Article pubs.acs.org/Langmuir
Microscale Mechanism of Age Dependent Wetting Properties of Prickly Pear Cacti (Opuntia) Konrad Rykaczewski,*,† Jacob S. Jordan,‡ Rubin Linder,† Erik T. Woods,† Xiaoda Sun,† Nicholas Kemme,† Kenneth C. Manning,† Brian R. Cherry,‡ Jeffery L. Yarger,‡ and Lucas C. Majure§,∥ †
School for Engineering of Matter, Transport and Energy, Arizona State University, Tempe, Arizona 85287, United States School of Molecular Sciences, Arizona State University, Tempe, Arizona 85287-1604, United States § Department of Research, Conservation and Collections, Desert Botanical Garden, Phoenix, Arizona 85008, United States ∥ School of Life Sciences, Arizona State University, Tempe, Arizona 85287-4701, United States ‡
S Supporting Information *
ABSTRACT: Cacti thrive in xeric environments through specialized water storage and collection tactics such as a shallow, widespread root system that maximizes rainwater absorption and spines adapted for fog droplet collection. However, in many cacti, the epidermis, not the spines, dominates the exterior surface area. Yet, little attention has been dedicated to studying interactions of the cactus epidermis with water drops. Surprisingly, the epidermis of plants in the genus Opuntia, also known as prickly pear cacti, has water-repelling characteristics. In this work, we report that surface properties of cladodes of 25 taxa of Opuntia grown in an arid Sonoran climate switch from water-repelling to superwetting under water impact over the span of a single season. We show that the old cladode surfaces are not superhydrophilic, but have nearly vanishing receding contact angle. We study water drop interactions with, as well as nano/microscale topology and chemistry of, the new and old cladodes of two Opuntia species and use this information to uncover the microscopic mechanism underlying this phenomenon. We demonstrate that composition of extracted wax and its contact angle do not change significantly with time. Instead, we show that the reported age dependent wetting behavior primarily stems from pinning of the receding contact line along multilayer surface microcracks in the epicuticular wax that expose the underlying highly hydrophilic layers.
1. INTRODUCTION One of the defining features of cacti is their ability to thrive in xeric environments through specialized water storage and collection tactics.1,2 Cacti store water within succulent tissue in their stems and minimize its loss in several ways, including a small volume to surface ratio and production of a waxy exterior coating that acts as a water permeation barrier. For collecting water, most cacti have developed a shallow, widespread root system that absorbs rainwater percolated through only upper parts of the soil.1,2 Some cacti such as Opuntia microdasys (Lehm.) Pfeiff., as well as all members of subfamily Opuntioideae, have complex multilevel, hairlike spines (i.e., glochids) that efficiently collect water droplets from fog.3 The dew or fog droplets collected by the spines could be absorbed by the areoles3−5 or shed to the ground to be absorbed by the roots.1 The fog collecting ability of O. microdasys along with similar observations6,7 has stimulated further research into fog collecting ability of various cacti8−12 and has provided inspiration for biomimetic fog collecting13−21 and oil−water separating22 technologies. However, in xeric climates such as the Sonoran desert, short seasonal rains, not fog, are the primary water source for the plants. In addition, in many cacti the epidermis, not the spines, dominates the exterior surface area. © 2016 American Chemical Society
Yet, by comparison to the fog collecting ability of spines, little attention has been dedicated to studying interactions of the cactus epidermis with water drops. The epidermis of plants in the genus Opuntia, also known as prickly pear cacti, has superhydrophobic characteristics23 stemming from the thin nano/microtextured epicuticular wax coating.24−26 In this work we report that the wetting properties of Opuntia cladodes (i.e., flattened, photosynthetic stems) change dramatically with age, which results in a “plant level” macroscopic step−like wetting gradient. Specifically, we observed that while fresh cladodes repel impacting drops, older cladodes on the same plant are completely wetted by them (see schematic and images in Figure 1). We show that this behavior is common to at least 25 Opuntia species native to numerous diverse climates. We studied water drop interactions with, as well as nano/microscale topology and chemistry of, the new and old cladodes of two Opuntia species and used this information to uncover the microscopic mechanism underlying the reported age dependent wettability change. Received: June 9, 2016 Revised: August 17, 2016 Published: August 18, 2016 9335
DOI: 10.1021/acs.langmuir.6b02173 Langmuir 2016, 32, 9335−9341
Article
Langmuir
solution was filtered through filter paper, and the solvent was completely evaporated off, leaving a waxy residue. Then, 5 mg of wax was dissolved in 650 μL of deuterated chloroform with 1%v/v tetramethylsilane as a chemical shift indicator. All experiments were performed on a Varian 500 MHz spectrometer equipped with a 5 mm triple-resonance probe operating in triple-resonance mode (1H/13C/15N). For 1H-NMR spectra, 64 scans were taken with a sweep width of 6009.6 Hz, a 5 s delay time, and a 5 s acquisition time.
3. RESULTS AND DISCUSSION To determine the universality of the wetting behavior illustrated for O. microdasys in Figure 1, we tested wetting properties of 25 taxa of Opuntia and one species of Tacinga that are native to numerous climates. After exposure to several sprays of water, all the studied live Opuntias growing within the Desert Botanical Garden’s collection displayed the same age-dependent wetting pattern. To obtain quantitative results, we collected various age cladodes of O. basilaris (see Figure 2a) and O. engelmannii var. lindheimeri (see Figure 2b). The representative sequence images in Figure 2c and d illustrate the dramatically contrasting water impact dynamics on cladodes of O. engelmannii grown during the current and previous growing season (see also Movie S1, identical behavior was observed for O. basilaris cladodes). It is evident that the new cladodes completely repel water drops, while a film of water remains after the impact of the drop on the old cladodes. Images of the cladodes of the two plants at different stages of growth are shown at various magnifications in the rest of Figure 2. We selected these two Opuntia species to explore for the possible effect of microscale topography of the plants. In particular, the ESEM images in Figure 2f and i shows that while the surface of O. basilaris is covered by large conical micropillars (i.e., unicellular trichomes), the surface of O. engelmannii is nearly planar on this length scale (i.e., glabrous). On the nanoscale, however, the surface of new cladodes of both of the plants is decorated by a complex three-dimensional epicuticular wax nanostructure. On the old cladodes that grew during the previous season, this nanostructure is partially eroded (see Figures 2g,j, S1, and S2). Furthermore, a predominant feature of old cladodes on both of the plants are the large cracks that break up the epicuticular wax into islands with size of tens of micrometers. The NMR spectra shown in Figure 3 for the epicuticular waxes collected from the new mature and old cladodes of the two cacti indicate that, matching previous reports,32 they are mostly composed of alkanes, with minor amounts of saturated ester fatty acids and ester fatty alcohols. In the NMR spectra, the peaks at 0.83 ppm are primarily the resonances of protons bound to terminal methyl groups, the peak at 1.25 ppm is the resonance of protons bound to intermediate carbons in alkane chains, and the peaks at 1.48 and 1.58 ppm are the resonance of protons bound to beta-carbons with respect to ester fatty alcohols or ester fatty acids, respectively. The small, sharp peaks at 1.31, 1.34, 1.44, and 1.68 ppm were determined to be impurities from cellular components dissolved during the chloroform wash. The only detectable intensity difference between new and old spectra for O. engelmannii plants was in the peak at 1.48 ppm, which is indicative of a decrease in ester fatty alcohol concentration (see spectra in Figure 3a and b). There were no observed changes in intensity in the spectra for O. basilaris, indicating that no detectable change in wax chemical composition occurred in this species over time (see spectra in Figure 3c and d). Concurring these observations, the static contact angle of water on the new and old extracted wax spread and flattened on a glass slide did
Figure 1. (a) Schematic and (b) image of age-dependent wetting of Opuntia (in this case O. microdasys) cladodes (pads): new cladodes are superhydrophobic and remain dry after exposure to a stream of water drops, while the older cladode grown during the previous year are fully wetted, as clearly visible through the remaining water film.
2. EXPERIMENTAL SECTION We investigated wetting properties of over 25 taxa within the genus Opuntia and one species of the genus Tacinga (both in tribe Opuntieae; see Majure et al.,27 Majure and Puente28) from the Desert Botanical Garden’s living plant collection. All the studied species as well as their distribution and type of habitat/climate are listed in Support Information. The macroscopic wetting properties of all the plants were qualitatively observed in the field, while samples of O. engelmannii var. lindheimeri (Engelmann’s prickly pear) and O. basilaris (beavertail prickly pear) were collected and analyzed in the lab. Specifically, we explored the two cacti’s wetting properties by measuring static, advancing, and receding contact angles (see Table S1), by using a high speed camera to image water drop impact, and by using an optical microscope to image triple phase contact line motion of a receding water drop. In addition, we used an environmental scanning electron microscope (ESEM) to image the nano/microscale surface topology of the cladodes and used nuclear magnetic resonance (NMR) to study the chemistry of the epicuticular wax. The wetting properties of the cacti in the field were observed by exposing them to several short bursts of water drops dispensed using a garden sprayer while the interaction was recorded using a digital camera. The age of the cladodes was evaluated in terms of current or previous growth season by observing their size and color as well as presence of leaves, which fall off after the cladode reaches maturity.1 The spray experiments were conducted twice, once in the fall of 2015 and once in late spring of 2016. In turn, the contact angles of the collected specimens were measured using a Ramé-Hart 290 goniometer with six locations studied per each cladode. The indicated uncertainty corresponds to a two-tailed T-student’s distribution with 95% confidence interval. Water drop impact onto the cactus cladode surface was imaged using Photron Fastcam Mini UX100 high-speed camera with a Sigma DC Macro OS 18−250 mm F3.5−6.3 lens at 4000 fps. The samples were mounted on a plexiglass stage that was tilted to about 30° in room environment at 22 °C and relative humidity of 10 to 15%. The impact of the drops was imaged from the side with back illumination provided by a Litepanels ENG light. Individual water drops were dispensed from a needle with 0.15 mm inner diameter using Harvard apparatus PhD Ultra CP syringe pump from high of about 10 cm. The topology of the samples was imaged using a Zeiss Axio-Zoom V16 microscope with Apo 1.5× lens with a ring light and an XL-30 FEI ESEM with electron beam energy of 15 keV, spot size 4, and water vapor pressure of about 600 Pa (4.5 to 5 Torr). To avoid dehydration during ESEM imaging, the samples were cooled during imaging to about 3 °C using a water-cooled Peltier cooling stage. An ESEM rather than regular SEM was utilized to minimize morphological artifacts imposed by sample fixation.29,30 The movement of the receding water contact line was imaged under the optical microscope using the same approach as in our previous work.31 To prepare the wax for NMR analysis, young and old cladodes were washed with 300 mL of 99.8% chloroform for 3 s. The chloroform 9336
DOI: 10.1021/acs.langmuir.6b02173 Langmuir 2016, 32, 9335−9341
Article
Langmuir not change. For example, we measured static contact angles of 82° ± 4° and 80° ± 3° for the flattened wax collected from the new and old cladodes of O. engelmannii, respectively. We note that in many plants the epicuticular wax can be mildly hydrophilic in nature,33,34 but can attain superhydrophobic characteristics through complex topology with re-entrant geometrical features (as those observed in our case, see Figures S1 and S2).34−37 In the case of the studied cacti, weathering primarily results in the topographical changes along with minor chemical alterations to the epicuticular wax. Put together, these changes significantly increase wettability of the surfaces with the static water contact angle changing from 158° ± 1° to 77° ± 4° and 158° ± 5° to 92° ± 2° from example new, mature, to old cladodes of O. engelmannii and O. basilaris, respectively. We note that the static contact angles measured on the older cladodes were consistent from cladode to cladode for the O. engelmannii, but varied significantly between ∼50° to ∼90° for the O. basilaris. This variation could stem from the difficulty in determining the exact age of the cladodes as well as from the presence of micropillar trichomes that could induce some air entrapment even on older samples. The consistent feature in all the older cladodes of both of the species was a nearly vanishing value of the receding contact angle. Consequently, the complete wetting of the older cladodes by impacting water drops is due to the
Figure 3. 1H NMR spectra of the extracted epicuticular wax for the indicated new and old cladodes of (a, b) O. engelmannii and (c, d) O. basilaris.
dramatic decrease of the receding contact angle (from above 135° to below 10°, see Table S1). Our results demonstrate a clear correlation between changes in the wetting properties and the evolution of the epicuticular
Figure 2. Appearance and wetting properties of various age cladodes of O. basilaris (a, e−g) and O. engelmannii (b−d, h−j): (a,b) images of the plants in the field, (c,d) high speed images contrasting water drop impact on old and new cladodes, (e, h) optical images of various age cladodes and static water drop on these surfaces, and (f, g, i, j) ESEM images of the cladode surfaces. 9337
DOI: 10.1021/acs.langmuir.6b02173 Langmuir 2016, 32, 9335−9341
Article
Langmuir
The topological changes due to weathering of the Opuntia wax that we have observed match those previously described in the literature,26,49 however, the impact of these changes on wetting properties and the underlying mechanism behind the observed wetting transition has not been reported. The epicuticular wax layer in the cuticle of cacti is separated from the cell wall by an intracuticular wax and pectine layers (see schematic in Figure 4a).24 A closer inspection of the microcracks shown in ESEM images in Figure 4b−d reveals hierarchical fractures that penetrate into these layers. Since the layers differ in their chemical composition,24 they are likely to have different wetting properties. To test this possibility, we measured static water contact angles of the old O. engelmannii cladodes with the wax layer removed using a crude mechanical and a chemical approach. The surface with its wax removed through light scrapping with a metal blade had a contact angle of 27° ± 7° (see inset in Figure 4b), while the surface with its wax removed through washing with chloroform a static contact angle of 38° ± 12°. The large variation in the measured contact angles, as well as visual inspection of the treated surfaces (see Figure S3), shows that neither of the treatments fully removed the wax. However, since the extracted wax was still nearly hydrophobic after evaporation of the solvent, our experiments demonstrate that exposure of the inner layers of the cuticle via microfracturing leads to formation of a surface with spatially heterogeneous wetting properties. Such composite surface characteristics can dramatically alter wetting properties.50−53 The apparent contact angle of such composite surface, θ*, can be estimated using the Cassie−Baxter equation:50
wax topology. In a majority of plants, synthesis of this material is high during development of leaves24,38,39 and its morphology develops into complex three-dimensional nanostructures through self-assembly and crystallization.40−42 The ESEM images in Figure S1 show that this is also true in case of both of the studied opuntias. Specifically, the complexity of the wax nanostructure increased significantly as the cladodes developed and matured. Implying formation of sufficiently complex nanostructure to create re-entrant features, the growth related topological changes correlated to transition from a hydrophobic to a superhydrophobic wetting state. For example, the surface of the O. engelmannii developing cladode had a static contact angle of 105° ± 8° that increased to 137° ± 7° and 158° ± 1° as the cladode developed and matured (i.e., lost majority of the leaves). Besides growth, the morphology and composition of the wax can also be altered through many environmental stresses including solar, wind, rain, and chemical exposure.43,44 Such stresses can naturally induce changes in surface wettability, but the degree of wax degradation during a growing season can vary dramatically for different plants.45 Neinhuis and Barthlott45 found that Ginkgo biloba L. (ginko) leaves were highly hydrophobic (contact angle of 130°−140°) and showed little wax erosion during the entire growth season (5 months), while leaves of Quercus robur L. (oak) had a contact angle decrease from 110° to 60° due to uniform erosion of the wax nanostructure within a few weeks after termination of the leaf’s expansion. In another example, Anfodollo et al.46 noted that temperature induced recrystallization of conifer needle wax from tubular to planar forms decreased the contact angle by 30°. Similarly, increase in wettability was documented for Nicotiana tabacum L. due to alteration of the wax composition following exposure to elevated ultraviolet light.47 In some cases the waxes can self-heal and regenerate, however, this ability is highly dependent on the species and age of the plants24,48 and does not appear to be present in the studied opuntias.
cos(θ*) = f1 cos(θ1) + f2 cos(θ2)
(1)
where f1 and f 2 are the solid−liquid area fractions and θ1 and θ2 are the inherent static contact angles of the hydrophilic and hydrophobic portions of the surface. From image analysis,
Figure 4. (a) Schematic of cactus cuticle structure, (b−d) ESEM images that microcracks in multiple levels of the O. engelmannii cuticle (the inset in b shows water contact angle on the old O. engelmannii cladode with mechanically removed wax); (e−g) imaging of receding contact line movement: (e) schematic of the experimental setup, and images of the contact line movement on (f) O. engelmannii and (g) O. basilaris. 9338
DOI: 10.1021/acs.langmuir.6b02173 Langmuir 2016, 32, 9335−9341
Article
Langmuir
prevent splashing of raindrops and redirection of the water flow toward roots at the base of the plant. Analogous macroscopic patterning of wettability has recently been used to manipulate liquid flow and separation.63 However, because the threedimensional arrangement of Opuntia cladodes is unique to individual plants, quantifying this effect in the field in a systematic way is challenging. As in synthetic membranes with nanocracks,64 the microcracks could also play a role in modulating the moisture barrier properties of the cactus cuticle.
the microcracks occupy about 30% of the O. engelmannii surface, leading to f1 = 0.3. Since this plant does not have pronounced microscale features once the wax nanostructure is partially eroded, we neglect effects of topography for purpose of obtaining a crude estimate of the effective contact angle. With θ1 assumed to be an average between the two measured values (∼33°) and θ2 assumed to be 82° for the flattened wax portion of the interface, eq 1 yields an effective contact angle of ∼70°. Providing another confirmation of the formation of a composite interfacethis crude theoretical estimate is reasonably close to the experimentally measured value of 77° ± 4°. Chemical and topological surface heterogeneities can also significantly affect movement of the triple phase contact line, which dictates the value of the advancing and receding contact angles.54−58 To illuminate the effect of these features of the aged Opuntia cladodes’ surfaces on wetting, we imaged the microscopic movement of the triple phase contact line of a receding water droplet (see schematic of the experimental setup in Figure 4e31). The sequences of images in Figure 4f and g show that the contact line does not appreciably move as the droplet volume is decreased until only a film remains (see also Movie S2). Furthermore, these images show that the contact line is strongly distorted and is pinned along a line connecting multiple microcracks. Consequently, the vanishing receding contact angle on the old cladodes is predominantly due to pinning along multilayer surface microcracks in the nearly hydrophobic epicuticular wax that expose the underlying hydrophilic layer.
■
ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.langmuir.6b02173. Table of measured contact angles, additional ESEM images of the epicuticular wax nanostructure, images of cladode surface after chemical and mechanical wax removal, and list and images of all the studied cacti species (PDF) Movie (4000 fps) of water drops impacting new and old cladode of O. engelmannii (AVI) Movie (50 fps) of water receding drop contact line movement on old cladode of O. engelmannii (AVI)
■
AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Notes
The authors declare no competing financial interest.
4. CONCLUSIONS In this work, we reported that surface properties of cladodes of 25 taxa of Opuntia (26 taxa of Opuntieae altogether) grown in an arid Sonoran climate switch from water-repelling to superwetting under water exposure over the span of a single growth season. In particular, the old cladode surfaces are not superhydrophilic, but have a nearly vanishing receding contact angle. We showed that this wetting behavior stems from pinning of the receding contact line along multilayer surface microcracks in the nearly hydrophobic epicuticular wax that expose the underlying highly hydrophilic layers. As epicuticular waxes can fracture under relatively minor strain,59 these microcracks likely form during cyclical expansion and compression of the cladodes associated with seasonal water intake and evaporation. The described mechanism differs from previously reported pinning induced through Cassie−Baxter to Wenzel state transition,60,61 and represents a Cassie−Baxter to Cassie−Baxter state transition with change of the nonwax phase from air to the strongly hydrophilic initially buried layers. We note that in some cases the environmental conditions during plant growth can have an effect on surface wettability, for example, Koch et al. reported that Brassica oleracea (Brassicaceae), Eucalyptus gunnii (Myrtaceae), and Tropaeolum majus (Tropaeolaceae) had a higher contact angle when grown in lower humidity conditions.62 It is untested whether all opuntias grown in more humid climates exhibit the same age dependent wetting properties, although anecdotal data suggest that this is the case. In xeric environments in which cacti thrive, regardless of humidity, this behavior could be universal and have an impact on water collection. In case of rain, the glochids and spines growing out of the aeroles may aid water collection by pinning and absorbing raindrops interacting with the cuticle. In addition, since stomata do not play a role in intake of liquid water, it is unlikely that the water film formed by the drop impact onto old fully wetting cladodes is directly absorbed over the cladode surface. Instead formation of the film might
■
ACKNOWLEDGMENTS The authors acknowledge funding from the Biomimicry Center and R.L. from Fulton Undergraduate Research Initiative, both at Arizona State University. J.L.Y. acknowledges funding from NSF Division of Materials Research under award no. DMR-1264801 for the NMR work. We also thank Desert Botanical Garden for providing access to their living collection. K.R. would also like to thank Prof. Maria Wieczynska for her forbearing encouragement of his botanical aspirations.
■
REFERENCES
(1) Anderson, E. F. The Cactus Family; Timber Press: Portland, OR, 2001. (2) Nobel, P. S. Remarkable Agaves and Cacti.; Oxford University Press: New York, 1994. (3) Ju, J.; Bai, H.; Zheng, Y.; Zhao, T.; Fang, R.; Jiang, L. A MultiStructural and Multi-Functional Integrated Fog Collection System in Cactus. Nat. Commun. 2012, 3, 1247. (4) Mauseth, J. D. Structure-Function Relationships in Highly Modified Shoots of Cactaceae. Ann. Bot. 2006, 98 (5), 901−926. (5) Mooney, H. A.; Weisser, P. J.; Gulmon, S. L. Environmental Adaptations of the Atacaman Desert Cactus Copiapoa Haseltoniana. Flora 1977, 166, 117−124. (6) Andrews, H. G.; Eccles, E. a.; Schofield, W. C. E.; Badyal, J. P. S. Three-Dimensional Hierarchical Structures for Fog Harvesting. Langmuir 2011, 27 (7), 3798−3802. (7) Ebner, M.; Miranda, T.; Roth-Nebelsick, A. Efficient Fog Harvesting by Stipagrostis Sabulicola (Namib Dune Bushman Grass). J. Arid Environ. 2011, 75 (6), 524−531. (8) Malik, F. T.; Clement, R. M.; Gethin, D. T.; Beysens, D.; Cohen, R. E.; Krawszik, W.; Parker, A. R. Dew Harvesting Efficiency of Four Species of Cacti. Bioinspir. Biomim. 2015, 10 (3), 036005. (9) Liu, C.; Xue, Y.; Chen, Y.; Zheng, Y. Effective Directional SelfGathering of Drops on Spine of Cactus with Splayed Capillary Arrays. Sci. Rep. 2015, 5, 17757. 9339
DOI: 10.1021/acs.langmuir.6b02173 Langmuir 2016, 32, 9335−9341
Article
Langmuir (10) Guo, L.; Tang, G. H. Experimental Study on Directional Motion of a Single Droplet on Cactus Spines. Int. J. Heat Mass Transfer 2015, 84, 198−202. (11) Xue, Y.; Wang, T.; Shi, W.; Sun, L.; Zheng, Y. Water Collection Abilities of Green Bristlegrass Bristle. RSC Adv. 2014, 4 (77), 40837− 40840. (12) Azad, M. A. K.; Barthlott, W.; Koch, K. Hierarchical Surface Architecture of Plants as an Inspiration for Biomimetic Fog Collectors. Langmuir 2015, 31 (48), 13172−13179. (13) Cao, M.; Ju, J.; Li, K.; Dou, S.; Liu, K.; Jiang, L. Facile and LargeScale Fabrication of a Cactus-Inspired Continuous Fog Collector. Adv. Funct. Mater. 2014, 24 (21), 3235−3240. (14) Ju, J.; Zheng, Y.; Jiang, L. Bioinspired One-Dimensional Materials for Directional Liquid Transport. Acc. Chem. Res. 2014, 47 (8), 2342− 2352. (15) Azad, M. A. K.; Ellerbrok, D.; Barthlott, W.; Koch, K. Fog Collecting Biomimetic Surfaces: Influence of Microstructure and Wettability. Bioinspir. Biomim. 2015, 10 (1), 016004. (16) Heng, X.; Luo, C. Bioinspired Plate-Based Fog Collectors. ACS Appl. Mater. Interfaces 2014, 6 (18), 16257−16266. (17) Ju, J.; Xiao, K.; Yao, X.; Bai, H.; Jiang, L. Bioinspired Conical Copper Wire with Gradient Wettability for Continuous and Efficient Fog Collection. Adv. Mater. 2013, 25 (41), 5937−5942. (18) Hou, Y.; Chen, Y.; Xue, Y.; Zheng, Y.; Jiang, L. Water Collection Behavior and Hanging Ability of Bioinspired Fiber. Langmuir 2012, 28 (10), 4737−4743. (19) Bai, F.; Wu, J.; Gong, G.; Guo, L. Biomimetic “Cactus Spine” with Hierarchical Groove Structure for Efficient Fog Collection. Adv. Sci. 2015, 2 (7), 1500047. (20) Seo, D.; Lee, J.; Lee, C.; Nam, Y. The Effects of Surface Wettability on the Fog and Dew Moisture Harvesting Performance on Tubular Surfaces. Sci. Rep. 2016, 6, 24276. (21) Shigezawa, N.; Ito, F.; Murakami, Y.; Yamanaka, S.; Morikawa, H. Development of Combination Textile of Thin and Thick Fiber for Fog Collection Bioinspired by Burkheya Purpurea. J. Text. Inst. 2015, 107, 1−8. (22) Li, K.; Ju, J.; Xue, Z.; Ma, J.; Feng, L.; Gao, S.; Jiang, L. Structured Cone Arrays for Continuous and Effective Collection of Micron-Sized Oil Droplets from Water. Nat. Commun. 2013, 4, 2276. (23) Barthlott, W.; Neinhuis, C. Purity of the Sacred Lotus, or Escape from Contamination in Biological Surfaces. Planta 1997, 202 (1), 1−8. (24) Koch, K.; Barthlott, W. Superhydrophobic and Superhydrophilic Plant Surfaces: An Inspiration for Biomimetic Materials. Philos. Trans. R. Soc., A 2009, 367 (1893), 1487−1509. (25) Koch, K.; Bohn, H. F.; Barthlott, W. Hierarchically Sculptured Plant Surfaces and Superhydrophobicity. Langmuir 2009, 25 (24), 14116−14120. (26) Ben Salem-Fnayou, A.; Zemni, H.; Nefzaoui, A.; Ghorbel, A. Micromorphology of Cactus-Pear (Opuntia Ficus-Indica (L.) Mill) Cladodes Based on Scanning Microscopies. Micron 2014, 56, 68−72. (27) Majure, L. C.; Puente, R.; Griffith, M. P.; Judd, W. S.; Soltis, P. S.; Soltis, D. E. Phylogeny of Opuntia Ss (Cactaceae): Clade Delineation, Geographic Origins, and Reticulate Evolution. Am. J. Bot. 2012, 99 (5), 847−864. (28) Majure, L.; Puente, R. Phylogenetic Relationships and Morphological Evolution in Opuntia S. Str. and Closely Related Members of Tribe Opuntieae. Succulent Plant Res. 2014, 8, 9−30. (29) Kim, K. W. Visualization of Micromorphology of Leaf Epicuticular Waxes of the Rubber Tree Ficus Elastica by Electron Microscopy. Micron 2008, 39 (7), 976−984. (30) Ensikat, H. J.; Ditsche-Kuru, P.; Barthlott, W. Scanning Electron Microscopy of Plant Surfaces: Simple but Sophisticated Methods for Preparation and Examination. Microsc. Sci. Technol. Appl. Educ. 2010, 248−255. (31) Osborn Popp, T. M.; Addison, J. B.; Jordan, J. S.; Damle, V. G.; Rykaczewski, K.; Chang, S. L. Y.; Stokes, G. Y.; Edgerly, J. S.; Yarger, J. L. Surface and Wetting Properties of Embiopteran (Webspinner) Nanofiber Silk. Langmuir 2016, 32 (18), 4681−4687.
(32) Wilkinson, R. E.; Mayeux, H. S. Composition of Epicuticular Wax on Opuntia-Engelmannii. Bot. Gaz. 1990, 151 (3), 342−347. (33) Cheng, Y. T.; Rodak, D. E. Is the Lotus Leaf Superhydrophobic? Appl. Phys. Lett. 2005, 86 (14), 144101. (34) Herminghaus, S. Roughness-Induced Non-Wetting. Europhys. Lett. 2000, 52 (2), 165−170. (35) Tuteja, A.; Choi, W.; Ma, M.; Mabry, J. M.; Mazzella, S. A.; Rutledge, G. C.; McKinley, G. H.; Cohen, R. E. Designing Superoleophobic Surfaces. Science 2007, 318 (5856), 1618−1622. (36) Liu, T.; Kim, C.-J. Turning a Surface Superrepellent Even to Completely Wetting Liquids. Science 2014, 346 (6213), 1096−1100. (37) Rykaczewski, K.; Paxson, A. T.; Staymates, M.; Walker, M. L.; Sun, X.; Anand, S.; Srinivasan, S.; McKinley, G. H.; Chinn, J.; Scott, J. H. J.; et al. Dropwise Condensation of Low Surface Tension Fluids on Omniphobic Surfaces. Sci. Rep. 2014, 4, 4158. (38) Jetter, R.; Schäffer, S. Chemical Composition of the Prunus Laurocerasus Leaf Surface. Dynamic Changes of the Epicuticular Wax Film during Leaf Development. Plant Physiol. 2001, 126 (4), 1725− 1737. (39) Post-Beittenmiller, D. Biochemistry and Molecular Biology of Wax Production in Plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1996, 47 (1), 405−430. (40) Meusel, I.; Neinhuis, C.; Markstädter, C.; Barthlott, W. Chemical Composition and Recrystallization of Epicuticular Waxes: Coiled Rodlets and Tubules. Plant Biol. 2000, 2 (4), 462−470. (41) Pechook, S.; Pokroy, B. Self-Assembling, Bioinspired Wax Crystalline Surfaces with Time-Dependent Wettability. Adv. Funct. Mater. 2012, 22 (4), 745−750. (42) Pechook, S.; Pokroy, B. Bioinspired Hierarchical Superhydrophobic Structures Formed by N-Paraffin Waxes of Varying Chain Lengths. Soft Matter 2013, 9 (24), 5710. (43) Shepherd, T.; Griffiths, D. W. The Effects of Stress on Plant Cuticular Waxes. New Phytol. 2006, 171, 469−499. (44) Jenks, M. A.; Gaston, C. H.; Goodwin, M. S.; Keith, J. A.; Teusink, R. S.; Wood, K. V. Seasonal Variation in Cuticular Waxes on Hosta Genotypes Differing in Leaf Surface Glaucousness. HortScience 2002, 37 (4), 673−677. (45) Neinhuis, C.; Barthlott, W. Seasonal Changes of Leaf Surface Contamination in Beech, Oak, and Ginkgo in Relation to Leaf Micromorphology and Wettability. New Phytol. 1998, 138 (1), 91−98. (46) Anfodillo, T.; Di Bisceglie, D. P.; Urso, T. Minimum Cuticular Conductance and Cuticle Features of Picea Abies and Pinus Cembra Needles along an Altitudinal Gradient in the Dolomites (NE Italian Alps). Tree Physiol. 2002, 22 (7), 479−487. (47) Barnes, J. D.; Percy, K. E.; Paul, N. D.; Jones, P.; McLaughlin, C. K.; Mullineaux, P. M.; Creissen, G.; Wellburn, A. R. The Influence of UV-B Radiation on the Physicochemical Nature of Tobacco (Nicotiana Tabacum L.) Leaf Surfaces. J. Exp. Bot. 1996, 47 (1), 99−109. (48) Gao, L.; Burnier, A.; Huang, Y. Quantifying Instantaneous Regeneration Rates of Plant Leaf Waxes Using Stable Hydrogen Isotope Labeling. Rapid Commun. Mass Spectrom. 2012, 26 (2), 115−122. (49) Chessa, I.; Nieddu, G.; De Pau, L.; Satta, D. Changes in the Morphology and Structure of Opuntia Ficus-Indica (Mill.) Cladodes Surface. In IV International Congress on Cactus Pear and Cochineal 581; International Society for Horticultural Science: Leuven, Belgium, 2002; Hammamet, Tunisia; pp 185−189. (50) Cassie, A. B. D.; Baxter, S. Wettability of Porous Surfaces. Trans. Faraday Soc. 1944, 40, 546−551. (51) Quéré, D. Wetting and Roughness. Annu. Rev. Mater. Res. 2008, 38 (1), 71−99. (52) Drelich, J.; Miller, J. D.; Kumar, A.; Whitesides, G. M. Wetting Characteristics of Liquid Drops at Heterogeneous Surfaces. Colloids Surf., A 1994, 93, 1−13. (53) Drelich, J.; Wilbur, J. L.; Miller, J. D.; Whitesides, G. M. Contact Angles for Liquid Drops at a Model Heterogeneous Surface Consisting of Alternating and Parallel Hydrophobic/hydrophilic Strips. Langmuir 1996, 12 (7), 1913−1922. 9340
DOI: 10.1021/acs.langmuir.6b02173 Langmuir 2016, 32, 9335−9341
Article
Langmuir (54) De Gennes, P.-G.; Brochard-Wyart, F.; Quéré, D. Capillarity and Wetting Phenomena: Drops, Bubbles, Pearls, Waves; Springer Science & Business Media: Berlin, 2013. (55) He, B.; Lee, J.; Patankar, N. A. Contact Angle Hysteresis on Rough Hydrophobic Surfaces. Colloids Surf., A 2004, 248 (1−3), 101− 104. (56) Paxson, A. T.; Varanasi, K. K. Self-Similarity of Contact Line Depinning from Textured Surfaces. Nat. Commun. 2013, 4, 1492. (57) Raj, R.; Enright, R.; Zhu, Y.; Adera, S.; Wang, E. N. Unified Model for Contact Angle Hysteresis on Heterogeneous and Superhydrophobic Surfaces. Langmuir 2012, 28, 15777−15788. (58) Damle, V. G.; Sun, X.; Rykaczewski, K. Can Metal MatrixHydrophobic Nanoparticle Composites Enhance Water Condensation by Promoting the Dropwise Mode? Adv. Mater. Interfaces 2015, 2, 1500202. (59) Borodich, F. M.; Gorb, E. V.; Gorb, S. N. Fracture Behaviour of Plant Epicuticular Wax Crystals and Its Role in Preventing Insect Attachment: A Theoretical Approach. Appl. Phys. A: Mater. Sci. Process. 2010, 100 (1), 63−71. (60) Mockenhaupt, B.; Ensikat, H.-J.; Spaeth, M.; Barthlott, W. Superhydrophobicity of Biological and Technical Surfaces under Moisture Condensation: Stability in Relation to Surface Structure. Langmuir 2008, 24 (23), 13591−13597. (61) Boreyko, J. B.; Chen, C. H. Restoring Superhydrophobicity of Lotus Leaves with Vibration-Induced Dewetting. Phys. Rev. Lett. 2009, 103, 1−4. (62) Koch, K.; Hartmann, K. D.; Schreiber, L.; Barthlott, W.; Neinhuis, C. Influences of Air Humidity during the Cultivation of Plants on Wax Chemical Composition, Morphology and Leaf Surface Wettability. Environ. Exp. Bot. 2006, 56 (1), 1−9. (63) Dong, Z.; Wu, L.; Li, N.; Ma, J.; Jiang, L. Manipulating Overflow Separation Directions by Wettability Boundary Positions. ACS Nano 2015, 9 (6), 6595−6602. (64) Park, C. H.; Lee, S. Y.; Hwang, D. S.; Shin, D. W.; Cho, D. H.; Lee, K. H.; Kim, T.-W.; Kim, T.-W.; Lee, M.; Kim, D.-S.; et al. NanocrackRegulated Self-Humidifying Membranes. Nature 2016, 532 (7600), 480−483.
9341
DOI: 10.1021/acs.langmuir.6b02173 Langmuir 2016, 32, 9335−9341
