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Title: Mouthpart conduit sizes of fluid-feeding insects determine the ability to feed from pores

Abstract

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. In conclusion, given that natural selection independently favored mouthpart architectures that support these methods of fluid uptake (Diptera and Lepidoptera share a common ancestor 280 mya 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 porousmore » surfaces.« less

Authors:
ORCiD logo; ; ; ; ; ; ;
Publication Date:
Research Org.:
Brookhaven National Lab. (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); National Science Foundation (NSF)
OSTI Identifier:
1341685
Report Number(s):
BNL-113414-2017-JA
Journal ID: ISSN 0962-8452
Grant/Contract Number:  
SC00112704; IOS 1354956; DBI 1429113; AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the Royal Society B: Biological Sciences
Additional Journal Information:
Journal Volume: 284; Journal Issue: 1846; Journal ID: ISSN 0962-8452
Publisher:
The Royal Society Publishing
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Lepidoptera; Diptera; capillarity; liquid bridges; nanoparticles

Citation Formats

Lehnert, Matthew S., Bennett, Andrew, Reiter, Kristen E., Gerard, Patrick D., Wei, Qi-Huo, Byler, Miranda, Yan, Huan, and Lee, Wah-Keat. Mouthpart conduit sizes of fluid-feeding insects determine the ability to feed from pores. United States: N. p., 2017. Web. doi:10.1098/rspb.2016.2026.
Lehnert, Matthew S., Bennett, Andrew, Reiter, Kristen E., Gerard, Patrick D., Wei, Qi-Huo, Byler, Miranda, Yan, Huan, & Lee, Wah-Keat. Mouthpart conduit sizes of fluid-feeding insects determine the ability to feed from pores. United States. doi:10.1098/rspb.2016.2026.
Lehnert, Matthew S., Bennett, Andrew, Reiter, Kristen E., Gerard, Patrick D., Wei, Qi-Huo, Byler, Miranda, Yan, Huan, and Lee, Wah-Keat. Wed . "Mouthpart conduit sizes of fluid-feeding insects determine the ability to feed from pores". United States. doi:10.1098/rspb.2016.2026. https://www.osti.gov/servlets/purl/1341685.
@article{osti_1341685,
title = {Mouthpart conduit sizes of fluid-feeding insects determine the ability to feed from pores},
author = {Lehnert, Matthew S. and Bennett, Andrew and Reiter, Kristen E. and Gerard, Patrick D. and Wei, Qi-Huo and Byler, Miranda and Yan, Huan and Lee, Wah-Keat},
abstractNote = {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. In conclusion, given that natural selection independently favored mouthpart architectures that support these methods of fluid uptake (Diptera and Lepidoptera share a common ancestor 280 mya 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.},
doi = {10.1098/rspb.2016.2026},
journal = {Proceedings of the Royal Society B: Biological Sciences},
number = 1846,
volume = 284,
place = {United States},
year = {2017},
month = {1}
}

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Cited by: 2 works
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Works referenced in this record:

Mouthparts and nectar feeding of the flower visiting cricket Glomeremus orchidophilus (Gryllacrididae)
journal, May 2016

  • Krenn, Harald W.; Fournel, Jacques; Bauder, Julia A-S.
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Feeding Mechanisms of Adult Lepidoptera: Structure, Function, and Evolution of the Mouthparts
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Erection pattern and section-wise wettability of honeybee glossal hairs in nectar feeding
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Uptake of liquid from wet surfaces by the brush-tipped proboscis of a butterfly
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  • DOI: 10.1038/srep06934

Mouthpart Structure, Feeding Mechanisms, and Natural Food Sources of Adult Bactrocera (Diptera: Tephritidae)
journal, March 1997

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Paradox of the drinking-straw model of the butterfly proboscis
journal, June 2014

  • Tsai, C. -C.; Monaenkova, D.; Beard, C. E.
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Long-Proboscid Flies as Pollinators of Cretaceous Gymnosperms
journal, July 2015

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Experimental analysis of the liquid-feeding mechanism of the butterfly Pieris rapae
journal, March 2014

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Evidence of protease in the saliva of the butterfly Heliconius melpomene (L.) (Nymphalidae, Lepidoptera)
journal, February 2007


Hydrophobic–hydrophilic dichotomy of the butterfly proboscis
journal, August 2013

  • Lehnert, Matthew S.; Monaenkova, Daria; Andrukh, Taras
  • Journal of The Royal Society Interface, Vol. 10, Issue 85
  • DOI: 10.1098/rsif.2013.0336

A Spectrum of Nectar-Eater Communities
journal, November 1978


Sodium: Stimulus for Puddling Behavior by Tiger Swallowtail Butterflies, Papilio glaucus
journal, July 1974


A novel strategy for functionalizable photoluminescent magnetic nanoparticles
journal, November 2014


Structure of the lepidopteran proboscis in relation to feeding guild: STRUCTURE OF BUTTERFLY PROBOSCIS
journal, November 2015

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  • Journal of Morphology, Vol. 277, Issue 2
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Puddling: from natural history to understanding how it affects fitness
journal, February 2010


Time management and nectar flow: flower handling and suction feeding in long-proboscid flies (Nemestrinidae: Prosoeca)
journal, November 2013

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Natural drinking strategies
journal, April 2012


Effects of erectable glossal hairs on a honeybee's nectar-drinking strategy
journal, June 2014

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  • DOI: 10.1063/1.4886115

Erection mechanism of glossal hairs during honeybee feeding
journal, December 2015


The Phylogenetic Study of Adaptive Zones: Has Phytophagy Promoted Insect Diversification?
journal, July 1988

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Mouthparts of flower-visiting insects
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Mud-puddling behavior in tropical butterflies: in search of proteins or minerals?
journal, April 1999


Wing Measure as a Size Index in Lepidoptera: the Family Olethreutidae
journal, March 1977

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One proboscis, two tasks: Adaptations to blood-feeding and nectar-extracting in long-proboscid horse flies (Tabanidae, Philoliche)
journal, September 2014

  • Karolyi, Florian; Colville, Jonathan F.; Handschuh, Stephan
  • Arthropod Structure & Development, Vol. 43, Issue 5
  • DOI: 10.1016/j.asd.2014.07.003

On the mechanics and energetics of nectar feeding in butterflies
journal, January 1979


Oscillating selection on Darwin's finches
journal, June 1987

  • Gibbs, H. Lisle; Grant, Peter R.
  • Nature, Vol. 327, Issue 6122
  • DOI: 10.1038/327511a0

Butterfly proboscis: combining a drinking straw with a nanosponge facilitated diversification of feeding habits
journal, August 2011

  • Monaenkova, Daria; Lehnert, Matthew S.; Andrukh, Taras
  • Journal of The Royal Society Interface, Vol. 9, Issue 69
  • DOI: 10.1098/rsif.2011.0392

Phylogenomics resolves the timing and pattern of insect evolution
journal, November 2014


Blood-feeding and nectar-feeding in adult tabanidae (Diptera)
journal, July 1980


Phylogenetics and temporal diversification of the earliest true flies (Insecta: Diptera) based on multiple nuclear genes
journal, October 2008


Nectar resource use by Colias butterflies: Chemical and visual aspects
journal, January 1974

  • Watt, Ward B.; Hoch, Peter C.; Mills, Susan G.
  • Oecologia, Vol. 14, Issue 4
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Energetics and Pollination Ecology
journal, May 1972


Data from: Mouthpart conduit sizes of fluid-feeding insects determine the ability to feed from pores
dataset, December 2016


    Works referencing / citing this record:

    Data from: Mouthpart conduit sizes of fluid-feeding insects determine the ability to feed from pores
    dataset, December 2016


    Supplementary material from "Mouthpart conduit sizes of fluid-feeding insects determine the ability to feed from pores"
    dataset, January 2017


    Structure of the lepidopteran proboscis in relation to feeding guild: STRUCTURE OF BUTTERFLY PROBOSCIS
    journal, November 2015

    • Lehnert, Matthew S.; Beard, Charles E.; Gerard, Patrick D.
    • Journal of Morphology, Vol. 277, Issue 2
    • DOI: 10.1002/jmor.20487

    Time management and nectar flow: flower handling and suction feeding in long-proboscid flies (Nemestrinidae: Prosoeca)
    journal, November 2013

    • Karolyi, Florian; Morawetz, Linde; Colville, Jonathan F.
    • Naturwissenschaften, Vol. 100, Issue 11
    • DOI: 10.1007/s00114-013-1114-6

    Mud-puddling behavior in tropical butterflies: in search of proteins or minerals?
    journal, April 1999


    On the mechanics and energetics of nectar feeding in butterflies
    journal, January 1979


    Mouthparts of flower-visiting insects
    journal, January 2005

    • Krenn, Harald W.; Plant, John D.; Szucsich, Nikolaus U.
    • Arthropod Structure & Development, Vol. 34, Issue 1
    • DOI: 10.1016/j.asd.2004.10.002

    One proboscis, two tasks: Adaptations to blood-feeding and nectar-extracting in long-proboscid horse flies (Tabanidae, Philoliche)
    journal, September 2014

    • Karolyi, Florian; Colville, Jonathan F.; Handschuh, Stephan
    • Arthropod Structure & Development, Vol. 43, Issue 5
    • DOI: 10.1016/j.asd.2014.07.003

    Mouthparts and nectar feeding of the flower visiting cricket Glomeremus orchidophilus (Gryllacrididae)
    journal, May 2016

    • Krenn, Harald W.; Fournel, Jacques; Bauder, Julia A-S.
    • Arthropod Structure & Development, Vol. 45, Issue 3
    • DOI: 10.1016/j.asd.2016.03.002

    Long-Proboscid Flies as Pollinators of Cretaceous Gymnosperms
    journal, July 2015

    • Peñalver, Enrique; Arillo, Antonio; Pérez-de la Fuente, Ricardo
    • Current Biology, Vol. 25, Issue 14
    • DOI: 10.1016/j.cub.2015.05.062

    Evidence of protease in the saliva of the butterfly Heliconius melpomene (L.) (Nymphalidae, Lepidoptera)
    journal, February 2007


    Erection mechanism of glossal hairs during honeybee feeding
    journal, December 2015


    Natural drinking strategies
    journal, April 2012


    Oscillating selection on Darwin's finches
    journal, June 1987

    • Gibbs, H. Lisle; Grant, Peter R.
    • Nature, Vol. 327, Issue 6122
    • DOI: 10.1038/327511a0

    Uptake of liquid from wet surfaces by the brush-tipped proboscis of a butterfly
    journal, November 2014

    • Lee, Seung Chul; Lee, Sang Joon
    • Scientific Reports, Vol. 4, Issue 1
    • DOI: 10.1038/srep06934

    Effects of erectable glossal hairs on a honeybee's nectar-drinking strategy
    journal, June 2014

    • Yang, Heng; Wu, Jianing; Yan, Shaoze
    • Applied Physics Letters, Vol. 104, Issue 26
    • DOI: 10.1063/1.4886115

    The Phylogenetic Study of Adaptive Zones: Has Phytophagy Promoted Insect Diversification?
    journal, July 1988

    • Mitter, Charles; Farrell, Brian; Wiegmann, Brian
    • The American Naturalist, Vol. 132, Issue 1
    • DOI: 10.1086/284840

    A novel strategy for functionalizable photoluminescent magnetic nanoparticles
    journal, November 2014


    Wing Measure as a Size Index in Lepidoptera: the Family Olethreutidae
    journal, March 1977

    • Miller, William E.
    • Annals of the Entomological Society of America, Vol. 70, Issue 2
    • DOI: 10.1093/aesa/70.2.253

    Mouthpart Structure, Feeding Mechanisms, and Natural Food Sources of Adult Bactrocera (Diptera: Tephritidae)
    journal, March 1997

    • Vijaysegaran, S.; Walter, G. H.; Drew, R. A. I.
    • Annals of the Entomological Society of America, Vol. 90, Issue 2
    • DOI: 10.1093/aesa/90.2.184

    A Spectrum of Nectar-Eater Communities
    journal, November 1978


    Butterfly proboscis: combining a drinking straw with a nanosponge facilitated diversification of feeding habits
    journal, August 2011

    • Monaenkova, Daria; Lehnert, Matthew S.; Andrukh, Taras
    • Journal of The Royal Society Interface, Vol. 9, Issue 69
    • DOI: 10.1098/rsif.2011.0392

    Hydrophobic–hydrophilic dichotomy of the butterfly proboscis
    journal, August 2013

    • Lehnert, Matthew S.; Monaenkova, Daria; Andrukh, Taras
    • Journal of The Royal Society Interface, Vol. 10, Issue 85
    • DOI: 10.1098/rsif.2013.0336

    Phylogenetics and temporal diversification of the earliest true flies (Insecta: Diptera) based on multiple nuclear genes
    journal, October 2008


    Puddling: from natural history to understanding how it affects fitness
    journal, February 2010


    Phylogenomics resolves the timing and pattern of insect evolution
    journal, November 2014


    Energetics and Pollination Ecology
    journal, May 1972


    Sodium: Stimulus for Puddling Behavior by Tiger Swallowtail Butterflies, Papilio glaucus
    journal, July 1974


    Feeding Mechanisms of Adult Lepidoptera: Structure, Function, and Evolution of the Mouthparts
    journal, January 2010


    Paradox of the drinking-straw model of the butterfly proboscis
    journal, June 2014

    • Tsai, C. -C.; Monaenkova, D.; Beard, C. E.
    • Journal of Experimental Biology, Vol. 217, Issue 12
    • DOI: 10.1242/jeb.097998

    Experimental analysis of the liquid-feeding mechanism of the butterfly Pieris rapae
    journal, March 2014

    • Lee, S. C.; Kim, B. H.; Lee, S. J.
    • Journal of Experimental Biology, Vol. 217, Issue 11
    • DOI: 10.1242/jeb.100222

    Erection pattern and section-wise wettability of honeybee glossal hairs in nectar feeding
    journal, January 2015

    • Wu, J.; Zhu, R.; Yan, S.
    • Journal of Experimental Biology, Vol. 218, Issue 5
    • DOI: 10.1242/jeb.111013