Surface and Wetting Properties of Embiopteran (Webspinner

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Surface and Wetting Properties of Embiopteran (Webspinner) Nanofiber Silk Thomas M. Osborn Popp,† J. Bennett Addison,† Jacob S. Jordan,† Viraj G. Damle,‡ Konrad Rykaczewski,‡ Shery L. Y. Chang,§ Grace Y. Stokes,∥ Janice S. Edgerly,⊥ and Jeffery L. Yarger*,† †

School of Molecular Sciences, Arizona State University, Tempe, Arizona 85287-1604, United States School for Engineering of Matter, Transport and Energy, Arizona State University, Tempe, Arizona 85287-1604, United States § LeRoy Eyring Center for Solid State Science, Arizona State University, Tempe, Arizona 85287-1604, United States ∥ Department of Chemistry and Biochemistry, Santa Clara University, Santa Clara, California 95053, United States ⊥ Department of Biology, Santa Clara University, Santa Clara, California 95053, United States ‡

S Supporting Information *

ABSTRACT: Insects of the order Embioptera, known as embiopterans, embiids, or webspinners, weave silk fibers together into sheets to make shelters called galleries. In this study, we show that silk galleries produced by the embiopteran Antipaluria urichi exhibit a highly hydrophobic wetting state with high water adhesion macroscopically equivalent to the rose petal effect. Specifically, the silk sheets have advancing contact angles above 150°, but receding contact angle approaching 0°. The silk sheets consist of layered fiber bundles with single strands spaced by microscale gaps. Scanning and transmission electron microscopy (SEM, TEM) images of silk treated with organic solvent and gas chromatography mass spectrometry (GC-MS) of the organic extract support the presence of a lipid outer layer on the silk fibers. We use cryogenic SEM to demonstrate that water drops reside on only the first layer of the silk fibers. The area fraction of this sparse outer silk layers is 0.1 to 0.3, which according to the Cassie−Baxter equation yields an effective static contact angle of ∼130° even for a mildly hydrophobic lipid coating. Using high magnification optical imaging of the three phase contact line of a water droplet receding from the silk sheet, we show that the high adhesion of the drop stems from water pinning along bundles of multiple silk fibers. The bundles likely form when the drop contact line is pinned on individual fibers and pulls them together as it recedes. The dynamic reorganization of the silk sheets during the droplet movement leads to formation of “super-pinning sites” that give embiopteran silk one of the strongest adhesions to water of any natural hydrophobic surface.

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INTRODUCTION

of silk attached to a piece of lichen held perpendicular to the surface of a table. Illustrating the waterproof nature of the silk, the water droplet “beads” up and takes on a nearly spherical shape. However, rather than rolling off, as is common to many natural superhydrophobic surfaces like the lotus leaf, the drop remains attached to the silk surface.5 Embiids exploit the highly adhesive yet hydrophobic property of their silk not only to keep dry during tropical rainstorms, but to drink from the water

Embiids, also commonly called webspinners or embiopterans, are tropical insects that use silk to build shelters of interconnected tunnels called galleries.1,2 Embiids spin very thin (50−150 nm in diameter3,4) protein-based silk fibers from their forelimbs, or tarsi, which are covered with hundreds of silk ejectors that enable the insect to spin hundreds of fibers at once into sheets. An adult female embiid of the species Antipaluria urichi is shown in Figure 1A. From observations in the field and in the laboratory, the interior of the silk galleries remains protected and dry even following extensive wetting of the exterior.5 The images in Figure 1B,C show a typical gallery situated vertically on a tree and a water droplet on the exterior © XXXX American Chemical Society

Received: February 26, 2016 Revised: April 7, 2016

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Figure 1. Optical images of Antipaluria urichi and their associated silk. (A) Adult female A. urichi on tree bark. (B) A. urichi silk gallery covering over 1 square meter seen on tree bark in Trinidad. (C) A silk gallery attached to lichen held perpendicular to the ground. Drops on the silk bead up, yet remain pinned to the sheet against gravity. removed manually with tweezers. A lipid extract was obtained by soaking 6 mg of cleaned A. urichi silk in 20 mL of 2:1 chloroform/ methanol for 24 h. The solvent from this extract was evaporated away with a stream of N2 gas, resulting in a lipid residue that was then dissolved in 250 μL analytical grade dichloromethane. Silyl derivatization was performed by mixing 50 μL of the extract with 50 μL 99% N,O-bis(trimethylsilyl) trifluoroacetamide (BSTFA) with 1% trimethylchlorosilane (TMCS) and heating in an oven at 65 °C for 3 h. The unmodified and silyl-derivatized extracts were analyzed with an Agilent 6890N/5973 inert GC-MS, operated in electron ionization mode using a HP-5MS column (30 mm × 0.250 mm x 0.25 μm) with splitless injection (10 psi) set at 300 °C. The helium carrier gas was set at a rate of 1.2 mL/min. The oven temperature was initially set to 65 °C for 10 min followed by an increase to 300 at 10 °C/min and held for 20 min. Mass spectra were compared to spectra from the NIST database. Scanning Electron Microscopy. Sheets of natural A. urichi silk and of 2:1 chloroform/methanol-treated silk were imaged with SEM. The sheets were secured to conductive carbon tape and gold-coated using a Denton vacuum sputter coater desk II for 3 min at a deposition rate of 5 nm/min. The images were obtained using an FEI XL30 Environmental SEM. The secondary electron detector was used for imaging. Images were collected under a vacuum pressure of less than 9 × 10−5 mbar and with an accelerating voltage of 10 kV. The area fraction of the silk fibers was quantified using ImageJ software from representative images of individual silk sheets that were converted to binary mode using thresholding. Energy-dispersive X-ray (EDS) spectra of the samples were collected for 600 s using an EDAX Apollo detector with Genesis software mounted onto an Amray 1910 SEM with an electron beam energy of 10 keV and condenser lens setting of −25 mm. Cryogenic SEM Procedure. The cryo-SEM experiments were conducted using FEI Nova 200 Focused Ion Beam and SEM equipped with Gatan Alto 2500 cryogenic cooling stage and vacuum transfer chamber. Several 0.2 μL drops of water were placed on top of the silk sheets mounted to a pretilted ∼10 mm diameter copper cylinder that was secured to the cryo-shuttle attached to the end of a transfer rod. The assembly was plunge frozen in liquid nitrogen slush, which was made by partially evacuating a chamber with liquid nitrogen. The sample was held in the liquid nitrogen slush for about 30 s until bubbling around the rod terminated. The freezing chamber was evacuated, and the sample was transferred to the SEM with mounted cryogenic staged cooled to −160 °C. SEM imaging was performed with energy of 5 keV and current of 98 pA with a working distance of 5.3 mm and absolute tilt between ∼45° and 85° with respect to the electron beam. Transmission Electron Microscopy. TEM images of natural and solvent-washed silk were taken using a Titan (FEI Company) electron microscope at 300 kV. The images taken were bright field TEM images. Care was taken that the dose rate remained low during image acquisition. Contact Angle Hysteresis. Twenty-one debris-free sections of silk were collected from the terrarium and were secured to glass slides

drops adhered to the exterior of the silk from the safety of their silk gallery interior.6 The rose petal displays wetting behavior that is macroscopically equivalent to that of embiopteran silk.7 Specifically, the surface of the rose petal has a static water contact angle greater than 150°, and yet surprisingly, drops of water adhere to it strongly even when turned upside down. This wetting property is known as the Cassie-impregnating wetting state, or the petal effect.8 The rose petal surface has a hierarchal roughness with two length scales: microscale bumps covered with nanoscale ridges. Water can penetrate in between the microscale features of the surface, but not into the nanoscale spaces between the ridges. As a result, the drop has high contact angle due to the composite interface with air pockets on the nanoscale, but pins to the surface due to wetting of the larger features.8 Similar to the rose petal, the surface of an embiopteran silk sheet has nanoscale features due to the thin diameter of the silk fibers, and the hydrophobicity of these fibers may arise from a lipid coating. Previous studies have shown the presence of lipids in a variety of arthropod silks.9−12 Our recent work has suggested the presence of a lipid layer on the silk of the embiopteran Antipaluria urichi via infrared absorption spectroscopy (IR) and solid-state nuclear magnetic resonance (NMR) spectroscopy, with IR peaks and 13C NMR resonances associated with alkanes decreasing in intensity after treating the natural silk with organic solvent.4 In this study, the hydrophobic properties of embiopteran silk are investigated for the first time. We show the existence of an external lipid coating on A. urichi silk fibers through scanning and transmission electron microscopy (SEM, TEM), and observe lipid species present in this layer through gas chromatography mass spectrometry (GC-MS). Using a variety of experimental methods, we demonstrate that the microscopic mechanisms responsible for the wetting behavior of the A. urichi silk sheets is markedly different from the rose petal effect. Specifically, the high adhesion of the drop stems from a dynamic reorganization of individual silk fibers into large bundles during recession that results in a receding contact angle approaching zero.

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EXPERIMENTAL SECTION

Insect Rearing. Antipaluria urichi were collected from Trinidad and Tobago, reared in a plastic terrarium with a mesh top and dried oak leaves as substrate, and fed fresh lettuce leaves every few days. Humidity was maintained by misting the sides of the container every few days. Gas Chromatography Mass Spectroscopy. Sections of silk were collected from the terrarium. Fecal matter and debris were B

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Langmuir with masking tape at the edges of the sheets. The silk sample was made to be sufficiently thick that the water would not contact the glass slide. A Rame-Hart 290-UI Contact Angle Goniometer was used to place and image drops of Millipore water on the silk surfaces for contact angle analysis. To measure the advancing contact angle for each sheet, volume was added to a starting droplet volume until the baseline of the drop increased in width. The starting droplet volumes used were 1 μL, 5 μL, 10 μL, 25 μL, 50 μL, and 75 μL. The volume increase was done in increments of 0.25 μL per step for the 1 and 5 μL starting volumes and in increments of 0.5 μL per step for all other starting volumes. Volume was removed from the droplet in 0.25 μL increments for 1 and 5 μL starting volumes and in 0.5 μL increments for all other starting volumes. The droplet contact angle was determined via the Young−Laplace fitting method. The uncertainty associated with the advancing contact angle measurement (n = 7 trials for starting droplet volume of 1 and 5 μL) was calculated using a two-tailed student t test with a 95% confidence interval. Solvent-treated samples were prepared by soaking the sheets in 2:1 chloroform/methanol for 30 min. Silk Surface Polytetrafluoroethylene (PTFE) Modification. An ∼1 cm2 sheet of the silk sheet placed on a glass slide was modified with an ∼20 to 30 nm layer of PTFE-like thin film using plasma deposition. Specifically, the sample was placed inside Blue Lantern 2 plasma deposition system from Integrated Surface Technologies (IST), Inc. The chamber was pumped down to 300 mTorr and purged with the precursor gas (Shieldex from IST, Inc.) several times prior to deposition. The plasma power was set to 150 W and maintained constant during the 30 min deposition time. Contact Line Movement Imaging. To observe the triple phase contact line movement for receding water drops on the untreated and PTFE modified silk sheets, the samples were placed on a glass slide under Zeiss Axio-Zoom V16 microscope with Apo 2.3x lens with bottom up illumination. Drops 7.5 to 15 μL in volume were dispensed and retracted from a tip of a horizontally placed micropipette that was in contact with the silk sheet and was placed at the edge of the field of view (80X zoom). The process was recorded using the microscope’s camera with a 20 Hz frequency.

Figure 2. SEM images of silk and A. urichi tarsi. (A) A natural silk sheet, with individual fibers between 90 and 100 nm in width. (B) Higher magnification showing silk fibers in bundles. (C) Surface of a tarsus, showing the variety of hair-like setae present, with a silk ejector highlighted in the white rectangle. Silk ejectors are spaced approximately 50−100 μm apart. (D) A silk ejector in the process of extruding a single silk fiber.

repeated tarsal sweeps built up an excess of silk. Figure 2C shows an SEM image of an adult female embiid tarsus, where the silk ejectors (larger, rough hairs) are visible amidst smaller setae.2 The extrusion of silk through a single silk ejector is shown in Figure 2D. The spacing between silk ejectors is on the order of 50−100 μm, indicating that a single pass with the tarsus results in a single layer of loosely spaced nanofibers on the microscale. After treating the silk sheets with 2:1 chloroform/methanol, a common solvent used for lipid extractions, SEM images reveal a change in the organization and morphology of the silk sheets, seen in Figure 3A,B. The solvent-treated silk fibers have an

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RESULTS AND DISCUSSION Surface coating of fibers and morphology of the silk sheets. The ability of embiopteran silk to keep water from entering the interior of the galleries suggests there may be some form of hydrophobic coating on the silk surface. Analysis of the organic extract of the silk by GC-MS revealed a mixture of many hydrocarbon species with overlapping elution times. Mass spectra of prominent peaks showed a variety of alkane species ranging from 10 to 30 carbons in length. Silyl ester derivatization of the extract enabled facile detection of fatty acids, as these peaks shifted from their initial elution times in the unmodified sample once derivatized. The major saturated fatty acid silyl esters identified were 16, 18, 20, and 22 carbons in length. Further analysis of lipid headgroups was not performed. Identification of lipids and long-chain fatty acids from other arthropod silks is not unprecedented; major dragline silk from the orbweaver spider Nephila clavipes has been shown to contain a variety of alkane lipid species, including fatty acids,9 and fatty acids have also been observed as a component of the lipid content in green lacewing cocoons.12 Images of silk obtained via SEM highlight the organization and spacing of the exceptionally fine fibers that comprise the silk galleries. Figure 2A,B shows SEM images of A. urichi silk taken from the surface of a colony from the lab terrarium. The individual silk fibers are approximately 90−100 nm in diameter, and appear to be laid down in layers. Embiids spin their galleries via repeated sweeps of their tarsi over a single area in order to build up a thick wall.13,14 Fibers from different layers appear to stack together and bundle in certain areas where

Figure 3. SEM (A,B) and TEM (C,D) images of natural silk (A,C) and of silk treated with 2:1 chloroform/methanol (B,D). SEM shows that the surface of the natural silk fibers has a smooth, uniform appearance, while the treated silk fiber surface has an uneven texture with small beads and clumps on the silk’s exterior, and fibers have aggregated together. The TEM image of a single silk fiber shows contrast between the fiber core and the exterior lipid layer. The lipid layer is approximately 10 nm or less in thickness, and is completely removed when treated with organic solvent as seen in D. C

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Figure 4. Optical and cryo-SEM images of water drops on the surface of A. urichi silk sheets. (A) A 1.5 μL drop exhibiting a static contact angle of 150.1°. (B) A 1.5 μL drop suspended upside down on natural silk. (C) Schematic drawing showing the orientation of the drop in the cryo-SEM. (D) A frozen drop on the surface of embiopteran silk (section in red at higher magnification), showing the drop sitting on only the first layer of silk fibers.

Consequently, the silk−water fsl can be roughly estimated from SEM images of the silk fibers (e.g., Figure 2A). For single and few silk sheets, the fsl range is 0.1 to 0.15 and 0.25 to 0.3, respectively. Even for the highest measured fsl of 0.3, the Cassie−Baxter equation predicts that the θ* of ∼130° to 135° that we observed in our experiments can be reached with θl ∼ 90°. Since a lower fsl and higher θl would significantly increase the θ*, we conclude that water drops residing on top of the silk are in contact with strands from a few overlapping outer sheets and that the lipid layer is only mildly hydrophobic. The microscale spacing between silk ejectors on the embiid tarsus is likely responsible for this low fsl value, which increases the hydrophobicity of the silk without requiring the embiid to produce a superhydrophobic lipid coating on the fibers. When this coating is removed using the 2:1 chloroform/methanol treatment, the individual fibers become hydrophilic, which makes the entire silk sheet completely permeable to water, as seen in Supporting Video V1. While water drops have been observed to easily roll off surfaces consisting of woven hydrophobic nanofibers,17 embiopteran silk exhibits remarkable drop “gripping” properties (see Figure 4B and Supporting Video V2). The adhesive properties of a composite surface can be characterized via study of the hysteresis between the maximum and minimum contact angle as the volume of a drop on the surface is varied.18,19 The advancing contact angle, θ a , is defined as the angle corresponding to the point where addition of water to the drop increases the baseline width without increasing the contact angle. The receding contact angle, θr, is defined as the angle where removal of water decreases the baseline width without decreasing the contact angle. The contact angle hysteresis, Δθ, is defined as the difference between the θa and the θr, and depends greatly on both the surface chemistry and the microscopic morphology of the rough surface.8,20 Low Δθ results in a drop with little resistance to rolling off the surface, while high CA hysteresis results in a drop with strong adhesion to the surface. To quantify the Δθ, we measured the dynamic water contact angles using the sessile drop method.21

uneven surface with clumps on their exterior, and aggregate into large bundles with less even spacing. TEM images show the internal structure of a single fiber, with a difference in contrast observed between the fiber core and an exterior layer seen in Figure 3C. Upon washing the fiber with 2:1 chloroform/methanol, the exterior layer is completely removed (Figure 3D), supporting the previously proposed hypothesis that embiopteran silk fibers are composed of a protein core with an external lipid coating.4 The lipid layer is around 10 nm or less in thickness along the length of each fiber. The beaded, rough surface of the solvent-treated silk fibers seen in Figure 3B may be the result of incomplete removal of this layer, and the clumping of fibers may be a result of the exposed proteinaceous fiber cores aggregating together in the presence of organic solvent. Wetting Properties of the Natural, Solvent-Treated, and PTFE-Modified Sheets. Embiopteran silk exhibits a wetting state that is macroscopically equivalent to the petal effect, as seen in Figure 4A,B, where a drop with a high static contact angle (131° ± 4°) adheres to the silk even when inverted. The static contact angle of a water drop residing on this composite surface stems from compounding effects of the morphology and chemistry of the base region of the drop. This so-called effective static contact angle, θ*, can be calculated using the Cassie−Baxter equation: cos(θ*) = fsl (cos(θ l) + 1) − 1

(1)

where fsl and θl are the solid−liquid area fraction of the composite interface and the inherent static contact angle of the lipid layer on top of individual silk fibers.15 To gain insight into the morphology of the composite interface, we used high-angle cryogenic SEM to image cryopreserved 0.2 μL drops resting on top of a silk sheet (see schematic in Figure 4C). Due to the high freezing rate for drops plunge-frozen in liquid nitrogen, the degree of distortion due to water crystallization should be minimal near the drop surface.16 The high tilt cryogenic SEM images in Figure 4D reveal that water resides on top of and does not penetrate below the outermost layers of the silk fibers. D

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Figure 5. Contact angle measurements for water on embiid silk. Discontinuities in the plots are due to droplet movement or deformation upon repositioning of the needle as volume is removed. (A) Drop volume starting at 1 μL. The advancing angle is reached at just above 150° coincident with an advancing baseline, but the drop size is too small to resolve the receding angle. (B) Drop volume starting at 75 μL. The advancing angle is observed to be around 150°, similar to the 1 μL measurement, and as volume is removed, the contact angle continuously decreases, never plateauing to a fixed value.

Figure 6. Optical microscopy of receding water drops on embiopteran silk. (A) Schematic representation of the method by which the drops were imaged. (B) Recession of a droplet on natural embiopteran silk, showing the formation of “super-pinning” sites circled in red as the surface fibers bundle together. (C) Recession of a droplet on PTFE-coated embiopteran silk. The number of pinning sites is reduced as the droplet recedes, resulting in a freely receding contact line.

The θa for 1 and 5 μL drops was 150 ± 2°. The θr was measured using larger droplet volumes in the method of Korhonen et al., as the θr can be difficult to determine for high-

hysteresis surfaces at low volumes.22 The θr for high-hysteresis surfaces tends to be a monotonically decreasing function of the droplet volume used for the measurement, eventually E

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Langmuir plateauing to a fixed value at high enough drop volumes.18 However, this was not the case for our measurements on embiopteran silk. A measurable θr was not reached at low volumes, nor at higher volumes. Across all trials, at no point did the contact angle plateau to a fixed value during the removal of volume from the drop, implying that the receding contact angle approaches 0° (see Figure 5 and Supporting Figures S2.1− S2.8). With a θr approaching 0°, the Δθ is approximately 150°.23 To understand the microscopic mechanism responsible for the vanishing macroscopic receding water contact angle, we imaged movement of the three phase contact line of a water droplet receding from the silk sheet using high magnification optical microscope. Specifically, as schematically shown in Figure 6A, we imaged the contact line of a drop resting on a silk sheet placed on a glass slide, while the volume of the drop was reduced via a horizontally placed syringe tip. The sequence of images in Figure 6B and Supporting Videos V3 and V4 show initiation of pinning sites due to movement of the contact line. It is also evident that as the volume of the drop is further reduced, more fibers are pulled toward the growing number of pinning sites. This bundling of multiple fibers leads to formation of several “super-pinning” sites that eventually completely anchor the contact line. The bundling of fibers likely occurs when the contact line is pinned at fiber bundles or chemical imperfections on fibers (e.g., nanoscale spaces between multiple fibers or hydrophilic hole defects in the lipid layer on the surface of fibers) and starts pulling them along as it recedes. As the fibers are not mechanically attached to each other, movement of the contact line easily rearranges the fibers, eventually leading to aggregation of multiple fibers and aggregation of individual pinning sites into a few “superpinning” sites. As formation of the pinning sites appears to be initiated with pinning of individual fibers or fiber bundles, conformal surface modification of the surface with a coating with lower surface energy than that of the lipid should reduce or eliminate the fiber bundling effect and reduce drop adhesion. To test this hypothesis, we plasma deposited a ∼ 20−30 nm thin PTFE-like amorphous film onto the silk fibers. We confirmed the presence of the thin PTFE-coating on the fibers using EDS (see Figure S3 in the Supporting Information). From the SEM images shown in Figure S2D, the coating appears smooth and did not appreciably thicken or mechanically stabilize the fibers. The latter effect was qualitatively observed during SEM imaging as the fibers easily moved around due to charging induced by insulating nature of the coating (which also made high quality imaging of these samples challenging). When applied to a smooth glass slide this low surface energy coating has θa of 116 ± 3°, θr of 81 ± 2°, and Δθ of 35 ± 4°. Modification of the silk fibers with this PTFE-like coating moderately increased the static contact angle to 149 ± 7°, while the value of the θa remained practically unchanged and equal to 151 ± 3°. Remarkably, the θr increased to 134 ± 5°, which reduced the Δθ from the unmodified value of ∼150° to 15 ± 6°. The sequence of images in Figure 6D and Supporting Video V5 show that, while some pinning occurs during retraction of the contact line on the PTFE-modified silk fibers, it is not accompanied by any significant rearrangement of the fibers. As a consequence of the reduction of the surface energy of the individual fibers, the fiber bundling effect was eliminated, and the contact line easily depinned and completely receded. These experiments provide further evidence that the remarkably high

adhesion of water droplets to embiopteran silk sheets stems from a rearrangement of the surface layers of silk into bundles of multiple fibers that form “super-pinning” sites.

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SUMMARY AND CONCLUSIONS Embiopteran silk shows wetting behavior that is macroscopically equivalent to the petal effect, yet achieves its adhesive properties via an entirely different mechanism of dynamic rearrangement of the surface upon droplet recession. The silk fibers are coated in a hydrophobic lipid layer, and are spun in into sheets in such a way as to reduce the surface area of contact between the fibers and the drop, yielding a highly hydrophobic surface. As these sheets are loosely woven, when the water contact line recedes along the surface it draws fibers together into “super-pinning” sites, which keep the water drop adhered to the silk surface. While several surfaces have already been synthesized mimicking the petal effect,23−25 embiopteran silk provides a paradigm to achieve a macroscopically similar effect with even greater contact angle hysteresis. The silk sheets resemble an electrospun material, making electrospinning a promising method for future development of a synthetic analogue to the silk. Several surfaces have been created via electrospinning that exhibit the petal effect, but in general they tend to be thick, coagulated mats that mimic the hierarchical roughness of the rose petal, and do not achieve their high hysteresis via the “super-pinning” mechanism found in embiopteran silk.26−28 Future development of high-hysteresis hydrophobic surfaces could focus on careful electrospinning of hydrophobic materials into sparse, loosely woven layered fiber sheets in order to achieve the dynamic bundling and “superpinning” effect that yields high water adhesion.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.langmuir.6b00762.

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Contact angle data (PDF) All videos referenced (ZIP)

AUTHOR INFORMATION

Corresponding Author

*E-mail to which correspondence should be addressed: [email protected]. Author Contributions

The manuscript was written through contributions of all authors. However, T.M.O.P. was the lead author and did the majority of the writing, corrections, and editing associated with this manuscript. All authors have given approval to the final version of the manuscript. Funding

The Department of Defense (DOD) Air Force Office of Scientific Research (AFOSR) under Award No. FA9550-14-10014 and the National Science Foundation (NSF), Division of Materials Research under award no. DMR-1264801 supported this work. NSF Grant DEB-0515865 awarded to J.S.E. at SCU supported collecting trips into the field and maintenance of cultures at SCU. Notes

The authors declare no competing financial interest. F

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(20) Wang, S.; Jiang, L. Definition of Superhydrophobic States. Adv. Mater. 2007, 19, 3423−3424. (21) Padday, J. Sessile Drop Profiles: Corrected Methods for Surface Tension and Spreading Coefficients. Proc. R. Soc. London, Ser. A 1972, 330, 561−572. (22) Korhonen, J.; Huhtamäki, T.; Ikkala, O.; Ras, R. Reliable Measurement of the Receding Contact Angle. Langmuir 2013, 29, 3858−63. (23) Bhushan, B.; Her, E. Fabrication of Superhydrophobic Surfaces with High and Low Adhesion Inspired from Rose Petal. Langmuir 2010, 26, 8207−8217. (24) Cheng, Z.; Du, M.; Lai, H.; Zhang, N.; Sun, K. From Petal Effect to Lotus Effect: A Facile Solution Immersion Process for the Fabrication of Super-Hydrophobic Surfaces with Controlled Adhesion. Nanoscale 2013, 5, 2776−83. (25) Karaman, M.; Ç abuk, N.; Ö zyurt, D.; Köysüren, Ö . SelfSupporting Superhydrophobic Thin Polymer Sheets That Mimic the Nature’s Petal Effect. Appl. Surf. Sci. 2012, 259, 542−546. (26) Gong, G.; Wu, J.; Liu, J.; Sun, N.; Zhao, Y.; Jiang, L. BioInspired Adhesive Superhydrophobic Polyimide Mat with High Thermal Stability. J. Mater. Chem. 2012, 22, 8257. (27) Ma, M.; Gupta, M.; Li, Z.; Zhai, L.; Gleason, K.; Cohen, R.; Rubner, M.; Rutledge, G. Decorated Electrospun Fibers Exhibiting Superhydrophobicity. Adv. Mater. 2007, 19, 255−259. (28) Pisuchpen, T.; Chaim-ngoen, N.; Intasanta, N.; Supaphol, P.; Hoven, V. Tuning Hydrophobicity and Water Adhesion by Electrospinning and Silanization. Langmuir 2011, 27, 3654−61.

ACKNOWLEDGMENTS We gratefully acknowledge the LeRoy Eyring Center for Solid State Science at Arizona State University for help with SEM imaging, and the Single Molecule Biophysics Center at the Biodesign Institute at Arizona State University for some use of contact angle instrumentation. We also thank Prof. Pierre Herckes of Arizona State University for both instrument usage and his time with GC-MS data collection and analysis.

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REFERENCES

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DOI: 10.1021/acs.langmuir.6b00762 Langmuir XXXX, XXX, XXX−XXX