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Research Article
Paradox of the drinking-straw model of the butterfly proboscis
Chen-Chih Tsai, Daria Monaenkova, Charles E. Beard, Peter H. Adler, Konstantin G. Kornev
Journal of Experimental Biology 2014 217: 2130-2138; doi: 10.1242/jeb.097998
Chen-Chih Tsai
1Department of Materials Science and Engineering, Clemson University, Clemson, SC 29634, USA
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Daria Monaenkova
1Department of Materials Science and Engineering, Clemson University, Clemson, SC 29634, USA
2School of Physics, Georgia Institute of Technology, Atlanta, GA 30332, USA
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Charles E. Beard
3School of Agricultural, Forest and Environmental Sciences, Clemson University, Clemson, SC 29634, USA
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Peter H. Adler
3School of Agricultural, Forest and Environmental Sciences, Clemson University, Clemson, SC 29634, USA
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Konstantin G. Kornev
1Department of Materials Science and Engineering, Clemson University, Clemson, SC 29634, USA
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  • For correspondence: kkornev@clemson.edu
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  • Fig. 1.
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    Fig. 1.

    Scanning electron micrographs of the monarch butterfly proboscis. (A) Single galea of the monarch proboscis, with the open food canal facing upward; the taper of the food canal is noticeable only in the drinking region. (B) Dorsal legulae with slit-like pores (interlegular spaces) enabling liquid to enter the food canal. (C) Proboscis tip showing a slit between opposing galeae; the spacing of the gap can change during feeding.

  • Fig. 2.
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    Fig. 2.

    Analysis of proboscis permeability. (A) Schematic diagram of the experiment showing operation of the Cahn DCA-322. A capillary tube with an inserted proboscis is connected to the balance arm by a hook. An oil droplet closes the rectangular vessel, preventing water evaporation and allowing the tube to move freely through the hole. Water moves from the reservoir to the tube by capillary action. The weight of the wicking water column is measured by the balance arm as the meniscus moves up the bore of the capillary tube. L, meniscus position; r, radius of the capillary tube; θ, contact angle; L(t), change in the length of the liquid column; Lp, length of the proboscis; R0, radius of opening; φ, taper angle; xy, the plane of proboscis placement; a–c, loops (see Materials and methods). (B) Closed vessel after 1 h of saturation with water vapor. The proboscis is suspended above the water. (C) The same vessel at the moment when the proboscis touches the water. (D) Example of measurement of Jurin height (Zc); arrow indicates the meniscus.

  • Fig. 3.
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    Fig. 3.

    Proboscis-in-a-tube model. Left: proboscis tip with one galea removed to expose the food canal of a monarch butterfly; scale bar, 1 mm. Right: schematic diagram of the food canal model. Lp is the proboscis length used in wicking experiments, H is the length of the drinking region, Rp is the radius of the straight section of the food canal, R0 is the radius of the opening and φ is the taper angle.

  • Fig. 4.
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    Fig. 4.

    The dimensionless meniscus position (L*) versus dimensionless time (t*) for a single proboscis of the monarch butterfly. Circles are experimental points and the solid line is the best fit with the proposed model.

  • Table 1.
  • Fig. 5.
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    Fig. 5.

    Pressure required to provide flow in tapered and non-tapered theoretical models of butterfly proboscises. PH is the pressure differential required in a tapered food canal at the drinking region (position H in Fig. 3); Pp is the pressure differential in the cibarial pump in a tapered food canal (position Lp in Fig. 3); Pt is the pressure differential in the cibarial pump in the drinking-straw (non-tapered) model when the radius (Rp) of the food canal does not change along the proboscis. Percentages indicate aqueous sucrose concentrations. The red horizontal dashed line at 1 atm indicates the maximum limit of pressure differential that could be produced by the cibarial pump. The dashed line below the x-axis indicates the measured flow rates for monarch butterflies.

  • Table 2.
  • Table 3.
  • Fig. 6.
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    Fig. 6.

    Image sequences extracted from a video recording of the proboscis tip of a monarch butterfly during feeding. The proboscis must be flexible to contract and expand quickly when the butterfly feeds. (A) Galeal sliding. (B) Galeal pulsing; the arrowheads are plotted to show the incremental change of the proboscis size. In the left image the arrowheads point to the proboscis boundary, while in the right image the proboscis boundary expands, making the arrowheads indented into the proboscis. The degree of expansion varies along the proboscis.

  • Fig. 7.
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    Fig. 7.

    Determination of droplet volume and sucrose concentrations fed from by monarch butterflies. (A) Monarch butterfly feeding from a droplet of sucrose as an example of an image used for estimation of droplet volume. (B) Dynamics of the change in droplet volume V with respect to initial volume V0 as a function of time for three sucrose concentrations; standard errors are from eight different experiments for each sucrose concentration.

  • Fig. 8.
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    Fig. 8.

    Typical experimental curve showing force changes at different steps of stage movement. A steep jump of the blue line allowed the zero depth of immersion (ZDOI) point to be defined. The proboscis was immersed farther into the water for 0.1 mm (green line). After 1 min (purple line), the change of water weight for 60 min was collected (red line). Arrow indicates the ZDOI threshold.

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Keywords

  • Butterfly feeding
  • Hagen–Poiseuille flow
  • Lepidoptera
  • Suction pressure
  • Wicking phenomena

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Research Article
Paradox of the drinking-straw model of the butterfly proboscis
Chen-Chih Tsai, Daria Monaenkova, Charles E. Beard, Peter H. Adler, Konstantin G. Kornev
Journal of Experimental Biology 2014 217: 2130-2138; doi: 10.1242/jeb.097998
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Research Article
Paradox of the drinking-straw model of the butterfly proboscis
Chen-Chih Tsai, Daria Monaenkova, Charles E. Beard, Peter H. Adler, Konstantin G. Kornev
Journal of Experimental Biology 2014 217: 2130-2138; doi: 10.1242/jeb.097998

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