Mobile animals can respond to a threatening event either by fighting against it or fleeing to a more favourable environment. For plants, such responses are physically impossible despite being exposed continuously to challenging environmental conditions, including mechanical forces induced by wind or water currents in flow-dominated habitats (Harder et al., 2006; Read and Stokes, 2006). In the short term, wind affects plants in the form of abrasion, wind throw, and by influencing heat and gas exchange. In the long run, prolonged exposure to wind can alter developmental processes such as growth (Nobel, 1981). Some plants are capable of responding rapidly to mechanically-induced stress with specialised cells which are part of the plants’ touch-response machinery (Braam, 2005). An example is the fast folding leaflets of Mimosa pudica when touched (Malone, 1994). Another well-documented response is termed “thigmomorphogenesis”, coined by Jaffe (1973) to describe the natural phenomenon where external mechanical stimuli induce gradual physiological and morphological alterations in the plant, which allow plants to withstand greater mechanical stresses (Braam, 2005; Telewski and Jaffe, 1986). For example, the degree of thigmomorphogenesis displayed by Phaseolus vulgaris is positively related to the amount of wind, an arguably adaptive response that minimizes damage by wind gusts (Hunt and Jaffe, 1980).
There has been extensive research since the 1970s to investigate morphological and biomechanical responses in trees and herbaceous plants subjected to wind loading (Jaffe et al., 2002). Such morphological changes are virtually universal in higher plants and include 1) reallocation of biomass between roots and shoots, 2) changes in shoot and root architecture, and 3) proportional changes of organs and internal plant structures (Fournier et al., 2006). These changes generally result in either an increase in tissue rigidity or higher flexibility to counteract the mechanical perturbations (Biddington, 1986). More specifically, developmental changes in trees and herbaceous plants include an increased tapering of stems, shorter branches, smaller leaves, more secondary xylem and decreased cell division in the vascular tissues and pith (Biro et al., 1980; Gartner, 1994; Heiligmann and Schneider, 1974; Hunt and Jaffe, 1980; Telewski and Jaffe, 1986). However, adaptive alterations in the root system, as a result of aboveground perturbations, have been studied in less detail (Reubens et al., 2009), and responses were often more varied and complex than the general responses described above for aboveground plant structures. For example, brushing of the shoot resulted in declined root length in cauliflower, lettuce and celery (Biddington and Dearman, 1985) but elicited no response in squash (Turgeon and Webb, 1971), sunflowers (Beyl and Mitchell, 1983) and peas (Akers and Mitchell, 1984). For trees, in spite of some general responses (i.e., root/shoot biomass ratio increases in mechanically stressed trees, Stokes et al., 1997), there are variations related to the specific root system and species (Reubens et al., 2009). For example, Stokes et al. (1995) found that wind-disturbed spruce trees had windward roots that were more branched with longer and larger woody tips than leeward roots. Wind-disturbed pines, in turn, had larger root diameter and leeward root tapering was stronger than on the windward side (Watson and Tombleson, 2002). Studying the root system is important because it plays a vital role in ensuring anchorage and stability to prevent a plant from falling or getting blown over when subjected to mechanical loading (Ennos, 2000).
Even less studied than the typical plant, which is rooted in soil, are plants that are mechanically dependent on other plants, e.g., root climbers and epiphytes, in which attachment to the host tree poses particular challenges. This paper focuses on vascular epiphytes, which - by definition - live on other plants without parasitizing them. Epiphytes take advantage of previously unexploited sites such as tree crotches or branches in the canopy (Zotz, 2016), and strong attachment to the host is pivotal to their establishment else they risk falling to the ground where chances of survival are low (Matelson et al., 1993). Ecological research on epiphytes focused mostly on their functional ecology in tropical forests (Zotz and Hietz, 2001) as well as on their key role in the hydrological cycle, circulation of nutrient fluxes and on provision of favourable habitats for other biota (e.g., Coxson and Nadkarni, 1995; Goncalves et al., 2016; Köhler et al., 2007). The challenges of epiphytic growth due to changing atmospheric conditions are also well-studied (e.g., Bader et al., 2009; Cervantes et al., 2005; Gehrig-Downie et al., 2011; Wagner and Zotz, 2018; Zotz et al., 2010). Besides high fluctuation in moisture and temperature, life in treetops means higher exposure to wind as compared to terrestrial herbs in the forest understorey (Freiberg, 1996; Moore et al., 2018).
As mentioned above, plants growing in highly dynamic habitats exposed to potentially high flow velocities, can respond either by rapid response in terms of structural reconfiguration or a more delayed change in growth (Ennos, 1999). A typical wind profile of tropical forests has wind speeds of 0.03 m s− 1 to 3.5 m s− 1 at 2 and 60 meters above the ground, respectively (i.e., lowland forest in Northern Colombia, Baynton et al., 1965). While these numbers might seem unlikely to dislodge an individual epiphyte from its host tree, wind gusts within the canopy can be potentially stronger than that on the outer canopy, as resulted from the irregular forest edges (Moore et al., 2018). Ongoing forest fragmentation exacerbates the impact of wind disturbance due to the ever increased presence of abrupt artificial forest edges (Laurance and Curran, 2008) with wind gusts penetrating deeper into sparse forest stands compared to dense forests (Ruck et al., 2012). Hence, previously sheltered epiphytes may become more exposed to wind disturbances in the future. In addition, epiphytes’ habitats are often exposed to tropical storms during which wind speeds may reach 70 m s− 1 as recorded in Typhoon Haiyan in the Philippines in 2013 (Long et al., 2016). In a previous study, Tay et al. (2021, in production) determined drag forces on epiphytic bromeliads with longest leaf length of 9–89 cm in a wind tunnel experiment with wind speeds of up to 22 m s− 1. Drag forces at the highest wind speed were generally small (i.e., < 0.5 N in the smallest juveniles and a maximum of 9 N in one large individual) and did not cause any visible damage to the plants. Results showed that reconfiguration of the plant body effectively reduced relative drag forces on the plant as wind speeds increased, as compared to a rigid plant model. However, such a reduction does not preclude the possibility that wind induces adaptive growth over time. Although the occurrence of tropical storms is a natural phenomenon, global climate change is expected to intensify the magnitude of such storms (Holland and Bruyère, 2014; Mousavi et al., 2011), and mechanical stresses may increase in the future and exert additional challenges to epiphyte attachment to their host. However, before any evaluations can be made as to whether future changing climate has an impact on vascular epiphytes, a basic understanding of the effect of mechanical stress on the growth of epiphytes under current conditions is essential.
Therefore, as a first step in this direction, this paper aims to investigate the thigmomorphogenic responses of epiphytes to mechanically induced stress by documenting the responses of two bromeliad species subjected to various types of mechanical stress. Based on the results from previous studies with ground-rooted herbaceous plants, we wanted to test if the following responses were also displayed in bromeliads: 1) reduced growth (Goodman and Ennos, 1996); 2) increased root/shoot biomass ratio (Gartner, 1994); 3) thicker roots (Goodman and Ennos, 1998); 4) higher root biomass allocated to the leeward than the windward side of the stem (Goodman and Ennos, 1998).