Glochids microstructure and dew harvesting ability in Opuntia stricta (Cactaceae)

1 Introduction

Of planet earth́s mainland, about one-third is classified as arid or semiarid (Whitford, 2002). Drought represents the prominent environmental condition of these areas, controlled largely by climatic factors, especially temperature and precipitation. In all arid or semiarid regions, annual rates of evaporation exceed that of precipitation, resulting in shortage or absence of surface fresh water. Organisms in such habitats must cope with water shortage, thus often morphological and metabolic adaptations enable them to acquire enough amounts of water (Cloudsley-Thompson, 1996; Batanouny, 2001). Most organisms obtain liquid water through absorption or imbibition, ingestion of hydrated solids, or metabolically from the food (O'Donnell and Machin, 1988). As liquid water is usually scarce in arid and semiarid habitats, many organisms inhabiting such environments are adapted to obtain water directly from the atmosphere (i.e. airborne moisture) (Henschel and Seely, 2008; Malik et al., 2014). These “moisture harvesters” include some animals like desert beetles, frogs, lizards and spiders (Parker and Lawrence, 2001; Zheng et al., 2010; Malik et al., 2014), and many plants (Ju et al., 2012; Malik et al., 2014, 2015; Azad et al., 2015; Sharma et al., 2016; Gürsoy et al., 2017).

Fog and dew are most prominent sources of airborne water that emerge from excess water vapour in the air, condensing on surfaces as water droplets. If droplets are suspended in the air and visible as shallow clouds, they are called fog (Fessehaye et al., 2014). Fog is formed through cooling of air below dew point that condenses as water drops on surfaces. Dew is formed when the humid air condenses on a surface as water drops (Beysens, 1995). In many arid and semiarid regions, fog and dew represent a constant water source depending on prevailing climatic conditions (Jacobs et al., 1999; Eckardt et al., 2013) and may even exceed the amount of annual rain during severe drought years (Evinari et al., 1971). Therefore, fog and dew play an important role in those environmentally demanding habitats.

To condensate atmospheric moisture to a dew-drop, preceding nucleation must progressively enhance. Nucleation means the formation and coalescence of minute, thermodynamically stable droplets from water vapour (Beysens, 1995). In a favorable microclimate, nucleation is largely dependent on the microstructure of the surface (Beysens, 1995; Agam and Berliner, 2006).

Important for drop formation on a solid surface is the contact angle (θ_c), the angle that forms at the three-phase boundary (where the liquid–vapour interface meets a solid surface (Koch and Barthlott, 2009)). When the contact angle is less than 90°, the surface is called hydrophilic, which means that wetting occurs and a drop will cover a large area on the surface. Whereas with a contact angle more than 90°, the surface is called hydrophobic with less wettability. A water drop on a hydrophobic surface tends to take a more spherical shape (Fig. 1a) and will only touch a small area on the surface. When the drop is moving on the surface, the contact angles of both sides of the drop tend to take a maximum (expanding) and a minimum (contracting) value, called advancing contact angle (θ_a) and receding contact angle (θ_r), respectively (Fig. 1b) (Yuan and Lee, 2013).

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Fig. 1

A. Drop behavior on the surface. Value of contact angle (θ_c) represents the measure of hydrophobicity or hydrophilicity of the surface. B. In the state of drop motion, the contact angles of both sides tend to take a maximum and minimum value, called advanced contact angle (θ_a) and receding contact angle (θ_r), respectively.

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Few cacti inhabiting arid and semiarid regions are known to collect fog and dew with their spines or glochids (Mooney et al., 1977; Ju et al., 2012; Liu et al., 2015; Malik et al., 2015). Although there are hundreds of cacti species, their spines, and especially glochids vary greatly in surface microstructure (Gibson and Nobel, 1986; Mosco, 2009; Liu et al., 2015). Since dew condensation on a surface is controlled by air temperature, humidity and the surface microstructure (Beysens, 1995), spine microstructure determines the ability of a cactus species for effective dew harvesting under a suitable microclimate (Malik et al., 2015; Guo and Tang, 2015). To date, only a few cacti species have been confirmed to be efficient moisture harvesters (Malik et al., 2014, 2015; Guo and Tang, 2015).

Opuntia stricta (Haw.) Haw. is a spiny stem succulent of the Cactaceae family, native to southeast America, eastern Mexico and Caribbean islands, and is invasive in other regions including south and east Africa, south-western Saudi Arabia, Yemen, India and Australia (Masrahi, 2012; Masrahi and Sayed, 2017; Shackleton et al., 2017). So far, no studies describe this species as an atmospheric moisture harvester. Therefore, this study aims to investigate the microstructure of O. stricta glochids in relation to its dew harvesting ability. For this, SEM imaging was used to characterize microstructural features of glochid. Mist stream generator was used to simulate dew formation events on the glochids in the field. Glochid microstructural features and dew harvesting ability have been discussed with the applicable physical principles.

2 Materials and methods

2.1

2.1 Plant materials

The stem of O. stricta consists of segments. Every segment has scattered bud areas (areoles) bearing spines (2–3, each 10–25 mm) and many glochids (tiny spines) with dense minute trichomes at the base (Fig. 2a,b, Fig. 4a). Samples of stem segments were collected in May 2018 from rocky habitats east of Tihama of Jazan region (Saudi Arabia), at an altitude of 300–400 m, in which the plant invaded vast areas (Masrahi and Sayed, 2017). The areoles bearing spines and glochids were carefully selected for subsequent analyses. The spines of this cactus species are almost glabrous without any prominent structures on their surfaces, and did not show efficient dew collection ability. Thus, they were ignored in this study.

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Fig. 2

A. Stem segments of Opuntia stricta that bearing bud areas (areoles) with spines and glochids. B. One areole with its spines and glochids (one glochid enclosed by rectangle). C. SEM image of a single glochid with oriented barbs on the surface. D and E. Apex angle for glochid tip (δ₁) and barb (δ₂), respectively. In E, it's clear that tip of each barb is smooth whereas the base is rougher with microgrooves (arrowheads).

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3 Results

3.2

3.2 Dew harvesting observations

After one minute, glochids located in front of the mist stream show deposited water droplets on their surfaces. A progressive manner of droplet growth is observed at the glochids, whereby in the first step droplets nucleate at the tip of the barbs and also on the glochid tips (Fig. 3). Then small droplets move from the tip to the base of the glochid and coalesce together to form bigger droplets. The bigger droplets of ∼130 µm diameter start to move down to the glochid base (Fig. 3a–c). Analyses reveal a big advancing contact angle (θ_a) and relatively small receding contact angle (θ_r) (76.25 ± 16.8° and 52.5 ± 12.6°, respectively) for the “moving” droplets. Although most glochids in the experiment are vertical or semi-vertical, droplet deposition also happens at glochids with semi-horizontal orientation (tilt angle ∼ 0). The mean diameter of growing droplets that start to move towards the base of the glochids is = 131.25 ± 40.3 µm, which is appears as a critical size for droplet moving.

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Fig. 3

A-C. Optical microscopic images of water collection on the glochids. Each glochid reveals a progressive manner of droplets growing, which appeared to start at the tip of the barbs and also on glochid tips. D. Diagram of starting deposition of droplets and the gradually growing (coalesce with each other) to become a large drop moving to the base.

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Fig. 4

A. Optical image of areole with its glochids and dense mat of trichomes in the base. The insertion is SEM image of trichomes. B. Geometry of barb and glochid (cone-shape). In the cone shape, the difference between small radius (R₁) and large radius (R₂) generate Laplace pressure gradient that drives the drop to the base.

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4 Discussion

The glochids of O. stricta have a unique microstructure ordered in a hierarchical manner, and organized into substructures that contribute to dew harvesting ability. The glochids and barbs covering them have a conical shape in the range of cone-apex angles of 9.25–41.5°. The conical shape of such morphological features produce a Laplace pressure gradient on the surface (Lorenceau and Quéré, 2004; Ma et al., 2015; Masrahi and Al Shaye, 2017). The tip of the cone (tip of the glochid or barb) has a larger Laplace pressure than the base of the cone (base of the glochid or barb). This difference is generated by the small radius-high curvature at the tip of the cone to the large radius-low curvature at the base of the cone (Fig. 4b), which can expressed by the Laplace theorem (Eggers and Villermaux, 2008):$$\mathrm{\Delta }p=\gamma (1/{\text{R}}_1+1/{\text{R}}_2)$$where R₁ and R₂ are the radii of curvature, γ is the surface tension of water droplet. The Laplace pressure gradient along the cone, from the tip to the base, and hence between the two sides of the droplet, represent one of the driving forces that lead to a spontaneous movement of the droplet from the tip of the glochid (and tip of the barb) to the base, but only when a critical size of ∼130 µm of the droplet is reached.

The glochid exhibits more prominent grooves towards the base. The same surface features also appear on the barbs, in which microgrooves increase toward the base. This increasing “roughness” of the surfaces of glochids and barbs from the tip to the base, may generate another driving force for droplet movement from the tip to the base of cone structures, according to the Wenzel relation (Quéré, 2008; Zhao et al., 2014; Guo and Tang, 2015):$$cos{\theta }^{\ast }=rcos\theta$$where r is surface roughness, θ* and θ are the apparent and intrinsic contact angles on rough and smooth surfaces, respectively.

In the principle of surface energy gradient, water droplets tend to be driven along a gradient of wettability, from low surface energy (less wettable) to high surface energy (more wettable) (Brochard, 1989; Chaudhury and Whitesides, 1992). In general, spines and glochids of plants from the family of Cactaceae have a similar character. They are waterproof due to cuticle and sclerified cells (Gibson and Nobel, 1986), while the trichomes in the base of the glochids have high wettability (Kim et al., 2017). The tips of glochids and barbs have a low surface energy, compared to the hygroscopic trichomes at the base of glochids that have high wettability. This gradient of surface energy seems to be the third driving force for the droplet movement, especially when droplets move and coalesce with each other to become a larger drop that gets absorbed by the highly wettable trichomes.

The experimental observations reveal the mechanisms behind dew harvesting of O. stricta enabled by a specialized microstructure of its glochids and barbs with anisotropic surfaces. Under favorable conditions, water molecules are captured as very small droplets on the tip of the cone structure (Cao et al., 2014). At the glochids and barbs, once the droplet is captured by the tip, it moves to the base, and all droplets from the barbs move by the same manner and coalesce together forming larger droplets, progressively forming larger drops that move towards the base where the trichomes are located (Fig. 3d). The trichomes then absorb the drops (Fig. 4). A big advancing contact angle (θ_a) and a small receding contact angle (θ_r) result in a “movement” of the droplets (Yuan and Lee, 2013). The droplet movement proceeds always towards the base of the glochids, even if the tilt angle is semi-horizontal. The mean volume of the growing droplets on the glochids is small (131 µm). When the droplet volume is small, the surface energy overcomes the gravitational force, and vice versa if the droplet volume is too large (>500 µm) (Ren et al., 2010; Chou et al., 2011). This range in size of growing droplets is preferential if the glochids was down or semi-down vertical in direction.

5 Conclusion

The dew harvesting ability of the glochids in Opuntia stricta was investigated and can be attributed to the microstructure of glochids with a hierarchical manner and an anisotropic surface. The water droplet is nucleating on the tip of the cone structure (tip of the glochid and tips of the barbs on the glochid surface) and starts to move towards the base. Tiny droplets coalesce with each other, becoming larger drops and become absorbed by trichomes at the base of glochids. This ability of dew harvesting appears to be controlled by three forces, Laplace pressure difference, Wenzel relation and differences in surface wettability. Ability of dew harvesting in O. stricta represents an adaptive trait in this plant that inhabits mostly arid land. On the other hand, the ability of dew harvesting in O. stricta with its glochid microstructure may act as template for biomimetic inspired designs and contribute to solve the problem of water shortage in dry regions.