Water and nutrient uptake capacity of leaf-absorbing trichomes vs. roots in epiphytic tank bromeliads

https://doi.org/10.1016/j.envexpbot.2019.04.012Get rights and content

Highlights

  • Lutheria splendens and Aechmea aquilega are epiphytic tank bromeliad.

  • Leaf absorbing trichomes and roots have different functions in resource uptake in the two species.

  • The root system of L. splendens only plays a negligible role in resources uptake.

  • The root system of A. aquilega does contribute to water and nutrient uptake.

Abstract

The water and nutrient uptake mechanisms used by vascular epiphytes have been the subject of a few studies. While leaf absorbing trichomes (LATs) are the main organ involved in resource uptake by bromeliads, little attention has been paid to the absorbing role of epiphytic bromeliad roots. This study investigates the water and nutrient uptake capacity of LATs vs. roots in two epiphytic tank bromeliads Aechmea aquilega and Lutheria splendens. The tank and/or the roots of bromeliads were watered, or not watered at all, in different treatments. We show that LATs and roots have different functions in resource uptake in the two species, which we mainly attributed to dissimilarities in carbon acquisition and growth traits (e.g., photosynthesis, relative growth rate, non-structural carbohydrates, malate), to water relation traits (e.g., water and osmotic potentials, relative water content, hydrenchyma thickness) and nutrient uptake (e.g., 15N-labelling). While the roots of A. aquilega did contribute to water and nutrient uptake, the roots of L. splendens were less important than the role played by the LATs in resource uptake. We also provide evidenced for a synergistic effect of combined watering of tank and root in the Bromelioideae species. These results call for a more complex interpretation of LATs vs. roots in resource uptake in bromeliads.

Introduction

Vascular epiphytes, which grow on other plants without parasitism, have no contact with terrestrial soil resources, and consequently need to take up nutrients from rainfall, throughfall and stemflow water and/or from decomposing organic matter in the canopy (Gotsch et al., 2015). Epiphytes have evolved numerous remarkable adaptations (e.g., litter-trapping leaf arrangements, water-storing phytotelmata, leaf-absorbing trichomes, velamen radicum) to facilitate nutrient uptake (Benzing, 1990; Lüttge, 2008; Pridgeon, 1987). Bromeliads, one of the largest and most widespread families of vascular plants in the Neotropics, display many of these adaptations.

The Bromeliaceae family comprises 3140 species distributed in three subfamilies: Bromelioideae, Tillandsioideae and Pitcairnioideae (Crayn et al., 2004 but see Givnish et al., 2011 for recent systematic updates). Bromeliads account for a large proportion of vascular epiphyte species distributed throughout the tropical and subtropical regions of the Americas. The ecological success of this wide geographic distribution may be explained by the development of key innovations (Givnish et al., 2014; Males, 2016): (i) epiphytism, (ii) leaf-absorbing trichomes (hereafter LATs), which facilitate water and nutrient uptake, (iii) tank growth form, in which a rosette of leaves forms a reservoir to trap rainwater, leaf litter and aquatic organisms, and (iv) Crassulacean acid metabolism (CAM) photosynthesis, which enables bromeliads to survive under dry environmental conditions. Characteristic combinations of these innovations have been used to define five functional types (Benzing, 2000): Type I, C3 or CAM Soil-Root (Pitcairnioideae and Bromelioideae); Type II, CAM Tank-Root (Bromelioideae); Type III, CAM Tank-Absorbing Trichome (Bromelioideae); Type IV, C3 Tank-Absorbing Trichome (Tillandsioideae) and Type V, CAM Atmosphere-Absorbing Trichome (Tillandsioideae).

Bromeliads show varying degrees of dependency on LATs vs. roots for nutrient uptake depending on their functional type. The terrestrial species (Types I and II) have a well-developed root system for anchorage and resource uptake, whereas epiphytes (from Types III to V) are capable of absorbing water and nutrients through their LATs, thereby reducing the root function to pure mechanical support (Benzing, 2000; Martin, 1994; Winkler and Zotz, 2009). Some of the most “extreme” Type V epiphytes are rootless (e.g., Tillandsia usneoides) and depend solely on their LATs for water and mineral nutrition (Benzing and Ott, 1981). LATs enable very effective uptake of both inorganic and organic forms of nitrogen as well as various micronutrients (Inselsbacher et al., 2007; Winkler and Zotz, 2010, 2009). While a large panel of studies has focused on the structure and the importance of water and nutrient uptake by LATs (e.g., Benzing, 1976; North et al., 2013; Nyman et al., 1987), little attention has been paid to the structure and absorbing role of bromeliad root systems (but see Carvalho et al., 2017; Vanhoutte et al., 2016). To our knowledge, very few studies have investigated the role of LATs vs. roots in resource uptake, and their results are inconsistent. While some studies failed to detect any (Nadkarni and Primack, 1989; Winkler and Zotz, 2009) or very little root nutrient uptake (Nievola and Mercier, 1996), others underlined efficient root nutrient uptake (Silva et al., 2018; Carvalho et al., 2017; Vanhoutte et al., 2017, 2016). More studies are thus needed to better grasp the role of roots in water and nutrient uptake in comparison to that of LATs.

These contradictory results could be due to the variety of experimental approaches used in each study (e.g., radioactive or isotopic labelling, gamma spectrometry, enzymatic activity). Additionally, in some studies, the role of roots was investigated while the tank continued to receive water (Carvalho et al., 2017; Vanhoutte et al., 2017). In such experimental conditions, the role of roots may be minimised as tank bromeliads can rely on the tank reservoir and water-storage tissues in the leaves (i.e., hydrenchyma) which may be responsible for external and internal water (and nutrient) storage, respectively (Freschi et al., 2010b; Males, 2016). A situation in which only the roots receive water and minerals, and not the tank, is unlikely to happen under natural conditions but this experimental design makes it possible to properly separate the functioning of LATs vs. roots in resource uptake, and subsequently in plant performance. An integrative approach with measurements of functional traits should provide information on resource capture, use and allocation.

The aim of the present study was to investigate the resource uptake capacity of LATs vs. roots in two common epiphytic tank-bromeliad species: Aechmea aquilega (Salib.) Griseb and Lutheria splendens (Brongn.) Lem. These two species were chosen because they differ in their ontogenic development: L. splendens is a heteroblastic species which change from juvenile atmospheric to adult tank forms whereas A. aquilega is homoblastic. Thus, at the juvenile stage L. splendens have narrow, lanceolate leaves, densely covered with LATs (pers. obs., see also Meisner et al. (2013) for others Tillandsioiseae species), whereas A. aquilega do not have any LATs at the juvenile stage indicating that the roots is of prime importance for nutrient absorption (Leroy et al., 2019). On the contrary, at the adult tank form both species have LATs that are non-homogeneously distributed throughout the leaf blade. There is a longitudinal gradient of LATs density where the basal portion of the leaf, in contact with water and nutrients in the tank, has higher LATs density than the apical portion (Takahashi et al., 2007). The ontogenic specificities of these two species led us to speculate that there may be differences in the degree of dependence on LATs vs. roots for resource uptake at the adult tank form. Specifically, we hypothesised that A. aquilega would acquire water and nutrients through its roots more efficiently than L. splendens, subsequently providing greater nutritional benefits to the plant. To test these hypotheses, we used a semi-controlled experimental approach consisting of watering potted tank form bromeliads in a greenhouse using four different treatments: (i) watering both the tank and the roots, (ii) watering only the tank, (iii) watering only the roots, and (iv) not watering the plants at all. The last treatment, corresponding to drought conditions, enabled us to identify symptoms of drought stress, which were then compared to the species responses under the other treatments. We compared the way the two bromeliad species responded to the water treatments by using a unique set of functional traits related to growth, carbon metabolism, water status, and nutrient uptake.

Section snippets

Plant materials and growth conditions

Aechmea aquilega (Salib.) Griseb (Fig. 1A) is a Type III tank-forming bromeliad belonging to the subfamily Bromelioideae with CAM photosynthesis (Crayn et al., 2004). This species occurs as an epiphytic, rupicolous or secondary terrestrial bromeliad in full sun or partial shade environments (Leroy et al., 2013). Adult tank form A. aquilega growing in a shaded greenhouse at the Campus agronomique in Kourou French Guiana were used for the experiment. The plants (n = 24) were characterised by a

Results

Species and treatment had significant effects on most of the measured traits (Table 1). The interaction between species and treatment had significant effects on some of the traits, indicating that the two species responded differently to the treatments.

Discussion

Our study revealed that the two bromeliads species differ substantially in the role played by LATs vs. roots in resource uptake. In A. aquilega, both LATs and roots absorbed water and nutrients whereas in L. splendens, roots were less important than the role played by LATs. These results were supported by a unique set of functional traits related to species response to water depletion.

Conclusion

The two tank-forming bromeliads investigated in this study exhibited substantial differences in their carbon, water, and nutrient-related traits when only their root system was watered, A. aquilega having trait values indicative of well-watered plants and L. splendens having trait values indicative of drought-stressed plants. Consequently, the LATs and roots of the two species play contrasted roles in resource uptake that confirm our hypothesis. Specifically, the roots of A. aquilega

Author contribution statement

CL, conceived and designed the experiment, supervised EG, performed the acquisition of ecophysiological data, performed the statistical analysis, contributed to the interpretations of results, wrote the manuscript, compiled the authors’ contributions; EG, performed the experiment, performed the acquisition of ecophysiological data, organized the database, performed the statistical analysis; LSO, performed NSC analysis, contributed to the interpretations of results; SC, performed the acquisition

Acknowledgements

We would like to thank Jocelyn Cazal and Jean-Yves Goret for their help in the field, in the greenhouse installation and for technical assistances, Aline Bertinatto Cruz for malate HPLC analyses and SILVATECH, ISC from UMR 1434 SILVA, 1136 IAM, 1138 BEF and 4370 EA LERMAB research center INRA Nancy-Lorraine for it contribution to NSC analyses. SILVATECH facility is supported by the Agence Nationale de la Recherche through the Laboratory of Excellence ARBRE (ANR-11-LABX-0002-01). We are grateful

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