Leaf trichomes of Dendrobium species (epiphytic orchids) in relation to foliar water uptake, leaf surface wettability, and water balance

Highlights

• The epiphytic species with trichomes show a higher percentage increase in leaf water content.

• The trichome density is closely related to stomatal traits, but not with leaf water loss rates.

• The epiphytic species with trichomes dries faster from saturated leaves to 70 % relative water content.

• A potential trade-off exists between leaf water absorption and conservation in epiphytic species.

• Different water use strategies are utilized by the leaves of epiphytic orchids with and without trichomes.

Abstract

Vascular epiphytes play an important role in the water and carbon cycles of forest ecosystems. While trichomes are found on the leaf surface of many epiphytic species, few studies have investigated the effect of leaf trichomes on their foliar water uptake, leaf surface wettability, and water balance. In our study, leaf water absorption, storage, and retention capacities, as well as leaf surface wettability of twelve Dendrobium species with glabrous (n = 6) and piliferous (n = 6) leaves were investigated and related to their leaf morphological and anatomical characteristics. Our results showed that no significant difference in foliar water uptake capacity was found between groups with different leaf surface types (with and without trichomes). However, the piliferous Dendrobium species showed a significantly larger increase in leaf water content (%LWC) and lower values for both saturated water content per unit mass and water retention capacity compared to glabrous ones. Across Dendrobium species with piliferous leaves, the trichome density on leaf abaxial surface was positively correlated with foliar water uptake capacity per unit area, contact angle, stomatal density and stomata area per unit index. Besides, species with a higher %LWC after leaf immersion dried faster from saturated leaves to a relative water content of 70 %, which suggests a potential trade-off between leaf water absorption and conservation in epiphytic Dendrobium species. The variation in leaf water absorption and conservation suggests that different water use strategies are utilized by epiphytic orchids with glabrous and piliferous leaves.

Introduction

Vascular epiphytes are an important component of tropical and subtropical forests, and are of great significance to the maintenance and stability of the entire forest ecosystem (Zotz and Bader, 2009; Zotz, 2016). Unlike soil-rooted plants, the roots of vascular epiphytes are mostly exposed to the atmosphere, making them unable to obtain sufficient water from the soil through their root systems (Benzing, 1998). Therefore, atmospheric water availability is one of the most important environmental factors that limit the survival, growth, and vegetative function of vascular epiphytes (Zotz et al., 2010; Zotz, 2016). In the context of global warming and increasing variability in precipitation, drought events occur more frequently and exacerbate the water stress of epiphytes and even threaten their survival, growth, and distribution (Eller et al., 2020). Revealing the difference and diversity in the strategies for maintaining water balance by vascular epiphytes could help predict their potential responses to global warming and increasing drought.

Water management and/or water utilization strategies of leaves plays an important role in the water balance of vascular epiphytes. The leaf water balance is largely determined by leaf structural characteristics (Pivovaroff et al., 2014). The leaves of vascular epiphytes are usually thick and highly succulent, with a thick epidermis and densely distributed trichomes. These distinctive leaf traits contribute to improving the water storage capacity (the ability to store water) and water retention capacity (the ability to minimize water loss; Zhang et al., 2015; Yang et al., 2016). Recently, foliar water uptake (FWU) has been realized as a global physiological phenomenon in plants (Berry et al., 2019; Schreel et al., 2019a; Boanares et al., 2020; Schreel and Steppe, 2020; Fernández et al., 2021), and attracts a lot of attention because of its important role in plant response to climate change and increasing drought (Schreel and Steppe, 2019; Schreel et al., 2019b; Boanares et al., 2021; Waseem et al., 2021). FWU is also an important strategy for epiphytes to maintain their water balance (Gotsch et al., 2015; Darby et al., 2016; Wu et al., 2018). Stomata (Burkhardt, 2010; Burkhardt et al., 2012; Binks et al., 2020; Guzmán-Delgado et al., 2021), cuticles (or epidermis) (Grammatikopoulos and Manetas, 1994), hydathodes (Martin and von Willert, 2000; Boanares et al., 2019), and trichomes (Fernández et al., 2014; Pina et al. 2016; Schreel et al., 2020) are considered to be the potential pathways for FWU. However, few studies have investigated the synergistic relationship between FWU and leaf anatomical structures for vascular epiphytes.

The interaction between leaf surface and water status has always been a matter of scientific interest (Fernández and Eichert, 2009). The contact angle (θ, CA) between the leaf surface and an applied water droplet is used to reflect the leaf surface wettability (Brewer et al., 1991). According to the difference of CA, a leaf is defined as wettable when CA < 90°, and non-wettable when CA > 90° (Fernández et al., 2021). Leaf wettability depends on leaf surface cuticle properties and trichomes, and is also related to leaf shape morphology such as the presence of drip tips (Fernández et al., 2017; Goldsmith et al., 2017; Dawson and Goldsmith, 2018). High wettability reduces leaf transpiration and could promote FWU (Dawson and Goldsmith, 2018; Fernández et al., 2021). Leaf wettability and its influence on leaf wetness, transpirational water loss and FWU are of great importance for the water balance of epiphytic plants as their physiological processes are highly dependant on the leaf wetness and the relative humidity of the habitat (Koch et al., 2006). However, how the leaf structures of vascular epiphytes, such as trichomes, influence their leaf surface wettability remains to be investigated.

Trichomes are epidermal appendages on many plant organs. Structurally, trichomes are either unicellular or multicellular, and can be divided into glandular or non-glandular types based on their function (Werker, 2000). The growth of most trichomes is closely related to extreme moisture environments (arid or humid) (Kessler et al. 2007; Schwerbrock and Leuschner, 2016; Waseem et al., 2021). Many studies have shown that leaf trichomes have crucial ecophysiological consequences for the leaf water balance (Benzing, 1976; Ohrui et al., 2007; Bickford, 2016; Amada et al., 2020). Trichomes can affect leaf wettability (Brewer et al., 1991; Grammatikopoulos and Manetas, 1994; Brewer and Smith, 1997; Fernández et al., 2014), promote the absorption of water and nutrients (Benzing, 1976; Schmitt et al., 1989; Munné-Bosch et al., 1999; Vanhoutte et al., 2017; Leroy et al., 2019), and are related to drought adaptation (Waseem et al., 2021). A previous study indicated that the foliar water uptake capacity and the wettability of the leaf surfaces of Tillandsia species (epiphytic plants) are influenced by their foliar trichomes (Zambrano et al., 2019). However, the ecophysiological significance of leaf trichomes in epiphytic orchids, an important group of epiphytic vascular plants, is not well-studied.

Epiphytic orchids account for a large proportion of vascular epiphytes, which are widely distributed in tropical and subtropical regions (Zotz, 2013). Dendrobium Sw. plants (epiphytic orchids) are one of the largest genera in the orchid family with around 1000 species (Ji, 1999), with Sect. Formosae (Benth and Hook. f.) a group of epiphytic Dendrobium whose leaf surface, sheath, and pseudobulb covered with non-glandular trichomes. However, both glandular and non-glandular trichomes are observed on the leaf surfaces of the same species. In our study, we mainly focused on the non-glandular trichomes (Sect. Formosae as piliferous Dendrobium, others as glabrous Dendrobium). Non-glandular trichomes are predominantly present on the abaxial leaf surface, while the adaxial leaf surface is mostly glabrous or with sparse trichomes. The density of non-glandular trichomes growth on the abaxial and adaxial leaf surfaces may play an important role in their leaf water balance, leaf surface wettability, and ecological adaptations.

In this study, we compared leaf water balance, leaf wettability and leaf anatomical structures of six piliferous and six glabrous Dendrobium species grown in a common garden. The aim of our study was to understand the influence of non-glandular trichomes on the leaf water balance and surface wettability of Dendrobium epiphytes. We hypothesized that the Dendrobium species with piliferous leaves show lower drought tolerance but more water absorption than species with glabrous leaves. We also hypothesized that there is a trade-off between water absorption and conservation (retention and storage) in leaves of epiphytic orchids. The results from the present study will improve our understanding of different water-use strategies by epiphytic orchids in relation to leaf surface structures.