New insights into the role of the root system of epiphytic bromeliads: comparison of root and leaf trichome functions in acquisition of water and nutrients

Abstract

Background

In epiphytic bromeliads, the roots were previously considered to be poorly functional organs in the processes of absorption and metabolization of water and nutrients, while the leaves were considered to always act as protagonists in both functions. More recent discoveries have been changing this old view of the root system.

Scope

In this review, we address previous ideas regarding the function performed by the roots of epiphytic bromeliads (mere holdfast structures with low physiological activity) and the importance of a reduced or lack of a root system for the emergence of epiphytism. We present indirect and direct evidence that contradicts this older hypothesis. Furthermore, the importance of the root absorptive function mainly for juvenile tankless epiphytic bromeliads and the characteristics of the root absorption process of adult epiphytic tank bromeliads are discussed thoroughly from a physiological perspective. Finally, some factors (species, substrate, environmental conditions) that influence the absorptive capability of the roots of epiphytic tank bromeliads are also be considered, highlighting the importance that the absorptive role of the roots has for the plasticity of bromeliads that live on trees, which is an environment characterized by intermittent availability of water and nutrients.

Conclusions

The roots of tank-forming epiphytic bromeliads play important roles in the absorption and metabolization of nutrients and water. The importance of roots is greatest for juvenile tankless bromeliads since the root is the main absorptive organ. In larger plants with a tank, although the leaves become the protagonists in the resource acquisition process, the roots complement the absorptive function of the leaf trichomes, resulting in improved growth of these bromeliad. The physiological and biochemical properties of the processes of absorption and distribution of resources in the tissues appear to differ between absorption by trichomes and roots.

INTRODUCTION

A striking feature of the family Bromeliaceae is that many of its species are able to live and reproduce successfully in very specific environments such as the forest canopy. The epiphytic environment is an ecologically important subsystem of the forest where nutrient and water availability are intermittent and come from peculiar external and internal sources (Zotz, 2016). Among the external sources are dry atmospheric deposition, precipitation, fog, dew, gases and direct contact with clouds (Zotz, 2016). Internal sources include leaching of mineral elements from plant tissues, plant exudates and the decomposition of organic matter accumulated in the canopy (Benzing, 2000; Zotz, 2016).

The availability of nutrients in the canopy is also intrinsically associated with the frequency of precipitation since the nutritional compounds need to be previously dissolved in water to be absorbed by bromeliads (Benzing and Renfrow, 1974). The availability of nutrients in the canopy is therefore sporadic and brief. In addition, the concentration of mineral elements diluted in rainwater is temporally variable (Zotz, 2016). In the first moments of an individual rainfall event, the concentration of nutrients in the stemflow and throughfall is relatively high due to the wash-off of dry deposition present on the surfaces of leaves, branches and trunk of the tree. As the duration of rainfall increases, the concentration of compounds diluted in rainwater decreases exponentially (Levia et al., 2011).

Based on the above, it is clear that there are several challenges that epiphytic bromeliads need to face in order to access the nutrients present in the canopy; that is, they need: (1) to capture nutritional resources from unusual sources, (2) to absorb mineral elements quickly and effectively in the short periods when resources are more available in the canopy, (3) to have a high resource-use efficiency and (4) to survive when environmental conditions become even more oligotrophic and dry (periods of low rainfall). Throughout evolution, the leaves of epiphytic bromeliads have developed several specific morphological structures and peculiar adaptive strategies that have allowed these plants to overcome all these challenges in order to achieve total independence from the soil and be able to live in the canopy (Benzing, 2000). According to Benzing (2000), the success of the epiphytism achieved by bromeliads is closely linked to two morphological features that ensure the efficient acquisition of resources in the epiphytic habitat: (1) the absorbing trichomes on the leaves and (2) the tank rosette structure.

Absorbing trichomes are special multicellular structures that cover the surface of leaves, one function of which is to increase leaf permeability to water and nutrients (Benzing and Burt, 1970). These trichomes can be basically divided into two regions: (1) the peltate part, whose structure forms a disc with dead cells that is always exposed to the atmosphere, and (2) the stalk, which consists of living cells that are embedded in the foliar epidermis (Benzing, 2000). The arrangement and density of trichomes greatly influence the ability of liquid to spread over the epidermal surface, facilitating the distribution of water over the peltate structures present on the leaf blade and increasing the effectiveness of trichomes in absorbing water and nutrients (Takahashi et al., 2022).

Depending on the lifeform and growth conditions, the absorbing trichomes of epiphytic bromeliads can differ among species in terms of size, shape, density and anatomical structure (Benzing, 2000). The most highly specialized absorbing trichomes are usually found in atmospheric bromeliads. These absorbing trichomes are bigger, have stalk cells with larger diameters, denser protoplasm and larger nuclei, and densely cover the entire blade of long and narrow leaves of atmospheric lifeforms (Benzing, 1970, 1973; Benzing and Burt, 1970; Benzing and Renfrow, 1974). These leaf structures absorb all nutrients and water required by the plants, not only from pulses of precipitation, but also from fog and dew (Reyes-Garcia et al., 2011) and even from atmospheric gases (Tamaki and Mercier, 2001). In bromeliads with an epiphytic tank lifeform, the absorbing trichomes are densest in the basal portion of the broad leaves, gradually decreasing towards the apex (Takahashi and Mercier, 2011; Rodrigues et al., 2016; Kleingesinds et al., 2018). The leaves of tank bromeliads are arranged in a rosette with overlapping leaf bases, creating a type of ‘natural cistern’. The trichomes effectively absorb the water, trapped among the leaf bases, and nutrients from (1) the decomposition of organic matter and (2) particles of atmospheric deposition that accumulate inside the tank (Benzing and Renfrow, 1974). Several species of invertebrates and vertebrates visit tank bromeliads in search of water and a place to live or reproduce. These animals provide alternative nutritional sources for the bromeliad, such as excrement and food, left by the animals inside the tank (Romero et al., 2008, 2010; Leroy et al., 2013; Gonçalves et al., 2016).

Due to the presence of these special features of the shoot, the leaves of epiphytic bromeliads have always been regarded as protagonists in the processes of absorption of water and nutrients and metabolization of many inorganic and organic compounds. In the leaves of these bromeliads, resources can be transported into cells by the actions of high- and low-affinity membrane transport proteins (Winkler and Zotz, 2009; Gonçalves et al., 2020), and the transport of some nutrients such as urea and ammonium can also be facilitated by aquaporins (Ohrui et al., 2007; Matiz et al., 2019). In the metabolization of nitrogen (N) compounds, different regions of the leaf can play very specific roles. In Vriesea gigantea Gaudichaud, the leaf base is the main region where the first steps of N uptake and metabolism occur (e.g. nitrate reduction, urea hydrolysis), while the apex is mainly associated with the steps in which N is effectively incorporated into amino acids (Takahashi and Mercier, 2011; Mercier et al., 2019).

The latest discoveries have shown that the roots, previously considered as an organ with low absorptive capability, also have an important role in the nutrition of epiphytic tank bromeliads. The objectives of this review are (1) to describe how the roots of epiphytic tank bromeliads were seen in the past by the scientific community, (2) to show how this view has changed recently, (3) to describe some physiological aspects behind the process of root absorption of epiphytic tank bromeliads and (4) to discuss how some factors (species, substrate, environmental conditions) influence the absorptive capability of the roots of these bromeliads.

THE OLD VIEW OF ROOTS OF EPIPHYTIC TANK BROMELIADS: HOLDFAST STRUCTURES WITHOUT ABSORPTIVE FUNCTION

For decades, the prevailing view of the scientific community studying epiphytic vascular plants was that the roots of epiphytic tank bromeliads had low functionality in the process of resource absorption. According to older literature (Benzing and Renfrow, 1974), the root system was responsible mainly for keeping the epiphytic plant firmly anchored in the branches or trunks of trees, while leaves assumed the role of resource uptake to support the metabolism of the entire plant body. The contrast between shoot and root parts in the body of epiphytic bromeliads can easily be seen in their morphology: the leaves are often exuberant and plentiful, comprising the major part of the vegetative body, while the roots are often lignified, not very abundant (i.e. low total number of developed roots) and scarcely branched (Benzing, 2000).

In tank-forming epiphytic bromeliads, the marked morphological and functional differences between the shoot and root parts and the great importance of the leaves for nutrient and water uptake aroused the curiosity of scientists. Pittendrigh (1948) suggested a theory that attempted to explain evolutionarily the means by which the leaves became the main absorption organs to the detriment of the uptake capability of the roots, and the relationship between the development of tank nutrition and the emergence of epiphytism. According to Pittendrigh (1948), the bromeliad prototype was a terrestrial form with a well-developed root system and adapted to survive in arid environments. Throughout evolution, the bases of the leaves were progressively modified, becoming able to capture water and debris from atmospheric deposition. The leaf bases subsequently became more inflated and able to accumulate some resources, such as water and organic debris, creating the tank. As the leaves played an increasingly important role in absorbing resources, bromeliads became more independent of the soil, leading to the emergence of epiphytism. In this context, foliar absorption prevailed compared with root absorption, and perhaps, as a consequence, the root system progressively became reduced in its capability to take up resources and started to perform, as its main function, fixation of the bromeliad on the host tree.

For some researchers, the reduced root system was considered an important adaptation for bromeliads living in the canopy (Benzing, 1973; Benzing and Ott, 1981). The drastic reduction of the root system might provide a decrease in water loss through transpiration by epiphytic bromeliads due to the resulting low surface to volume ratio. This feature might increase the ability of bromeliads to tolerate the driest conditions found in some areas of the canopy (Benzing, 1973). Moreover, Benzing and Ott (1981) inferred that the reduction of the root system might lead to an economy in the use of nutrients, water and energy for epiphytic bromeliads. In evolutionary terms, the maintenance of an uptake organ (root) whose functions are relatively ‘obsolete’ may not be advantageous to an epiphytic bromeliad that has a tank with leaf bases densely covered by absorbing trichomes since such plants would have to expend more energy and resources to keep its root system physiologically active for the uptake function throughout the entire lifespan. Those epiphytic tank bromeliads that managed to ‘eliminate’ their active roots and intensify the capabilities for absorption and assimilation of nutrients and water in their leaf bases may have had greater advantages to ensure their survival in the oligotrophic environment. Although these hypotheses have been well accepted by many scientists, Zotz (2016) cautioned that these inferences are still open questions requiring further investigation because how relevant this ‘resource economy’ would be for the survival of epiphytic bromeliads remains unknown.

Currently, the accumulated knowledge on the leaves of epiphytic bromeliads has very different viewpoints, for example from anatomical, morphological, physiological, ecological, taxonomic and molecular perspectives (Lüttge, 1989; Benzing, 1990, 2000, 2012; Zotz, 2016). On the other hand, due to the general consensus that roots are restricted to being mere holdfast structures, study of the root system of epiphytic tank bromeliads has been relatively neglected. Studies that have investigated the absorptive capability of the roots of these bromeliads are rare.

STUDIES SUGGESTING THE PHYSIOLOGICAL INACTIVITY OF BROMELIAD ROOTS

One of the first studies that investigated the absorptive capability of the root system of tank-forming epiphytic bromeliads used specimens of Guzmania lingulata (L.) Mez cultivated in a glasshouse (Nadkarni and Primack, 1989). Although the bases of the leaves were able to absorb gamma-emitting radionuclides such as Se-75, Cs-137, Mn-54 and Zn-65 effectively, a similar performance was not seen for the roots. These elements are not incorporated by the leaf tissues or the inflorescence after adding the diluted radionuclide to the soil substrate, indicating that uptake of these elements may not have occurred through the root system. The hypothesis that the elements are taken up but not mobilized to the shoot part is considered unlikely because in only one plant was slight incorporation of radionuclide elements in the shoot part tissues detected. According to Nadkarni and Primack (1989), the root system of only one bromeliad is still capable of absorbing resources to some degree, while in the other bromeliads studied, roots were not able to absorb radionuclides due to either a possible non-absorptive functionality, the radionuclides were adsorbed on the soil surface and did not reach the roots, or the radionuclides were immobilized by the soil microflora.

The roots of Aechmea fasciata ‘Primera’, an epiphytic tank bromeliad, have virtually no capability to capture inorganic phosphate (Pi) (Winkler and Zotz, 2009). When the root system of this bromeliad comes into contact with a solution containing ³²P, phosphorus can be adsorbed to the surface of the roots; however, nothing is effectively absorbed by this organ since no ³²P was detected in the root tissues after a thorough rinse of its surface. The root tissues incorporate a small amount of Pi only through redistribution of the ³²P absorbed effectively by the leaves (Winkler and Zotz, 2009). The Pi captured by the leaf base is translocated mainly to younger and mature leaves while the oldest leaves and roots receive the smallest amounts.

These studies on the functionality of the roots of epiphytic tank bromeliads confirmed the hypothesis that the root system had little relevance in the process of resource uptake (Nadkarni and Primack, 1989; Winkler and Zotz, 2009). However, other studies have also emerged, providing the first indirect evidence that the root system of epiphytic tank bromeliads may be physiologically active to absorb resources.

STUDIES SUGGESTING THE FUNCTIONALITY OF ROOTS IN THE PROCESS OF RESOURCE UPTAKE

In the root system of epiphytic bromeliads Aechmea sp. and Tillandsia bulbosa Hook., located in the LaSelva Biological Reserve on the Atlantic Coastal Plain of Costa Rica, enzymatic activity of acid phosphatases present on the surface of the roots was detected, suggesting that this organ can absorb Pi (Antibus and Lesica, 1990). Terrestrial plants usually have access to Pi through the action of root surface acid phosphatase enzymes that hydrolyse organic phosphorus compounds commonly found in the soil (Kroehler and Linkins, 1988). Antibus and Lesica (1990) reported that regions of the canopy where the tree branches are covered by organic debris and a rich mass of plants have a greater availability of organic phosphorus than sites with bare branches. Thus, the presence of acid phosphatases on the surface of the roots of epiphytic bromeliads might help these plants to access the rare reservoirs of Pi in the epiphytic environment. In fact, it has been shown that epiphytic plants living in canopy regions covered with organic debris tend to have a higher acid phosphatase activity on the surface of their roots and higher endogenous Pi content in the shoot tissues than epiphytic plants anchored on bare bark (Antibus and Lesica, 1990).

Although the study described above suggests that the roots of Aechmea sp. and T. bulbosa might have the ability to take up Pi, it has not been experimentally proven whether these roots are physiologically active with regard to nutrient uptake. Therefore, the hypothesis that the roots of epiphytic tank bromeliads are mere holdfast structures has prevailed for some decades in the literature. Only more recently has a new study presented further indirect evidence regarding the possible absorptive functionality of the roots of epiphytic tank bromeliads.

Petit et al. (2014) verified that young plants of the epiphytic tank bromeliad Aechmea mertensii Schult.f. seem to be able to capture nutrients through their roots. Aechmea mertensii usually grows in association with species of arboreal ants. When the roots of juvenile plants establish on the young, small nests of these ants, the root system becomes part of the nest architecture as the plant grows. The authors found that the natural abundance of ¹⁵N in young and adult bromeliads of A. mertensii are similar to each other, a very different result from that seen for epiphytic bromeliads that do not grow in association with ants. The plant tissue of adult bromeliads generally has a greater enrichment of ¹⁵N than that found in juvenile plants (Hietz and Wanek, 2003; Reich et al., 2003; Zotz et al., 2004). The isotopic labelling of ¹⁵N in the tissues of epiphytic bromeliads depends on which natural source the nitrogenous resources originate from before these nutrients are absorbed by the bromeliads, i.e. from atmospheric deposition (resulting in a lower ¹⁵N enrichment in plant tissues) or from the degradation of organic debris (resulting in a greater enrichment of ¹⁵N in tissues) (Reich et al., 2003). The discovery that the tissues of young plants of A. mertensii have the same ¹⁵N isotope labelling present in the tissues of adult bromeliads is indirect evidence that the juvenile root system may be able to absorb N from the degradation of organic compounds (e.g. stored food by ants, ant excrement, gathering plant debris) present in the structure of the nest (Petit et al., 2014).

The study by Petit et al. (2014) raised an important hypothesis that, in the early stages of development, tank-forming epiphytic bromeliads may have the ability to absorb resources through their roots. Interestingly, although Winkler and Zotz (2009) demonstrated that the root system of A. fasciata (adult stage) does not perform the ³²P absorption function, they do not rule out the possibility that the root system of epiphytic bromeliads is able to absorb other nutritional resources. According to these authors, in epiphytic tank bromeliads, the ability of the roots to absorb resources may be intrinsically related to very specific conditions, such as the ontogenetic stage in which the plant is passing through and the environmental conditions in which the epiphytic tank bromeliad lives.

THE INFLUENCE OF GROWTH STAGE ON THE ABSORPTIVE CAPABILITY OF ROOTS OF EPIPHYTIC BROMELIADS

Some bromeliads capable of developing a tank are initially tankless and have a morphology very similar to that found in atmospheric bromeliads. In these species, the tank only develops in later phases of growth (Benzing and Burt, 1970). Due to the inability to accumulate water and debris via the leaves and the reduced root system, some studies have suggested that young tank-forming epiphytic bromeliads take up nutrients and water mainly through leaf trichomes such as the atmospheric forms (Benzing et al., 1976; Adams and Martin, 1986; Zotz et al., 2004; Meisner et al., 2013). In juvenile tankless plants of V. gigantea (tank-forming epiphytic bromeliad in the adult phase) cultivated in a greenhouse (Fig. 1), the trichomes play an important role in the absorption of nitrate and urea, but the root system has also been shown to be very active in the uptake process of these N forms (Takahashi et al., 2022), even though the root system is little branched and composed of few short roots (Fig. 1).

Fig. 1.

Plants of the epiphytic bromeliad Vriesea gigantea in two different stages of development. (A) Juvenile atmospheric bromeliad and (B) detail of its root system. (C) Adult tank bromeliad and (D) detail of its lignified roots.

When young V. gigantea plants are restrictedly fertilized on the roots, nitrate and urea are rapidly absorbed (within 24 h) by the root system. Inside the root cells, N sources are effectively metabolized by the enzyme nitrate reductase (NR) that reduces nitrate, and urease that hydrolyses urea (Takahashi et al., 2022), indicating that roots also play an important role in the first biochemical steps of N metabolism. Compared with leaves, roots of young bromeliads are the main organs where nitrate reduction and urea hydrolysis occur, demonstrating the great importance of the root system for V. gigantea during the juvenile phase.

In adult V. gigantea plants with a large tank (Fig. 1), the roots lose their predominant role in nitrate and urea uptake and the leaf bases become the main organs for uptake and metabolization of nitrate and urea (Takahashi et al., 2022). These results reinforce the hypothesis that V. gigantea may be able to access greater amounts of nutrients through the tank, which could perhaps be stimulating all the physiological changes observed in the leaves and roots (Takahashi et al., 2022). This shift in functions between leaves and roots of smaller and larger V. gigantea in the process of resource uptake is probably a physiological change related primarily to plant size (Meisner et al., 2013) that occurs gradually over the growth stages, as has already been seen for the cultivars Vriesea ‘Splenriet’ and Vriesea ‘Galaxia’ (Vanhoutte et al., 2017).

When the V. ‘Splenriet’ and V. ‘Galaxia’ cultivars (epiphytic bromeliads grown in a greenhouse) have a small tank, the absorptive capability of the roots is greater than that of the root system of bromeliads with a larger tank formed (Vanhoutte et al., 2017). The authors showed that the uptake of water and nutrients by the roots gradually decrease along the different growth stages of these two cultivars [growth stages: (1) juvenile with small-volume tank → (2) older with large-volume tank → (3) older with large-volume tank and inflorescence], while the uptake of these same resources through leaf trichomes gradually increases throughout the growth phases.

The importance of the absorptive function of the roots for both young Vriesea cultivars may be related to their low capability to accumulate resources among the leaves due to the small volume of their tanks (Vanhoutte et al., 2017). The roots of juvenile bromeliads may help maximize total water and nutrient uptake capability when working together with the leaf trichomes. In addition, during the first stages of development, V. ‘Splenriet’ and V. ‘Galaxia’ have high total nutrient and water uptake that can become even greater than those of mature plants. In our view, this result reinforces the idea of the importance that roots have for these young Vriesea cultivars, since the great capability to capture resources might be an essential characteristic for these plants to be able to achieve a high growth rate.

The joint uptake process (leaf trichomes + root system) of nutritional and water resources is perhaps not an exclusive feature of these juvenile Vriesea cultivars. Young seedlings of some species of Tillandsiodeae have greater survival success when they grow in tree regions where the branches have rougher bark and are covered by organic debris and densely colonized by bryophytes than branches with smoother bark and fewer bryophytes (Winkler et al., 2005; Hietz et al., 2012). This organic mantle (debris, moss, etc.) that covers the branches has the ability to retain water and mineral elements from rainfall, steamflow and throughfall (Hietz et al., 2012). Tillandsiodeae seedlings without tanks can perhaps take advantage of these natural sources of nutrients and water through root absorption, since their roots are in direct contact with this organic mantle.

The studies described above have shown that the roots of juvenile tank-forming epiphytic bromeliads seem to have an even greater importance than leaf trichomes in resource uptake. However, in the adult stage, do the roots of most specimens of this type of bromeliad really almost completely lose their absorptive functions, as seen for G. lingulata (Nadkarni and Primack, 1989), A. fasciata (Winkler and Zotz, 2009) and V. gigantea (Takahashi et al., 2022)? In recent years, several studies have shown that even in adulthood the root system of some species of tank-forming epiphytic bromeliads remains physiologically active with an absorptive function (Vanhoutte et al., 2016, 2017; Da Silva et al., 2018; Leroy et al., 2019, 2022; Gomes et al., 2021), although the roots are no longer the protagonists in the process of water and nutrient uptake as seen in the juvenile phase (Vanhoutte et al., 2017). In the following, we discuss some physiological aspects of the absorption carried out by the root system of epiphytic tank bromeliads at the adult stage and compare this with the absorption performed by leaf trichomes.

PHYSIOLOGICAL ASPECTS OF ROOT ABSORPTION IN ADULT EPIPHYTIC TANK BROMELIADS

Leaf trichomes and roots have independent absorption mechanisms, both capable of absorbing enough water and nutrients to promote plant growth

The uptake of resources by leaf trichomes and roots of epiphytic tank bromeliads seem to be two independent processes with little interference between them. Vanhoutte et al. (2017) verified that the absorptive capability of leaf trichomes of adult Vriesea cultivars (‘Splenriet’ and ‘Galaxia’) grown in a greenhouse can increase as the availability of nutrients becomes greater inside the tank. They observed that the significant increase in uptake rate through foliar trichomes does not influence the absorption capability of the root system, suggesting that there is no immediate feedback between these two uptake mechanisms.

Furthermore, the root systems of some epiphytic tank bromeliads in the adult stage seem to be able to absorb enough nutrients to promote the growth and development of plants. In A. fasciata, after fertilization applied exclusively to the roots or strictly to the tank, the root system and the leaf trichomes are able to absorb inorganic N compounds effectively, resulting in an increase in the leaf N concentration and in the number of new leaves (Gomes et al., 2021). The root system of A. fasciata also absorbs N from urea when this organic N compound is applied to the substrate, which led to an increase in the total dry mass of the plant (Gomes et al., 2021). In addition, Young et al. (2022) showed that some biometric parameters such as bromeliad height, stem diameter, number of leaves, and fresh and dry mass of leaves and roots increase proportionally with an increase in concentration of nutrients offered to the roots of A. fasciata. When adult plants of Aechmea aquilega, a tank-forming epiphytic bromeliad, were cultivated in a greenhouse, with only the roots watered, the root system is able to absorb sufficient amounts of water and nutrients to maintain its rate of growth very similar to that of plants which receive water in both leaves and roots (Leroy et al., 2019).

The biochemical properties and the distribution process of the absorbed nutrients differ between the foliar and root absorption mechanisms

The sensitivity to different types of mineral elements may differ between leaf trichomes and roots, as seen in Nidularium minutum Mez (Carvalho et al., 2017). Although N. minutum is a tank-type bromeliad with a terrestrial habit, the absorbing trichomes present at the base of the leaves have an absorptive capability that is as effective as that of the root system. According to Carvalho et al. (2017), N. minutum has a higher endogenous leaf N concentration when it is fertilized exclusively via the roots than exclusively via the tank, showing that the root system of this bromeliad is far more effective in absorbing inorganic N compounds than leaf absorbing trichomes. By contrast, calcium seems to be more effectively absorbed by leaf trichomes than by roots since a greater accumulation of calcium in leaf tissues is detected when N. minutum is exclusively fertilized via the tank. In the case of potassium, both leaf trichomes and roots are similarly effective in absorbing this mineral element (Carvalho et al., 2017). The distinct sensitivities to different types of mineral elements show that the absorption mechanisms present in leaf trichomes and roots of this bromeliad may be being performed by distinct membrane transport proteins and/or regulated by different biochemical properties. These differences between the leaf absorbing trichome and root system may not be an exclusive characteristic of N. minutum, but also present in epiphytic tank bromeliads whose roots have been shown to be physiologically active in the process of resource absorption. According to Leroy et al. (2019), the functioning and regulation of membrane transport proteins related to the transport of various mineral elements and compounds such as water, and organic molecules still need to be elucidated in epiphytic tank bromeliads if we want to understand the true role of the roots of these plants in the processes of nutrient and water uptake.

Absorption by leaves or roots can also interfere with the way in which the mineral elements will be used by the epiphytic tank bromeliad, as reported for G. lingulata and Vriesea ‘Harmony’. Both of these epiphytic tank bromeliads are commercial plants with the ability to capture N through leaf absorbing trichomes and the root system (Da Silva et al., 2018). According to these authors, newly absorbed N can have different metabolic fates depending on which physiological mechanism is used for absorption. The conversion of N to increase biomass is far more effective in both bromeliads when this mineral element is absorbed through the root system than through the leaves. On the other hand, a large part of the N absorbed through the leaf trichomes seems to be destined for the synthesis of reserve compounds (e.g. some types of amino acids) which will first be stored in the tissues and later used gradually over several days. The absorption through leaf trichomes has very conserved physiological traits that remain present in commercial cultivars (Da Silva et al., 2018). Where the availability of nutrients is intermittent such as the epiphytic environment, the absorption of resources carried out by the leaf trichomes of tank bromeliads occurs according to a concept called ‘luxury consumption’, i.e. the leaves are able to capture resources in amounts much higher than are necessary for the nutritional needs of the plant in the short term (Snaydon and Bradshaw, 1962; Jeffrey, 1964; Rorison, 1969; Chapin, 1980). The excess of absorbed nutrients is stored in tissues and gradually consumed, allowing continuous, slow growth of the plant even during periods of nutrient scarcity (Winkler and Zotz, 2009).

Leaf and root absorption mechanisms interfere differently in the process of water distribution in leaf tissues

The effectiveness of distribution of the newly absorbed water in tissues is also influenced by the uptake mechanisms, as seen for the tank-forming bromeliad Guzmania ‘Rana’ (a commercial cultivar) whose leaf trichomes and root system are both capable of absorbing water (Vanhoutted et al., 2016). When G. ‘Rana’ grows under conditions where the tank remains without water and only the roots are abundantly watered, these plants undergo anomalous leaf development. Instead of the leaf bases of the bromeliad partially overlapping with each other, forming the typical structure of the open tank, the cistern has a vertical, twisted structure, whose morphological appearance is similar to a narrow tube (Vanhoutte et al., 2016) (Fig. 2).

Fig. 2.

Different tank morphologies of Vriesea carinata in the adult stage. (A) Typical structure of an open tank that allows water and organic debris to accumulate among the leaves. (B) Anomalous tank forming a tube-like structure (i.e. the cistern) which has a vertical, twisted morphology, whose appearance is similar to a narrow tube. (C) Top view of the normal tank, highlighting its large diameter. (D) Tank structure completely compressed in a bromeliad, resulting in a drastic reduction of its water-impounding capability.

According to Vanhoutte et al. (2016), this phenomenon occurs due to a physiological condition that leads to inadequate water distribution in the leaves when the water originates from root uptake. When water is absorbed by leaf trichomes, it spreads and distributes quickly throughout all leaf tissues, being transported later to all parts of plant body through mechanisms involving the vascular system and aquaporins; these mechanisms are not yet completely understood (Ohrui et al., 2007; North et al., 2013) (Fig. 3A). On the other hand, when water is taken up by the root system, it is transported to the leaves through the xylem vessels, as in terrestrial plants. Upon reaching the leaves, the water is subject to high radial resistance to move and distribute to the various cell layers that form the leaf tissues (North et al., 2013). The leaf tissues closest to the vascular bundles, such as the aerenchyma, chlorenchyma and abaxial hydrenchyma, are kept well hydrated, as the water from root absorption can reach these tissues. However, the adaxial hydrenchyma that forms the thickest tissue layer throughout the major part of leaf blade does not receive enough water to maintain hydration (Fig. 3B). The intense dehydration that occurs only in the adaxial hydrenchyma causes ‘rolling’ of the leaves inwards along their own axis, resulting in the anomalous formation of the ‘tubing’. The ‘tubing phenomenon’ is not a response to drought stress because when cultivars of G. ‘Rana’ were not watered via either their tank or roots, they did not develop this leaf anomaly (Vanhoutte et al., 2016).

Fig. 3.

Water distribution hypotheses in the leaf tissues of tank-forming epiphytic bromeliads. (A) Water absorption exclusively through leaf trichomes. The trichomes allow fast and efficient absorption of water via the surface of the leaves. Once the water reaches the interior of the leaf tissues, it quickly spreads and is distributed through all the cell layers, homogeneously hydrating the entire leaf. (B) Absorption of water strictly through the root system. The water absorbed by the roots is rapidly transported to the shoot part through the xylem vessels. After reaching the leaf vascular bundle, water is not easily distributed in the leaf tissue due to a strong radial hydraulic resistance generated by the lignified and suberized cell walls of the bundle sheath cells that surround the entire region of the conducting vessels. The cell layers closest to the vessels are able to remain well hydrated, but the adaxial hydrenchyma cannot receive enough water to maintain the integrity of its tissue. As a consequence of this partial dehydration, the thickness of the adaxial hydrenchyma is reduced, which may lead to the development of a leaf anomaly called the ‘tubing phenomenon’.

The problem of ‘tubing’ is commonly seen in bromeliad cultivars belonging to the genera Guzmania and Vriesea (Vanhoutte et al., 2016). However, A. aquilega shows certain physiological disturbances that may be related to an imbalance in the distribution of water in the tissues when this bromeliad is exclusively watered via roots. Although the growth and development of A. aquilega occur at normal rates when only its root system receives water and nutrients, stomatal conductance, photosynthetic assimilation rate and leaf starch content are significantly lower than in plants whose tanks are filled with fresh rainwater and nutrients (Leroy et al., 2019). Interestingly, when A. aquilega receives water exclusively via the roots, only the thickness of the adaxial hydrenchyma of the leaf blade becomes smaller than that measured in plants that receive water inside the tank (Leroy et al., 2019), indicating that the exclusive irrigation of water to the root system results in a certain degree of dehydration only of the leaf adaxial hydrenchyma.

Synergistic effect of root and foliar absorption in adult epiphytic tank bromeliads

In the adult stage, the root absorption ability of epiphytic tank bromeliads also effectively complements the process of resource uptake that is carried out by leaf trichomes as similarly seen in juvenile bromeliads. In A. aquilega, when both absorption organs (leaf and root) receive inorganic N compounds, total N uptake is maximized since the leaf trichomes and the root system start to work together in the absorption process, resulting in higher leaf N concentration and greater ¹⁵N isotopic abundance in the tissues of this bromeliad (Leroy et al., 2019). In G. ‘Rana’, the total capability for uptake of water and nutrients (leaf trichomes + roots) increases significantly, providing a considerable increase in the growth and development rates of this bromeliad (Vanhoutte et al., 2016). Da Silva et al. (2018) described that, working together with the absorbing trichomes, the active root systems of G. lingulata and V. ‘Harmony’ contribute positively to bromeliad nutrition, mainly in terms of increasing plant biomass.

CONTRADICTORY RESULTS: CAN ROOTS OF BROMELIADS WITHOUT ABSORPTION CAPABILITY BECOME COMPETENT TO UPTAKE RESOURCES?

At first glance, the results regarding resource uptake capability through roots of large epiphytic tank bromeliads may seem contradictory since studies have shown the non-absorptive functionality of the roots (Nadkarni and Primack, 1989; Winkler and Zotz, 2009; Takahashi et al., 2022) while others verified that the root system is capable of water and nutrient uptake (Vanhoutte et al., 2016, 2017; Da Silva et al., 2018; Leroy et al., 2019; Gomes et al., 2021). From our perspective, all these results are valid as there appear to be no methodological flaws in these studies. Furthermore, it seems plausible that there are variations in results among the studied bromeliads. Depending on the species, there may be adult epiphytic bromeliads whose roots act most of the time only as a holdfast structure and poorly absorb water and mineral resources. However, this does not mean that the root system of these bromeliads cannot become active at specific times through the development of new roots.

Another interesting fact observed in the studies carried out thus far is that several epiphytic tank bromeliads that have been shown to have a functional root system are cultivars adapted to grow on commercial substrate and cultivated under conditions that optimized their growth and development. In other words, the ‘luxury’ growing conditions of the greenhouses may have positively influenced these bromeliads to maintain their functional root system even into the adult stage.

In the epiphytic environment, growth conditions are different from those found in the greenhouses. In this oligotrophic environment where the availability of water and nutrients is intermittent and associated with periods of precipitation, the existence of the tank and absorbing trichomes are essential characteristics for many epiphytic bromeliads to ensure growth, development and reproduction (Benzing and Renfrow, 1974). Given the importance of foliar absorption and how conserved this characteristic is to epiphytic tank bromeliads, in our view very specific physiological and environmental conditions may be necessary for these plants to invest energy and metabolic resources in order to keep their root system active for the absorption function or to regain the absorptive capability of their roots. No studies have yet discussed which factors stimulate the development of new roots in epiphytic tank bromeliads and which factors influence these plants to keep their root system active to uptake resources. There is only limited evidence to suggest some possible positive relationships between certain factors (species or environmental) and the absorptive functionality of roots of epiphytic tank bromeliads. All the factors known so far will be discussed in the following sections.

Effect of species on root and foliar absorption capability

The ability to absorb nutrients and water through leaf trichomes and root system can vary among epiphytic bromeliad species due to morphological characteristics and genetic predisposition. Leroy et al. (2019) observed that uptake capability through the root system varies between adult plants of A. aquilega and Lutheria splendens (epiphytic tank bromeliads). While the roots of A. aquilega are as effective as foliar trichomes in absorbing water and nutrients, the root system of L. splendens captures water in very low amounts, and this amount was not sufficient to avoid the appearance of typical morphological and physiological characteristics in response to water stress. In the case of inorganic N compounds, the root system of L. splendens shows low effectiveness in absorbing N and contributes virtually nothing to increase the leaf total N concentration (Leroy et al., 2019). They concluded that L. splendens depends almost exclusively on the absorptive capability of leaf trichomes which, unlike the roots, perform effective and fast absorption of water and N.

The cultivar V. ‘Galaxia’ has a higher absorptive capability through leaf trichomes than V. ‘Splenriet’, while V. ‘Splenriet’ shows far more effective root absorption than V. ‘Galaxia’. Vriesea ‘Galaxia’ has characteristics that can provide a more effective foliar absorption system; for example, the base of the leaf surface presents a greater density of absorbing trichomes and the leaves have a proportionally greater area in contact with the tank solution (Vanhoutte et al., 2017). Vriesea ‘Galaxia’ displays a phenotype similar to epiphytic Vriesea species such as Vriesea duvaliana that have an effective mechanism of resource uptake through leaf trichomes (Vanhoutte et al., 2017). A previous study showed that V. duvaliana has higher uptake rates for some mineral elements such as potassium when compared to V. ‘Splenriet’ (Winkler and Zotz, 2009). On the other hand, according to Vanhoutte et al. (2017), it is not surprising that V. ‘Splenriet’ shows better root absorption than V. ‘Galaxia’, as the wild bromeliad species related to this cultivar (i.e. Vriesea splendens) is usually found living in the understorey of tropical rainforests with terrestrial or epiphytic habits. In other words, these two cultivars have a distinct genetic predisposition in terms of resource absorption due to the differences between the wild parent bromeliad species that produced these cultivars.

Effect of substrate on root absorption capability

The existence of epiphytic bromeliad cultivars (e.g. V. ‘Splenriet’, V. ‘Galaxia’) with great capability to capture nutritional and water resources through the roots may be a consequence of the pre-selection process carried out by breeders when they select the best adapted plants for growth in horticultural substrate (Vanhoutte et al., 2017). Due to cultivation in commercial substrate, bromeliad cultivars can develop a more branched root system than a plant grown in the canopy. We believe that the cultivation conditions and the type of substrate used to cultivate Vriesea species can also influence the abundance and frequency at which the roots develop and, consequently, influence the absorptive capability of the root system. Vriesea ‘Splenriet’ and V. ‘Galaxia’ were planted in horticultural stone wool blocks kept partially submerged in nutrient solution (Vanhoutte et al., 2017). In our view, these conditions appear to be quite favourable for these bromeliads to invest metabolite resources and energy in the development of new roots and keep their root systems physiologically active for absorption. This explains why Vanhoutte et al. (2017) found roots with absorptive capability even in adult bromeliads. Some recent studies have shown that substrate fertilization [e.g. addition of potting rich soil (Rapnouil et al., 2022) or nutrient solution with macro- and micronutrients (Young et al., 2022)] stimulates the development of the root system of A. aquilega (Rapnouil et al., 2022) and A. fasciata (Young et al., 2022), adult epiphytic tank bromeliads pre-adapted to cultivation in substrate and under greenhouse conditions. With a greater number of roots and a more branched root system, these bromeliads are able to increase their ability to capture nutrients present in fertilized substrates, resulting in far more vigorous development of their shoot parts.

When planting V. gigantea, an epiphytic tank bromeliad that is often cultivated in greenhouses, we usually use a mixed substrate (commercial organic substrate + pine bark). This mixed substrate does not remain constantly moist as seen for stone wool blocks, especially on hotter days. The water accumulated in the tank appears to be the main nutritional and water source for this plant. Although V. gigantea is able to develop its roots when planted in this mixed substrate (Fig. 1), we have rarely been able to find developing new roots whenever the pot is removed from adult plants. Generally, when we remove the pot from these adult bromeliads, the root system is extremely lignified and hardened (Fig. 1) and is practically no longer able to function in absorbing resources as N compounds (Takahashi et al., 2022). A recent study showed that the development of new roots in A. aquilega is greatly influenced by the type of substrate in which it is cultivated. Nutrient-poor substrates such as sand result in the development of a low number of new roots in A. aquilega (Rapnouil et al., 2022).

Epiphytic bromeliads cultivated in greenhouses under controlled conditions usually show great plasticity in adapting to the most diverse growing conditions (Schmidt and Zotz, 2002; Rapnouil et al., 2022). We believe that depending on the conditions under which these bromeliads grow in a natural environment or under controlled conditions (greenhouse), new roots may develop and remain active to capture additional water and nutrients beyond that absorbed by leaf trichomes, allowing bromeliads to significantly increase their growth rate. We believe that a phenomenon observed in V. gigantea, described in the next section, can provide some clues in this regard.

Effect of the environmental on root absorption capability: the development of new roots in V. gigantea

After a short acclimatization period (1 week) carried out inside climatized chambers, we witnessed an unusual phenomenon in V. gigantea bromeliads at the adult stage when the plants were grown in mixed substrate, which we routinely use in our experiments. Some bromeliads from the acclimatized group, corresponding to about 40 % of the total number of plants, showed increased development of many roots (Fig. 4A). Unlike the morphology of the old roots, the new roots were white, thick, virtually non-lignified, with tender tissues and very susceptible to mechanical injury. Root development occurred tangentially to the base of the leaves and radially throughout the base of the tank. The massive growth of new roots in V. gigantea is a rare phenomenon and is uncommon during the acclimatization procedure. In the climatized chambers, the plants only received tap water inside the tank daily. We have been working with this large tank bromeliad for at least a decade both under controlled environmental conditions (growth chambers) and in a greenhouse with variable environmental conditions; this was the first time that we witnessed this phenomenon. Furthermore, another interesting observation was that the new roots maintained their vigorous appearance for a few days (1 week or less), and their morphology soon began to change, the tissues lignifying and becoming stiff and dark, resembling the old roots (Fig. 4B).

Fig. 4.

Root system of the epiphytic tank bromeliad Vriesea gigantea. (A) Exacerbated growth and development of many roots tangentially at the base of the leaves in a short period of time (1 week). (B) After a few days (~1 week or less), the morphology of the new roots starts to quickly change: the root tissues lignified and became dark and stiff (red arrow).

In V. gigantea plants that developed new roots (Fig. 4), it was also possible to quantify the activities of some enzymes of N metabolism. Evaluation of the enzymatic activities of NR and glutamine synthetase (GS) in plant tissues after fertilization with nitrate or urea is considered a good method to investigate the uptake capability of these two N sources by plants since the activities of these enzymes are usually stimulated in the presence of their substrate. According to our results, the white roots showed the ability to capture the nitrate offered by fertilization in the soil, resulting in a significant increase in NR activity. These new roots were also able to take up urea and hydrolyse this compound (NH₄⁺ + CO₂). The ammonium generated was efficiently assimilated into amino acids through an expressive action of the GS enzyme.

Therefore, V. gigantea has the ability to invest metabolic resources and energy for the massive development of roots capable of absorbing and metabolizing nutritional sources, such as nitrate and urea. We believe that this phenomenon may be a response to very specific environmental conditions, such as high relative humidity. During acclimatization of these plants, only one parameter differed from what is usually used in climatized chambers: relative humidity was in the range 80–90 % (usual in the chambers before increasing the relative humidity: 40–50 %).

The shoot part of terrestrial plants is usually able to perceive the variation in relative humidity through sensing mechanism(s), signalling the root part about these changes in the environment. In this way, the root system may undergo morphological, physiological and molecular changes, preparing for the expected forthcoming dry or wet conditions (Levin et al., 2009). Shoot-to-root communication can be carried out through changes in the transcriptional expression of several genes, for example genes associated with phytohormone signalling pathways (Levin et al., 2009). In rice seedlings grown hydroponically, the shoot acts as a sensing organ for environmental humidity, while the roots act as a responding organ to this stimulus (Chhun et al., 2007). The high relative humidity (100 %) stimulates enhanced translocation of auxin, which is a phytohormone that plays a pivotal role in plant growth and development (e.g. root branching), via phloem from the shoot to the basal region of root tissues in rice, resulting in a large increase in the density of lateral roots (Chhun et al., 2007). Ethylene is another phytohormone that is responsive to changes in relative humidity. According to Azuma et al. (2007), ethylene suppressed or promoted shoot growth of rice seedlings when they were grown under low relative humidity (30 %) or high relative humidity (100 %), respectively. Although the joint effects of ethylene and relative humidity on the roots of vascular plants are still unknown, ethylene is known to regulate root growth through auxin. Ethylene stimulates auxin biosynthesis, induces basipetal auxin transport and modulates the transcription of various components of the auxin transport machinery (Ruzicka et al., 2007).

High relative humidity can indicate the occurrence of rains in the natural environment (Mawonike and Mandonga, 2017; Yu et al., 2023). The shoot part of V. gigantea may be able to perceive this stimulus, causing the massive development of new roots as a response. Root development in response to high relative humidity has already been observed in other plants. The exposure of rice plants to high relative humidity (90 %) during the light period resulted in an increase in both the number of roots and total root length (Hirai et al., 2000). In sweet potato, the number, and fresh and dry mass of storage roots increased under high relative humidity (85 %) (Mortley et al., 1994). In soybean, high relative humidity (90 %) allowed the development of more vigorous plants even in iron-deficient growing conditions, resulting, for example, in the development of longer roots (Roriz et al., 2014). In the case of V. gigantea that developed a large number of new roots in response possibly to high relative humidity, resource capture could be greatly optimized (synergistic effect of the combination of foliar and root absorption) exactly when the availability of water and nutrients is usually greatest in the natural environment (rainy period). We believe that V. gigantea may be able to utilize the absorptive function of the roots at opportune times through the growth of new roots and eliminate this function when necessary (drought periods) through the lignification of newly developed roots. This hypothesis needs to be verified through studies focused on the regulation of root development in epiphytic tank bromeliads involving hormonal signalling and abiotic factors. We emphasize that studies with this type of approach can be essential to better understand the role of roots for the plasticity of bromeliads that live in the canopy.

FUTURE PERSPECTIVES

Epiphytic bromeliads are widely found in several Neotropical regions (Ulloa Ulloa et al., 2017; Palma-Silva and Fay, 2020). They are quite diverse and it is possible to find species of bromeliads occupying the canopy of different forest ecosystems such as mesic forests or hot dry woodlands. The diversity of bromeliads contributes to the healthy functioning of ecosystems and human welfare (Ladino et al., 2019). Bromeliads help maintain biodiversity by providing microhabitats, nutritional resources and water to several species of animals and play an important role in the nutrient and water cycles of ecosystems. They also provide raw material for production of chemical and pharmaceutical products and are considered a source of food and fibre for human societies (Ladino et al., 2019). As ornamental plants, they are widely cultivated and traded (Negrelle et al., 2012). However, bromeliad diversity may be threatened by global climate change (Benzing, 2023).

One of the phenomena expected with the climate crisis is an increase in temperature. Rising temperatures can shift the frequency, duration and volume of rainfall in different regions. In forest areas, change in water availability does not need to be drastic to have a significant impact on the existence of epiphytic flora such as many species of bromeliads (Benzing, 2023). In regions where a delicate balance between epiphytic flora and climate exists, moderate changes in the rainfall regime (e.g. adding or subtracting a few weeks from the wet season) might be enough to influence photosynthetic rate, growth, development and reproduction of epiphytic bromeliads (Benzing, 2023).

In this context, the ability to develop functional roots to absorb resources might be important for epiphytic bromeliads to survive the impact of climate change. Even if rainfall, for example, decreases due to global climate change, epiphytic bromeliads would have the ability to further optimize the capture of water and nutrients with the development of new roots (synergistic effect), perhaps enabling these plants to absorb enough resources to survive even longer periods of scarcity. Furthermore, through the development of new roots, bromeliads may be able to forage the epiphytic environment in search of water and nutrients when these resources are scarce within the tank. To verify whether the root system would really be able to help epiphytic bromeliads overcome the effects of global climate change, we highlight the importance of finding answers to the following questions: (1) What abiotic stimuli would lead to the development of roots in epiphytic bromeliads? (2) How does the shoot detect environmental changes and communicate these shifts to the root system? (3) Which transporters are involved in the process of resource uptake carried out by newly developed roots and how are these proteins regulated? (4) Do epiphytic bromeliads that live in a natural environment also use the synergistic effect strategy to capture more resources as seen for cultivated bromeliads?

We believe that research involving the roots of epiphytic bromeliads is just beginning and many questions will soon be answered. Future studies are needed to explore (1) the importance of the absorptive function of the root system for the different functional types of bromeliads (e.g. terrestrial, saxicolous, tank epiphytes, atmospheric epiphytes) and (2) the real contribution that the absorptive capability of the roots can offer to promote better growth and development of epiphytic bromeliads living in the natural environment. In addition, we believe that physiological studies involving topics such as hormonal signalling or the influence of abiotic factors on the biosynthesis, activity and regulation of various molecules associated with root formation and its absorptive capability could greatly expand our understanding of the role of the root system in the plasticity of bromeliads that live in the forest canopy. A better understanding of the plasticity of bromeliads in the face of climate change will help us measure the impacts that, for example, global warming will have on different populations and species of epiphytic bromeliads, allowing us to focus conservation strategies on the most threatened species.

CONCLUSION

• For decades, the roots of epiphytic tank bromeliads were regarded as mere holdfast structures that had almost completely lost their ability to absorb water and nutrients. The reduced root system was considered an important adaptation for tank-forming epiphytic bromeliads since metabolic resources, water and energy could be saved through the non-necessity of keeping the root tissues physiologically active.

• The first few studies that investigated the absorptive capability of roots in epiphytic tank bromeliads confirmed the hypothesis that the root system was not physiologically active. However, more recent studies have brought indirect and direct evidence that has contradicted this older hypothesis.

• The absorptive capability of the roots varies according to the growth stage of the tank-forming epiphytic bromeliad. In the juvenile stage in which the plant has not yet developed a tank, the roots can be more important than the leaf trichomes in water and nutrient uptake. However, this importance gradually decreases as the bromeliad grows. In the adult stage when the bromeliad has a tank, the leaf trichomes become the main protagonists in the process of resource uptake.

• More recent studies have shown that even in epiphytic bromeliads with large tanks, some species continue to maintain an active root system, although the roots no longer act as protagonists in the process of water and nutrient uptake as seen in the juvenile phase.

• Regarding the characteristics of root and foliar uptake in adult epiphytic tank bromeliads: (1) the uptake of resources by leaf trichomes and roots appears to be two independent processes with little interference with each other; (2) the root system seems to be able to absorb enough nutrients to promote the growth and development of plant, as the absorbing trichomes are able to do in leaf surfaces; (3) the physiological characteristics and biochemical properties of the processes of absorption and distribution of nutrients and water in the tissues seem to differ between absorption through trichomes and by roots; and (4) absorption by roots effectively complements the process of resource uptake that is mainly carried out by trichomes (synergistic effect).

• The uptake capability of epiphytic tank bromeliads can vary according to several factors, such as species, genetic predisposition, type of substrate with which the roots are in contact and changes in environmental conditions, such as relative humidity.

• The ability to develop physiologically active roots for the absorptive function may offer greater plasticity for epiphytic bromeliads to absorb enough nutrients and water to guarantee their survival even in the face of the effects of global climate change on the epiphytic environment.

FUNDING

This work was financially supported by the Coordination of Superior Level Staff Improvement (CAPES-DS) [Finance Code 001] through the granting of a PhD fellowship to the first author. We also would like to thank the National Council of Technological and Scientific Development (CNPq) [grant numbers: 303497/2018-1] and São Paulo Research Foundation (FAPESP) [grant numbers: 2011/50637-0, 2018/12667-3] for financial support to develop the studies performed in our laboratory.

CONFLICT OF INTEREST

The authors declare no conflicts of interest.