The hydrophobic region bears overlapping dorsal legulae and small interlegular spaces with a large proportion of the circumference covered with hydrophobic microbumps [43]. The hydrophilic regions of S. trifolii and P. scutosa account for 5-20% of the total length of the proboscis [44,45], and bear slits at the tip which actively lead fluid into the food canal [46,47].…”

Section: Discussionmentioning

confidence: 99%

Ultramorphological Comparison of Proboscis and Associated Sensilla of Scotogramma trifolii and Protoschinia scutosa (Lepidoptera: Noctuidae)

Zhang

Niu

et al. 2021

Insects

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The proboscis is an important feeding organ for the glossatan moths, mainly adapted to the flower and non-flower visiting habits. The clover cutworm, Scotogramma trifolii Rottemberg, and the spotted clover moth, Protoschinia scutosa (Denis & Schiffermuller), are serious polyphagous pests, attacking numerous vegetables and crops, resulting in huge economic losses. However, the feeding behavior and mechanisms of the adult stage remain unsatisfactorily explored. In this study, the proboscis morphology of S. trifolii and P. scutosa are described in detail using scanning electron microscopy, with the aim of investigating the morphological differences and feeding behavior of these two species. The proboscises of S. trifolii and P. scutosa are similar in morphology and structure and are divided into three zones (Zone 1–3) based on the morphological changes of the dorsal legulae. Three sensillum types are located on the proboscises of both species, sensilla chaetica, sensilla basiconica, and sensilla styloconica. Significant differences were observed in the length of the proboscis and each zone between these two species, as well as in sensilla size and number. Based on the morphology of the proboscis and associated sensilla, S. trifolii and P. scutosa are potential flower visitors, which was also reinforced by the pollen observed at the proboscis tip. These results will strengthen our understanding of the structure of the proboscis related to the feeding behavior of Noctuidae.

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“…This might be due to the hydrophilic properties of the cuticle that play an important role in fluid ingestion through the tiny openings at the tip and the transport of liquid through the rather slim food canal in Lepidoptera (Lehnert et al, 2013;Lehnert & Wei, 2019). This phenomenon is probably especially important in sphingids with a rudimentary and split proboscis.…”

Section: Sensilla At the Proboscis Tipmentioning

confidence: 99%

“…They may display a great morphological diversity in some Lepidopteran taxa (Krenn et al, 2001;Ma et al, 2019;Petr & Stewart, 2004). In addition to their function as combined mechano-chemosensilla, they have been proposed to form brush-like nano-sponges in the drinking region of certain species which do not feed on floral nectar (Krenn et al, 2001;Lehnert et al, 2016;Lehnert & Wei, 2019;Molleman et al, 2005). Although mouthparts are indispensable for feeding, the morphology of the proboscis and the feeding apparatus as a whole has not yet been studied comparatively in Sphingidae.…”

Section: Introductionmentioning

confidence: 99%

“…Close to the apex, the dorsal legulae form slits into the food canal referred to as drinking slits. The cuticle of the drinking region has hydrophilic properties that promote the ingestion of fluid into the food canal (Lehnert et al, 2013 , 2017 ; reviewed in Lehnert & Wei, 2019 ). Each galea contains sensilla, a trachea, a nerve, and a basal galeal muscle as well as numerous intrinsic muscles inside the lumen (e.g., Eastham & Eassa, 1955 ; Eaton, 1971 ; Krenn, 1990 ; Krenn & Kristensen, 2004 ).…”

Section: Introductionmentioning

confidence: 99%

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Evolutionary functional morphology of the proboscis and feeding apparatus of hawk moths (Sphingidae: Lepidoptera)

Reinwald

Bauder

Karolyi

et al. 2022

Journal of Morphology

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The morphology of the proboscis and associated feeding organs was studied in several nectar-feeding hawk moths, as well as a specialized honey-feeder and two supposedly nonfeeding species. The proboscis lengths ranged from a few millimeters to more than 200 mm. Despite the variation in proboscis length and feeding strategy, the principle external and internal composition of the galeae, the stipes pump, and the suction pump were similar across all species. The morphology of the smooth and slender proboscis is highly conserved among all lineages of nectar-feeding Sphingidae. Remarkably, they share a typical arrangement of the sensilla at the tip.The number and length of sensilla styloconica are independent from proboscis length. A unique proboscis morphology was found in the honey-feeding species Acherontia atropos. Here, the distinctly pointed apex displays a large subterminal opening of the food canal, and thus characterizes a novel type of piercing proboscis in Lepidoptera. In the probably nonfeeding species, the rudimentary galeae are not interlocked and the apex lacks sensilla styloconica; galeal muscles, however, are present. All studied species demonstrate an identical anatomy of the stipes, and suction pump, regardless of proboscis length and diet. Even supposedly nonfeeding Sphingidae possess all organs of the feeding apparatus, suggesting that their proboscis rudiments might still be functional. The morphometric analyses indicate significant positive correlations between galea lumen volume and stipes muscle volume as well as the volume of the food canal and the muscular volume of the suction pump. Size correlations of these functionally connected organs reflect morphological fine-tuning in the evolution of proboscis length and function.

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Hierarchical Microstructures and Functions of the Lepidopteran Proboscis Cuticle

Cited by 7 publications

References 65 publications

Physical adaptations of butterfly proboscises enable feeding from narrow floral tubes

Physical adaptations of butterfly proboscises enable feeding from narrow floral tubes

Ultramorphological Comparison of Proboscis and Associated Sensilla of Scotogramma trifolii and Protoschinia scutosa (Lepidoptera: Noctuidae)

Evolutionary functional morphology of the proboscis and feeding apparatus of hawk moths (Sphingidae: Lepidoptera)

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