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How Plants Keep Dry: A Physicist’s Point of View Alexander Otten* and Stephan Herminghaus Department of Applied Physics, University of Ulm, Albert Einstein Allee 11, D-89069 Ulm, Germany Received June 2, 2003. In Final Form: January 4, 2004 This work describes the investigation of the physical basis of the amazing water repellence of some plant leaves, which is in addition to self-cleaning properties known as the “Lotus effect”. Two rather different possible mechanisms are proposed, which are suggested to cover the main physics in a majority of superhydrophobic systems. These concepts are illustrated with two different types of plant leaves as well as a model surface carrying carbon nanotube aggregates.
1. Introduction The amazing water repellence of many biological surfaces, in particular plant leaves, has recently received great interest.1-4 The ability of these surfaces to make water bead off completely and thereby wash off contamination very effectively has been termed the “Lotus effect”, although it is observed not only on the leaves of the Lotus (Nelumbo nucifera L.) but also on many other species, such as Tropaeolum majus L. (Indian Cress/Nasturtium) or Alchemilla vulgaris L. (Lady’s Mantle). Although this effect is very common among plants and is of great technological importance, as for example for the effective use of insecticides, its basic mechanisms are not yet well understood. Since it is well-known that plant surfaces are usually rough on the micrometer scale and covered with cuticular wax, many attempts have been made to manufacture industrially similar surfaces by introducing both hydrophobicity and roughness.5-7 However, success was very limited in comparison to the unrivalled perfection nature has achieved as a result of evolutionary optimization processes. Given the enormous chemical and topographical complexity of biological surfaces, it is of great interest to identify the fundamental principles underlying the remarkable wetting properties of these surfaces. A closer look at water-repellent plant leaves reveals at least two distinctly different types. The first type of leaves, such as Lotus and Indian Cress, look macroscopically smooth. The mat appearance suggests the presence of some structure at small scales, which has to be considered to understand the wetting behavior.8 The second type is haircovered leaves such as the Lady’s Mantle. Both types let water droplets run off easily. After rain or morning dew, they both show a dry surface, with sometimes a single collected water droplet. However, they differ so substantially in surface structure that one might suspect different mechanisms to be responsible for this superhydrophobic behavior. In the present paper, we will show that this is indeed the case and discuss simple models which are able to account for our experimental observations. * Corresponding author. (1) Barthlott, W.; Neinhuis, C. Planta 1997, 202, 1-8. (2) Wagner, P.; Fu¨rstner, R.; Barthlott, W.; Neinhuis, C. J. Exp. Bot. 2003, 54, 1295-1303. (3) Wagner, P.; Neinhuis, C.; Barthlott, W. Acta Zool. 1996, 77 (3), 213-255. (4) Blossey, R. Nat. Mater. 2003, 2 (5), 301-306. (5) Onda, T.; Shibuichi, S.; Satoh, N.; Tsujii, K. Langmuir 1996, 12, 129. (6) Miwa, M.; Nakajima, A.; Fujishima, A.; Hashimoto, K.; Watanabe, T. Langmuir 2000, 16, 5754-5760. (7) Nakajima, A.; Hashimoto, K.; Watanabe, T. Langmuir 2000, 16, 7044-7047. (8) Wenzel, R. N. J. Phys. Colloid Chem. 1949, 53, 1466.
Figure 1. Water droplets on Indian Cress (a) and Lady’s Mantle (b).
2. Experiments For investigating the water-repelling behavior of the different leaf surfaces, optical microscopy, scanning electron microscopy, and contact angle measurements were used. The optical microscopy pictures were taken with a CCD camera mounted on a Zeiss Stemi 200-C optical microscope. For electron microscopy, a Zeiss DSM 962 scanning electron microscope (SEM) with acceleration voltages up to 15 keV was used. The SEM leaf samples were either air-dried (sample type I) or fixated in glutaric aldehyde (sample type II). The type II samples were afterward washed with CO2 and dried above the critical point to avoid the collapse of cellular structures. For SEM contrast enhancement, the samples were coated with a 20 nm layer of Au-Pd. Contact angle measurements were performed using a Dataphysics OCA 15 video-based optical goniometer with the sessile drop method. For microscopically small droplets, the contact angle was obtained by measuring the droplet diameter and the distance between the focal planes of the surface and the center-plane of the droplet by optical microscopy. The contact angle then could be calculated by simple trigonometry. This method can only be used for droplets with a contact angle much larger than 90°, and the obtained contact angle has an error of ≈5°. As mentioned above, we will consider two kinds of surfaces (see Figure 1): Indian Cress as an example for leaves which are smooth on the macroscopic scale (but are microrough) and Lady’s Mantle as an example of a hairy water-repellent surface.
10.1021/la034961d CCC: $27.50 © 2004 American Chemical Society Published on Web 02/19/2004
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Figure 2. Electron microscopy images of an Indian Cress leaf. The individual cells can be seen in panel a, where the wax crystals have been washed off during the fixation process (sample type II). In panel b, the wax crystals of an air-dried leaf (sample type I) are shown.
3. Results and Discussion Overview studies of wetting of plant and grass leaves2,9,10 show that the surface structure of Indian Cress gives a good representation among the water-repelling microrough leaf species. Imaging the surface with the scanning electron microscope reveals structures on three different length scales. One is given by the epidermal cells of the cuticula and corresponds to a few tens of microns (Figure 2a). The size of the wax crystals on top of the cell surface determines a second length scale of ≈1 µm (Figure 2b). A third length scale (≈5 µm) is roughly defined by the distance of the wax crystal bundles. Roughness makes a significant influence on the wetting behavior of a given surface.11-14 The contact angle, which is found at a solid-liquid-gas boundary line on a rough surface, can be described by Wenzel’s law:8
cos Θ* ) r cos Θ
(1)
Here, Θ* is the resulting contact angle for a surface with a given roughness parameter r if the contact angle for an equivalent flat surface is Θ (r is the ratio of the real surface area divided by the projected flat surface area and is therefore always larger than 18). This holds if there is no air entrained in the pits of the roughness below the liquid. It can easily be seen from eq 1 that roughness drives the contact angle away from 90°, either toward complete wetting if Θ < 90 ° or to nonwetting if Θ > 90°. From the electron microscopy data, we can estimate the parameter r ≈ 4.7 of the cuticular wax crystals on top of the cell surfaces (Figure 2b). Using a contact angle for the cuticular wax of Θ ≈ 100°,15 we obtain a contact angle Θ* ≈ 145°. However, for a water droplet on a leaf of Indian Cress as shown in Figure 3a, a contact angle of Θ ≈ 180° is clearly observed. Up to this point, r was only obtained (9) Neinhuis, C.; Barthlott, W. Ann. Bot. 1997, 79, 667-677. (10) The Leaf Surface of Major Crops; Harr, J., Guggenheim, R., Eds.; Friedrich Reinhardt Verlag: Basel, 1995. (11) Bico, J.; Marzolin, C.; Que´re´, D. 1999, 47 (2). (12) Borgs, C.; De Coninck, J.; Kotecky´, R.; Zinque, M. Phys. Rev. Lett. 1995, 74 (12), 2292-2294. (13) Netz, R.; Andelman, D. Phys. Rev. E 1997, 55 (1), 687-700. (14) Patankar, N. A. Langmuir 2003, 19, 1249-1253. (15) Holloway, P. J. J. Sci. Food Agric. 1969, 20, 124-128.
Figure 3. A water droplet (1 mm diameter) on an Indian Cress leaf (a) and on a Lady’s Mantle leaf (b).
from the areal fraction of the rough structure. To search for possible reasons for this discrepancy in Θ, dew was condensed by cooling a leaf of Indian Cress on a Peltier element just below the dew condensation temperature. The microscopic contact angle on the surface was measured by inspecting the growing droplets with an optical microscope. In this way, the contact angle was found to be ≈140° (with an error of about 5°) for droplets ranging from 50 to 500 µm in diameter. While this is in good agreement with the contact angle we calculated from Wenzel’s law (eq 1), it still needs to be explained why a larger contact angle, close to 180°, is found if the water droplet is deposited onto the dry leaf. A hint can be gained by looking at grazing incidence through the drop onto its lower interface, toward the leaf. One observes a silvery shiny layer which is due to total reflection of light at some air trapped in the surface structure.1 In this case, eq 1 is not anymore valid, and it has been shown that the contact angle can be increased if air pockets underneath the liquid are allowed.11 It is clearly pointed out in the article of N. A. Patankar14 that there are multiple equilibrium states for a drop on a rough surface. The particular shape of the drop and therefore the corresponding minimum in energy strongly depend on the way the drop is formed. In the case of a composite interface, a reduced contact area Φs between solid and liquid is introduced, and the resulting contact angle is given by
cos Θ** ) -1 + Φs(cos Θ + 1)
(2)
The fact that the surface structure is based on different length scales suggests a subtle way of taking roughness into account, considering the hierarchical character of the surface. This leads to the concept of a hierarchically rough surface, as elaborated upon in ref 16. The main result is that a surface will be superhydrophobic if its roughness exponent F satisfies
Fg1+
ln Φs 2 ln b
(3)
where Φs refers to each of the roughness hierarchies individually, and b is the ratio of the length scales of two such scales consecutive in hierarchy.17 (16) Herminghaus, S. Europhys. Lett. 2000, 52 (2), 165-170.
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Figure 5. Condensed hair cluster holding a water droplet (2 mm diameter).
Figure 4. SEM image of a nanotube pattern (a). Optical microscopy image of the water-covered sample with air pockets (b).
The effect of the presence of air pockets in a periodically rough structure can be illustrated by using a model system composed of a patterned substrate (pattern size of about 50 µm) where the structure was made of about 10 µm high carbon nanotube bundles, shown in Figure 4. The nanotubes themselves have a diameter of few nanometers.18 Our sample was prepared by microcontact printing of a pattern with a catalyst on a silicon wafer. The nanotubes were then grown out of the gas phase on the catalyst pattern.19 In Figure 4a, bunches of nanotubes with a height of about 10 µm can be seen. This gives us a structured rough sample of two length scales. One scale is the pattern of the printed catalyst; the other scale is the roughness of the nanotube bundles. This system shows a water contact angle close to 180° when a water droplet is put on the dry substrate. However, if the substrate is cooled with a Peltier element below the dew condensation temperature, water droplets start nucleating on the silicon surface between the bundles of carbon nanotubes. A water droplet deposited on this already wetted surface now shows a contact angle of about 90°. This can be reverted to 180° by drying the substrate with for example nitrogen gas and putting a new droplet on the dry substrate. The significant difference between the dry and the prewetted state is that in the latter case, some water is already in contact with the substrate areas between the nanotube bundles. A droplet deposited afterward is then in contact with the water-coated substrate, and no air pockets emerge. Conversely, if the droplet is deposited on the dry substrate, the water-air interface spans from one nanotube bundle to the next, with air pockets in between. The presence of these air pockets can again be directly observed by looking through a drop of water onto the nanotube pattern with an optical microscope (Figure 4b). The drop was placed on the substrate in a slightly prewetted state, so that some of the pattern compartments had condensed water inside, and other compartments form a composite surface. The bright appearance of some of the fields (upper left) is due to air entrapments underneath (17) Please note that the 2 in the dominator on the right-hand side was erroneously missing in ref 16. Equation 3 in the present article represents the correct result. (18) Salvetat, J. P.; Bonard, J. M.; Thomson, N. H.; Kulik, A. J.; Forro´, L.; Benoit, W.; Zuppirolli, L. Appl. Phys. A 1999, 69, 255-260. (19) Kind, H.; Bonard, J. M. Adv. Mater. 1999, 11 (15), 1285-1289.
the water drop. This is accompanied by a large contact angle and was not observed on an already wetted sample. The findings presented above suggest that the water repellence of microrough plant leaves is due to a specific roughness comprising a hierarchy of length scales. The material of which the structure consists is supposed to have a contact angle >90° (which can be assumed for cuticular waxes), and the existence of air entrapments underneath the liquid is necessary to explain the particularly high contact angles observed. Further information about the interplay of different length scale structures has to be collected in order to understand other effects, like self-cleaning, which can also be found on many Lotuslike leaves.2 Let us now turn to the second type of surfaces to be discussed, the hairy leaves of some plants, such as Lady’s Mantle (Alchemilla vulgaris L.). As mentioned above, water droplets also run off these leaves very easily, and a water droplet put onto the leaf carefully rests on the fur as a sphere with seemingly no contact to the leaf surface, which may be taken as a contact angle of 180° (Figure 5). At first glance, one might attribute this behavior to the hairs being sufficiently hydrophobic (Θ > 90°) (with the caveat that with wetting of droplets on fibers, surface dimensions and curvature of the wetted substrate must be taken into account20-23). In this picture, the hairs would play a role perfectly analogous to the crystals of cuticular wax in the case of the microrough surfaces. However, the hairs of the Lady’s Mantle have in fact a contact angle well below 90°. To demonstrate this, a single hair of a Lady’s Mantle was stuck into a water droplet, and several optical microscopy pictures were taken as the drop evaporated, such that its surface moved to different positions along the hair (Figure 6a). The contact angle, as obtained from the droplet meniscus at the hair, was found to be below 60° all along the hair (Figure 6b). The advancing contact angle, which was checked by moving the hair into the drop, was not found to be significantly larger. This is astonishing, since one would expect a surface with a dense brush of hydrophilic hairs to be manifestly hydrophilic, with the liquid being sucked into the brush as into blotting paper. Another striking observation is made when looking with the optical microscope at small droplets nucleating on a cooled (by a Peltier element) Lady’s Mantle leaf. The small droplets nucleate on the ground (the cuticula) with a contact angle well above 90°, but as soon as they make contact with the hairs, they are lifted from the cuticula into the brush, stick to the hairs, as these are more hydrophilic than the (20) Carroll, B. J. Langmuir 1986, 2, 248-250. (21) Carroll, B. J. J. Colloid Interface Sci. 1984, 97 (1), 195-200. (22) Que´re´, D. Annu. Rev. Fluid Mech. 1999, 31, 347-384. (23) Bonard, J. M. EPFL-Lausanne, CH, Carbon Nanotube Samples.
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Figure 6. Contact angle measurements along a Lady’s Mantle hair: (a) overlay of the droplet meniscus at different positions (droplet to the right); (b) contact angle as a function of distance along the hair.
Figure 7. Sketch of the elastic deformation of the hairs due to bundle formation at the liquid-air interface.
cuticula, and are thus energetically preferred (Figure 5). The droplets sticking to the hairs show the known states of fiber wetting (roll-up shape) and coalesce when they get in contact with other droplets.20 Electron microscopy confirmed that on a small scale, the leaves of the Lady’s Mantle are covered with cuticular wax dandruffs. The cells are, like those of the Indian Cress, covered with a rough wax structure. Therefore, on a microscopic scale the droplets sense the same hydrophobicity as on the microrough surfaces discussed above. During the growth of the droplets, they are lifted into the brush of hydrophilic hairs, apparently because the latter are more hydrophilic than the cuticula. To understand why a brush of hydrophilic hairs might be effectively hydrophobic, we consider a bundle of hairs stuck into a liquid-air interface (Figure 7) and take into account the elasticity of the hairs. If the hairs have a contact angle different from 90°, the liquid surface will deform around the hair according to Young’s equation. The surface energy of a liquid is given by f(1 + |∆f 2|)1/2
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where f(r) describes the vertical surface position. Deformation of the liquid surface in either way will cost energy and results in an attractive (logarithmic) potential between the hairs. Note that this is the case for any microscopic contact angle different from 90°, either above or below. It is therefore to be expected that a number of hairs will condense to individual bundles, such that the hairs meet each other at the water-air interface. To force the hairs into bundles, most of them will have to bend, which costs elastic energy, according to the elastic modulus of the hairs. If one considers an infinite sample, one finds that the total energy of the system is minimized when the hairs group into bundles of a particular size, which depends on the distance h between the substrate (cuticula) and the water-air interface. If we now try to move the interface closer to the substrate, on which the hairs are anchored, it is directly seen from Figure 7 that the hairs will have to bend more strongly. We thus see that the elasticity of the hairs results in a repulsive interaction between the cuticula and the water/air interface. If we allow the number of hairs per bundle to rearrange when h is changed, we find for the elastic energy contribution
Γ ∝ xKh-1/2
(4)
where K represents the elastic modulus of the hairs. Therefore, if the mean density of hairs is high enough to form clusters and if the contact angle of water at the hairs differs significantly from 90° (as we have clearly observed), a water droplet will be kept away from the cuticula, as is observed on the macroscopic scale. Nevertheless, this state can also be overcome by forcing the liquid all the way to the cuticula, so that the hairs are completely immersed in water. In this state, the contact angle is only determined by the roughness of the cuticula. 4. Conclusion In this article, we were able to show that the water repellence of certain plant leaves can be explained by considering surface roughness on different length scales and sometimes additional elastic structures (hairs) covering the surface. The minimum hierarchical degree of roughness needed to achieve superhydrophobic behavior has not yet been revealed, but plants such as for example Indian Cress seem to get along with three different length scales of roughness. For the hairy plant leaves, the elastic modulus of the hairs and the areal coverage are important additional parameters to gain hydrophobicity with spherical droplets resting in the leaf’s fur, even though the hairs are hydrophilic. Acknowledgment. We are indebted to J. M. Bonard and his group for kindly providing the carbon nanotube samples. We thank Ch. Neinhuis and W. Barthlott for interesting discussions and for Lotus leaf samples used in some of our experiments. LA034961D
