Lepidopteran mouthpart architecture suggests a new mechanism of fluid uptake by insects with long proboscises

Salamatin, A. A.; Adler, Peter H.; Kornev, Konstantin G.

doi:10.1016/j.jtbi.2020.110525

Cited by 5 publications

(10 citation statements)

References 56 publications

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“…In hawkmoths, the hover-feeding mode further highlights these challenges because hovering is an energetically demanding flight mode [ 2 ], suggesting that the animals should maximize nectar uptake rate so as to minimize the duration of hovering [ 3 ]. As such, there has been much interest in how structural adaptations could speed nectar transport in the proboscis or otherwise reduce the needed feeding time, including a recent proposal that the lepidopteran (including hawkmoth) proboscis could fill through slits along the side, not just at the tip as in a drinking straw [ 10 ]. If this were the case, ingestion through upper submerged slits would help the moths reduce the amount friction that they need to overcome to ingest nectar due to the length of their proboscises [ 6 ], allowing more rapid nectar uptake.…”

Section: Discussionmentioning

confidence: 99%

“…To our knowledge, no extant published work addresses whether proboscis submergence depth influences nectar consumption rate. However, the depth to which M. sexta moths submerge their proboscis varies within and between recordings of feeding events, and recently published theoretical analysis of Lepidopteran mouthpart achitecture suggests that fluid uptake may occur along the length of the proboscis [ 10 ]. This suggests a possible increase in the feeding rate through a deeply submerged proboscis based on a model where transport of nectar through the proboscis has an energy cost proportional to travel distance, and that greater submergence would permit a shorter travel distance that decreased energy costs, increasing nectar ingestion rate.…”

Section: Introductionmentioning

confidence: 99%

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Feeding rate in adult Manduca sexta is unaffected by proboscis submersion depth

Pierce,

Hedrick

2024

PLoS ONE

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Adult moths from framily Spingidae (i.e. hawkmoths or sphinx moths) commonly feed on flower nectar through an extended proboscis, often several centimeters in length and longer than the body of the moth. Feeding on a viscous liquid (nectar) through a long and narrow tube is a challenging fluid dynamic problem and the subject of long-running scientific investigation. Here we characterized the relationship between proboscis submergence depth and nectar drinking rate in Manduca sexta hawkmoths. Video recordings of moth feeding bouts were collected and neural networks were used to extract data by object localization, tracking the location of the nectar meniscus and moths’ proboscis tips. We found that although feeding rates vary among bouts, the variation was not associated with proboscis submergence depth. These results show that despite the theoretical possibility of fluid uptake through the walls of the proboscis, such effects do not have a substantial effect on nectar uptake rate, and suggest that nectar must traverse the full length of the proboscis.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Feeding rate in adult Manduca sexta is unaffected by proboscis submersion depth

Pierce,

Hedrick

2024

PLoS ONE

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“…However, recent studies have revealed that Lepidoptera pull fluid from the porous surface into the food canal by capillary action via the interlegular spaces and the spaces between the hydrophilic sensilla styloconica and the pressure gradient created by the sucking sump [45,49]. Fluid uptake with the proboscis is mainly comprised of four steps: wetting, dewetting, absorbing, and pumping [50,51]. Many physical determinants represent the fundamental architecture of the proboscis affecting fluid uptake [52].…”

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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“…1E,F ). Adjacent legulae are separated from one another, creating a sieve-like legular band along the axis of the proboscis, which allows fluids to enter the food canal ( Kornev and Adler, 2019 ; Salamatin et al, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

“…The legulae are also hydrophilic throughout the entire length of the proboscis ( Lehnert et al, 2013 ; Zhang et al, 2018b ); thus, nectar or any other liquid would preferentially enter the food canal through the legular bands ( Fig. 1G ) ( Salamatin et al, 2021 ; Zhang et al, 2018a ). Although liquid also could enter the food canal through the permeable bands along the length of the butterfly proboscis, it hardly does so because liquids bead up on the hydrophobic surface.…”

Section: Introductionmentioning

confidence: 99%

Wettability and morphology of proboscises interweave with hawkmoth evolutionary history

Palaoro,

Gole,

Sun

et al. 2023

Journal of Experimental Biology

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Hovering hawkmoths expend significant energy while feeding, which should select for greater feeding efficiency. Although increased feeding efficiency has been implicitly assumed, it has never been assessed. We hypothesized that hawkmoths have proboscises specialized for gathering nectar passively. Using contact angle and capillary pressure to evaluate capillary action of the proboscis, we conducted a comparative analysis of wetting and absorption properties for 13 species of hawkmoths. We showed that all 13 species have a hydrophilic proboscis. In contradistinction, the proboscises of all other tested lepidopteran species have a wetting dichotomy with only the distal ∼10% hydrophilic. Longer proboscises are more wettable, suggesting that species of hawkmoths with long proboscises are more efficient at acquiring nectar by the proboscis surface than are species with shorter proboscises. All hawkmoth species also show strong capillary pressures which, together with the feeding behaviors we observed, ensure that nectar will be delivered to the food canal efficiently. The patterns we found suggest that different subfamilies of hawkmoths use different feeding strategies. Our comparative approach reveals that hawkmoths are unique among Lepidoptera and highlights the importance of considering the physical characteristics of the proboscis to understand the evolution and diversification of hawkmoths.

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Lepidopteran mouthpart architecture suggests a new mechanism of fluid uptake by insects with long proboscises

Cited by 5 publications

References 56 publications

Feeding rate in adult Manduca sexta is unaffected by proboscis submersion depth

Feeding rate in adult Manduca sexta is unaffected by proboscis submersion depth

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

Wettability and morphology of proboscises interweave with hawkmoth evolutionary history

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