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Passive Water Collection with the Integument: Mechanisms and Their Biomimetic Potential (Doi:10.1242/ Jeb.153130) Philipp Comanns

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Passive Water Collection with the Integument: Mechanisms and Their Biomimetic Potential (Doi:10.1242/ Jeb.153130) Philipp Comanns © 2018. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2018) 221, jeb185694. doi:10.1242/jeb.185694 CORRECTION Correction: Passive water collection with the integument: mechanisms and their biomimetic potential (doi:10.1242/ jeb.153130) Philipp Comanns There was an error published in J. Exp. Biol. (2018) 221, jeb153130 (doi:10.1242/jeb.153130). The corresponding author’s email address was incorrect. It should be [email protected]. This has been corrected in the online full-text and PDF versions. We apologise to authors and readers for any inconvenience this may have caused. Journal of Experimental Biology 1 © 2018. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2018) 221, jeb153130. doi:10.1242/jeb.153130 REVIEW Passive water collection with the integument: mechanisms and their biomimetic potential Philipp Comanns* ABSTRACT 2002). Furthermore, there are also infrequent rain falls that must be Several mechanisms of water acquisition have evolved in animals considered (Comanns et al., 2016a). living in arid habitats to cope with limited water supply. They enable Maintaining a water balance in xeric habitats (see Glossary) often access to water sources such as rain, dew, thermally facilitated requires significant reduction of cutaneous water loss. Reptiles condensation on the skin, fog, or moisture from a damp substrate. commonly have an almost water-proof skin owing to integumental This Review describes how a significant number of animals – in lipids, amongst other components (Hadley, 1989). In some snakes, excess of 39 species from 24 genera – have acquired the ability to for example, the chemical removal of lipids has been shown to – passively collect water with their integument. This ability results from increase transepidermal water permeation by a factor of 35 175 chemical and structural properties of the integument, which, in each (Burken et al., 1985). species, facilitate one or more of six basic mechanisms: increased Amphibians, by contrast, typically lack a significant resistance to surface wettability, increased spreading area, transport of water over cutaneous water loss (Bentley and Schmidt-Nielsen, 1966; Shoemaker relatively large distances, accumulation and storage of collected and Nagy, 1977; Toledo and Jared, 1993; Maderson et al., 1998; water, condensation, and utilization of gravity. Details are described for Lillywhite, 2006). The low resistance to cutaneous water loss can each basic mechanism. The potential for bio-inspired improvement of be seen as a cost for transcutaneous water uptake and respiration technical applications has been demonstrated in many cases, requiring a moist skin (Chew, 1961). In some arboreal hylid frogs, in particular for several wetting phenomena, fog collection and however, a significant reduction of evaporativewater loss is provided passive, directional transport of liquids. Also considered here are by a cutaneous secretion of lipids (Shoemaker et al., 1972; Blaylock potential applications in the fields of water supply, lubrication, heat et al., 1976; McClanahan et al., 1978; Toledo and Jared, 1993; Amey exchangers, microfluidics and hygiene products. These present and Grigg, 1995; Tracy et al., 2011). Similarly, arthropods achieve opportunities for innovations, not only in product functionality, but reduced water loss by protective lipid and wax layers of the cuticle also for fabrication processes, where resources and environmental (Beament, 1964; Edney, 1977; Hadley, 1989, 1991). impact can be reduced. Despite such reduction of water loss, additional water demand has been found in many species. In desert reptiles, a number of species KEY WORDS: Water collection, Moisture harvesting, Biomimetic, require additional water collection, although they often rely to a large Capillary channel, Surface structures, Hydrophilic, Wetting degree on the water content of their diet to cover their water demand (Bentley and Blumer, 1962; Nagy, 1987; Maderson et al., 1998; Introduction Lillywhite, 2006). For some desert lizards, this necessity results from There are numerous studies investigating the adaptations in nature their mainly myrmecophagous diet (see Glossary), which demands to limited resources. Some reptiles, amphibians, arthropods, birds special mechanisms to support excretion of high concentrations of and even mammals have been found to survive restrictions on water electrolytes (Bradshaw and Shoemaker, 1967; Withers and Dickman, supply by using their body surface to collect water from various 1995). Lately, some studies on diet-based water demand discuss the sources (Louw, 1972; Rijke, 1972; Lillywhite and Licht, 1974; uptake of freewateras a general strategyfora numberof desert reptiles, Gans et al., 1982; Lillywhite and Stein, 1987; Sherbrooke, 1990; in particular carnivorous reptiles, which often show a more or less Cardwell, 2006; Tracy et al., 2011). Collecting water in arid distinct need for uptake of free water in order to obtain a net gain of environments might appear to be contradictory at first, but water (Wright et al., 2013; Lillywhite, 2017). In many amphibians, nevertheless many such areas are known to provide water sources. water collection is required to replenish the water loss from mucus For example, dew is regularly found in most deserts early in the secretion, in particular for thermoregulation and counteracting morning, originating from significant day–night temperature dehydration of the epidermis (see Glossary) at higher temperatures differences (Louw, 1972). The Namib desert is famous for its fog (Lillywhite and Licht, 1975; Lillywhite et al., 1998). Some toads (Shanyengana et al., 2002); depending on the location, fog events prevent dehydration of the skin directly by collecting water from their occur 40–200 days per year (Seely, 1979; Shanyengana et al., environment (Lillywhite and Licht, 1974). In general, the need for water collection is often for rehydration, but it is also needed for water adsorption, which prevents dehydration of the skin (Lillywhite and Licht, 1974). Furthermore, collected water serves the RWTH Aachen University, Institute of Biology II (Zoology), Worringerweg 3, 52074 thermoregulation in elephants and wharf roaches (Hoese, 1981; Aachen, Germany. Lillywhite and Stein, 1987), is transported by adult sandgrouse from *Author for correspondence ([email protected]) water sources to hydrate the young (Cade and MacLean, 1967), and yields reduced reflectivity for camouflage in flat bugs (Silberglied and P.C., 0000-0002-2020-0515 Aiello, 1980; Hischen et al., 2017). This is an Open Access article distributed under the terms of the Creative Commons Attribution Passive water collection takes place from sources of the animals’ License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. environment; for example, from water puddles, infrequent Journal of Experimental Biology 1 REVIEW Journal of Experimental Biology (2018) 221, jeb153130. doi:10.1242/jeb.153130 drinking (snakes), spreading (see Glossary) over the body surface Glossary (toads, elephants, flat bugs and beetles), transport to other parts of Condensation the body surface (lizards, tortoises and wharf roaches) or storage in Phase transition of water from gaseous to liquid. the plumage (sandgrouse) (Table 1). In the end, water is Contact angle incorporated in some way in all described cases, but not in flat – Quantification of the liquid substrate interaction (see Fig. 2). bugs and elephants. Epidermis The outer skin layers. These collection processes and subsequent handling of collected Hydrophilic substrate water involve different, specific chemical or structural adaptations A substrate that can be wetted by aqueous liquids. of the body surface. Based on these general considerations, six basic Hydrophobic substrate mechanisms have been identified as being involved in passive water Water-repellent substrate surface. collection (Fig. 1): (1) increased surface wettability; (2) increased Hygroscopic substrate spreading area; (3) transport of water over relatively large distances; A material that can absorb moisture from air. Integument (4) accumulation and storage of collected water; (5) facilitating Body surface of animals (skin or cuticle), including its derivatives such as condensation; and (6) utilization of gravity (see Glossary for the scales, feathers, etc. terms described). Laser ablation In more detail, an increased surface wettability of the integument Removal (often favoured: sublimation) of substrate material by laser (1), i.e. smaller contact angles (see Glossary), results from either irradiation. chemical properties and/or microstructures (Fig. 2), such as different Micromilling A rotating cutting fabrication method in the micrometre range. kinds of pillar and hexagonal dimples (Bormashenko, 2010; Myrmecophagous diet Comanns et al., 2014). The spreading area (2) can be increased by A diet mostly consisting of ants. similar microstructures, which allow subsequent drinking of water Oleophilic substrate (Bico et al., 2002; Chandra and Yang, 2011). Further structures, i.e. A substrate that can be wetted by oil. grooves or channels, are required to transport water (3) over larger Pennaceous feather distances or precisely in one direction (Berthier and Silberzan, 2010; A type of feather present in most modern birds: containing a quill/rachis Comanns et al., 2015). It
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