Physical adaptations of butterfly proboscises enable feeding from narrow floral tubes

Abstract

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.

Mechanical properties, degree of sclerotisation and elemental composition of the gastric mill in the red swamp crayfish Procambarus clarkii (Decapoda, Crustacea)

“…(c) Blue signals were identified as regions containing high proportions of resilin, or related proteins. These studies were performed on wings 106 , foot attachment devices and legs 107 – 109 , mouthparts 38 , 110 , or genitals 111 , 112 . The proposed relationship between emitted autofluorescence signal, received by following the protocol 49 , and the mechanical properties was previously cross-validated by AFM-nanoindentation for the hair of foot attachment devices in a lady bird beetle 107 .…”

“…Knowledge about material properties complements morphology and gives rise to a profound understanding of function and also—when feeding structures are studied comparatively—of trophic specialisations. For invertebrate feeding structures, only very few studies comparing multiple taxa in the light of trophic specialisation implement both material properties and morphology [for fly teeth, see 37 ; for butterfly proboscises, see 38 and for radular teeth, see 39 – 43 .…”

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

“…to be an adaptation for optimized nectar uptake in nymphalid butterflies (Lehnert et al, 2021). A similar morphology has been described in Hesperiidae as well as long-proboscid Riodinidae (Bauder et al, 2013;Krenn & Bauder, 2017) and seems to be a feature displayed by all nectar-consuming Lepidoptera that are adapted to particularly long nectar spurs (Bauder & Karolyi, 2019).…”

Material Properties and Morphology of Prestomal Teeth in Relation to the Feeding Habits of Diptera (Brachycera)

“…Although there was a lack of inorganic elements in the cuticle of prestomal teeth, confocal microscopy and nanoindentation revealed that the teeth are hard. Confocal microscopy has been used on several arthropods to assess their material properties [3,27,[48][49][50]. Here, the labellum of all studied species had blue autofluorescence, an indicator of the elastomeric protein resilin.…”

“…Insect mouthparts provide notable examples of structure-function relationships [1][2][3], convergent evolution [4][5][6], and coevolution [7][8][9]. The mouthparts of adult flies (Diptera, +150,000 species) are no exception and exhibit adaptations for feeding on a wide variety of liquid foods, including nectar, blood, sweat, and fluids on carrion, dung, and rotting fruit [1,10,11].…”