Acessibilidade / Reportar erro

Adaptive morphoanatomy and ecophysiology of Billbergia euphemiae, a hemiepiphyte Bromeliaceae

Abstract

Habitats under distinct selective pressures exert adaptative pressures that can lead individuals of the same species to present different life strategies for their survival. The aim of this study was to analyse morphoanatomical and physiological traits for identification of adaptive ecological strategies related to both terrestrial and epiphytic life phases of Billbergia euphemiae. It was verified that B. euphemiae showed lower height, as well smaller length, width and foliar area in epiphytic phase than in terrestrial phase. Concerning to foliar anatomy, the thicknesses of leaf and water-storage parenchyma were higher in terrestrial phase, as densities of stomata and scales on the abaxial surface were higher in epiphytic phase. About the contents of photosynthetic pigments, only chlorophyll a/b ratio showed differences between life phases. In both habits, plants exhibited roots with absorption hair. In epiphytic phase, roots exhibited higher velamen thickness, smaller outer cortex, higher number of inner cortex cell layers and higher number of protoxylem poles. Thus, B. euphemiae individuals in epiphytic exhibited lots of traits related to water retention, once these plants are not into the ground. Besides, the plasticity observed may contribute for survival of this group in habitats submitted to modifications (e.g., climate change and other variations caused by human interference).

Key words:
anatomy; epiphyte; leaf; photosynthetic pigments; root

Resumo

Habitats com pressões seletivas diferentes exercem pressões adaptativas que podem levar indivíduos de uma mesma espécie a apresentar diferentes estratégias de vida para sua sobrevivência. O objetivo desse estudo foi analisar características funcionais para identificação de estratégias ecológicas adaptativas relacionadas às fases de vida terrestre e epifítica de Billbergia euphemiae. Foi verificado que B. euphemiae na fase epifítica possui menor altura, bem como folhas de menor comprimento, largura e área em relação às plantas na fase terrestre. Em relação à anatomia foliar, a espessura do limbo e do parênquima aquífero foram maiores em plantas na fase terrestre, enquanto a densidade de estômatos e de escamas na face abaxial foram maiores na fase epifítica. Em relação ao teor de pigmentos fotossintéticos, apenas clorofila a/b mostrou diferença entre as fases de vida. Em ambos os habitats, as plantas exibiram raízes com pelos absorventes. Na fase epifítica, as raízes exibiram maior espessura do velame, menor córtex externo, maior número de camadas celulares no córtex interno e maior número de polos de protoxilema. Dessa forma, indivíduos de B. euphemiae na fase epifítica exibiram muitas características relacionadas à retenção de água, uma vez que essas plantas não estão inseridas no solo. Além disso, a plasticidade observada pode contribuir para sobrevivência desse grupo em habitats sujeitos a mudanças (e.g., mudanças climáticas e outras variações causadas por interferência humana).

Palavras-chave:
anatomia; epífita; folha; pigmentos fotossintéticos; raiz

Introduction

Habitats under distinct selective pressures exert adaptative pressures that can lead individuals of the same species to present different life strategies for their survival (Bradshaw 1965Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Advances in Genetics 13: 115-155.; Ackerly 2003Ackerly DD (2003) Community assembly, niche conservatism, and adaptive evolution in changing environments. International Journal of Plant Sciences 164: S165-S184.; Nicotra et al. 2010Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladares F & van Kleunen M (2010) Plant phenotypic plasticity in a changing climate. Trends in Plant Science 15: 684-692.). Hemiepiphytes are known for being epiphytes that show a phase of life associated to the ground (Kress 1986Kress WJ (1986) The systematic distribution of vascular epiphytes: an update. Selbyana 9: 2-22.). They can be classified as primary hemiepiphytes when individuals start their lives as epiphytes and extend the roots to the ground, or as secondary hemiepiphytes, when individuals germinate in ground and adhere themselves on phorophytes through propagation stolons (Granados-Sánchez et al. 2003Granados-Sánchez D, López-Ríos GF, Hernández-García MA & Sánchez-González A (2003) Ecologia de las plantas epífitas. Revista Chapingo. Serie ciencias forestales y del ambiente 9: 101-111. ). These plants exhibit contrasting ecological strategies according to different phases of life (Holbrook & Putz 1996aHolbrook NM & Putz FE (1996a) Plants that climb up and plants that climb down: the physiology of tropical vines and hemiepiphytes. In: Smith AP, Mulkey SS & Chazdon RL (eds.) Tropical Forest Plant Ecophysiology. Chapman atid Hall Publishing Co., New York. Pp. 363-394.; Granados-Sánchez et al. 2003Granados-Sánchez D, López-Ríos GF, Hernández-García MA & Sánchez-González A (2003) Ecologia de las plantas epífitas. Revista Chapingo. Serie ciencias forestales y del ambiente 9: 101-111. ), which can be described by variations of anatomical, morphological and physiological traits (Violle et al. 2007Violle C, Navas M-L, Vile D, Kazakou E, Fortunel C, Hummel I & Garnier E (2007) Let the concept of trait be functional! Oikos 116: 882-892.).

In the past decades, many studies shown morphology and ecophysiology differences in epiphytic and terrestrial species in relation to environment (edaphic, luminosity, moisture) (Parrilla-Diaz & Ackerman 1990Parrilla-Diaz AT & Ackerman JD (1990) Epiphyte roots: anatomical correlates to environmental parameters in Puerto Rico orchids. Orquidea (Mex.) 12: 105-116.; Rada & Jaimez 1992Rada F & Jaimez R (1992) Comparative ecophysiology and anatomy of terrestrial and epiphytic Anthurium bredemeyeri Schott in a Tropical Andean Cloud Forest. Journal of Experimental Botany 43: 723-727.; Scarano et al. 2002Scarano FR, Duarte HM, Rôças G, Barreto SMB, Amado EF, Reinert F, Wendt T , Mantovani A , Lima HRP & Barros CF (2002) Acclimation or stress symptom? An integrated study of intraspecific variation in the clonal plant Aechmea bromeliifolia, a widespread CAM tank- bromeliad. Botanical Journal of the Linnean Society 140: 391-401.), biotic factors (Lawton & Williams-Linera 1996Lawton RO & Williams-Linera G (1996) Hemiepiphyte-host relationships: research problems and prospects. Selbyana 17: 71-74.) and evolution (Benzing 2000Benzing DH (2000) Bromeliaeae: profile of an adaptative radiation. Cambridge University Press, Cambridge. 690p.) in different vegetative organs (Moreira et al. 2009Moreira ASFP, Lemos-Filho JP, Zotz G & Isaias RMS (2009) Anatomy and photosynthetic parameters of roots and leaves of two shade-adapted orchids, Dichaea cogniauxiana Shltr. and epidendrum secundum Jacq. Flora 204: 604-611). Although the epiphytism has received general attention in literature, still few studies have explored adaptive strategies in hemiepiphytes (Ting et al. 1987Ting TP, Hann J, Holbrook NM , Putz FE , Sternberg LSL, Price D & Goldstein G (1987) Photosynthesis in hemiepiphytic species of Clusia and Ficus. Oecologia 74: 339-346.; Holbrook & Putz 1996bHolbrook NM & Putz FE (1996b) From epiphyte to tree: differences in leaf structure and leaf water relations associated with the transition in growth form in eight species of hemiepiphytes. Plant, Cell and Environment 19: 631-642.). In addition, among such studies much are restricts to genus Ficus sp. (Holbrook & Putz 1996bHolbrook NM & Putz FE (1996b) From epiphyte to tree: differences in leaf structure and leaf water relations associated with the transition in growth form in eight species of hemiepiphytes. Plant, Cell and Environment 19: 631-642.), still being unclear functional and ecological consequences of hemiepiphytism when take into account species belonging to other botanic family, as Bromeliaceae.

Epiphytes consist in a representative group in Bromeliaceae family, an ecologically diverse family, exhibiting high species richness among vascular plants in the neotropics (Kress 1986Kress WJ (1986) The systematic distribution of vascular epiphytes: an update. Selbyana 9: 2-22.; Zotz 2013Zotz G (2013) The systematic distribution of vascular epiphytes - a critical update. Botanical Journal of the Linnean Society 171: 453-481.), having estimated 3,352 species belonging to 58 genus (Luther 2012Luther H E (2012) An alphabetical list of bromeliad binomials. 13ª ed. Marie Selby Botanical Gardens and Bromeliad Society International, Sarasota. 44p.). Furthermore, Bromeliaceae is a group known for having several adaptations to limiting conditions (Benzing 2000Benzing DH (2000) Bromeliaeae: profile of an adaptative radiation. Cambridge University Press, Cambridge. 690p.). Some examples of those adaptations are presence of epidermal scales (Segecin & Scatena 2004Segecin S & Scatena VL (2004) Morfoanatomia de rizomas e raízes de Tillandsia L. (Bromeliaceae) dos Campos Gerais, PR. Acta Botânica Brasilica 18: 253-260. ; Proença & Sajo 2007Proença SL & Sajo MG (2007) Anatomia foliar de bromélias ocorrentes em áreas de Cerrado do estado de São Paulo, Brasil. Acta Botanica Brasilica 21: 657-673. ; Pereira et al. 2013Pereira TAR, da Silva LC, Azevedo AA, Francino DMT, Coser TS & Pereira JD (2013) Leaf morpho-anatomical variations in Billbergia elegans and Neoregelia mucugensis (Bromeliaceae) exposed to low and high solar radiation. Botany 91: 327-334.), velamen (Benzing 2000Benzing DH (2000) Bromeliaeae: profile of an adaptative radiation. Cambridge University Press, Cambridge. 690p.; Proença & Sajo 2008Proença SL & Sajo MG (2008) Rhizome and root anatomy of 14 species of Bromeliaceae. Rodriguésia 59: 113-128.) and CAM metabolism (Crassulacean Acid Metabolism) (Crayn et al. 2004Crayn DM, Winter K & Smith JAC (2004) Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae. Proceedings of the National Academy of Sciences 101: 3703-3708.). Such adaptations probably enabled these individuals to occupy a wide range of habitats, like those with low water and nutrients availability (Martin 1994Martin CE (1994) Physiological ecology of the Bromeliaceae. Botanical Review 60: 1-82.), specially in Bromelioideae subfamily. This is one of eight subfamily of Bromeliaceae (Givnish et al. 2011Givnish TJ , Barfuss MHJ, Van Ee B, Riina R, Schulte K, Horres R, Gonsiska PA, Jabaily RS, Crayn DM , Smith JAC , Winter K , Brown GK, Evans TM, Holst BK, Luther H, Till W, Zizka G, Berry PE & Sytsma KJ (2011) Phylogeny, adaptive radiation, and historical biogeography in Bromeliaceae: insights from an eight-locus plastid phylogeny. American Journal of Botany 98: 872-895.; Goetze et al. 2016Goetze M, Schulte K , Palma-Silva C, Zanella CM, Büttow MV, Capra F & Bered F (2016) Diversification of Bromelioideae (Bromeliaceae) in the Brazilian Atlantic rainforest: a case study in Aechmea subgenus Ortgiesia. Molecular phylogenetics and evolution 98: 346-357.), with more of 500 species occurring in phytophysiognomies of Atlantic Forest (Martinelli et al. 2008Martinelli G, Vieira CM, Gonzalez M, Leitman P, Piratininga A, Costa A F & Forzza RC (2008) Bromeliaceae da Mata Atlântica brasileira: lista de espécies, distribuição e conservação. Rodriguésia 59: 209-258).

Billbergia euphemiae E. Morren, is a secondary hemiepiphyte (Kress 1986Kress WJ (1986) The systematic distribution of vascular epiphytes: an update. Selbyana 9: 2-22.; Granados-Sánchez et al. 2003Granados-Sánchez D, López-Ríos GF, Hernández-García MA & Sánchez-González A (2003) Ecologia de las plantas epífitas. Revista Chapingo. Serie ciencias forestales y del ambiente 9: 101-111. ), native of Brazil, which belongs to Bromelioideae subfamily (Bromelieae tribe) (BFG 2018BFG - The Brazil Flora Group (2018) Brazilian Flora 2020: innovation and collaboration to meet Target 1 of the Global Strategy for Plant Conservation (GSPC). Rodriguésia 69: 1513-1527.). Such species occur normally in Atlantic Forest, including montane and submontane phytophysiognomies (Fontoura 1991Fontoura T, Costa A & Wendt T (1991) Preliminary checklist of Bromeliaceae of Rio de Janeiro state, Brazil. Selbyana 12: 1-45.), and is typical of restinga areas (Magnago et al. 2007Magnago LFS, Pereira OJ, Matos FAR & Souza PF (2007) Caracterização Fitofisionômica da Restinga na Morada do Sol, Vila Velha, ES. Revista Brasileira de Biociências 5: 456-458.). Its distribution is submitted to the influence of environmental factors variations, such as luminosity, humidity, availability of nutrients in ground and salinity, as well as biological factors, like reproduction and seed dispersion (Lüttge 2008Lüttge U (2008) Physiological ecology of tropical plants. Springer, Berlin. 458p. ). Overall, leaf anatomy of Billbergia euphemiae include an uniseriate and lignified epidermis with reduced lumen, cutinized. The stomata are in the same level of epidermis on abaxial surface of leaves and arranged in longitudinal rows. Peltate scales cover all surface in both surface of the epidermis, and disc cells do not differ from wing cells and have round shaped. This specie has water storage parenchyma, and subjacent, chlorenchyma with aeration channels and collateral vascular bundles in single series in the lower half of the leaf blade (Pereira et al. 2011Pereira TAR, Oliveira TS, Silva LC & Azevedo AA (2011) Comparative leaf anatomy of four species of Bromelioideae (Bromeliaceae) occurring in the Atlantic Forest, Brazil. Botany 89: 243-253.).

In this context, understanding anatomy, morphology and physiology of hemiepiphytes is important for knowing how these plants behave according to environmental conditions in different phases of life. Moreover, this study allow to complement a big range of studies that hemiepiphytes anatomy focused on taxonomy (Aoyama & Sajo 2003Aoyama EM & Sajo MG (2003) Estrutura foliar de Aechmea Ruiz & Pav. subgênero Lamprococcus (Beer) Baker e espécies relacionadas. Revista Brasileira de Botânica 26: 461-473. ; Ferreira et al. 2007Ferreira LMSL, Bellitani MC & Silva LB (2007) Anatomia Foliar de Orthophytum mucugense Wand. e Conceição (Bromeliaceae). Revista Brasileira de Biociências 59: 825-827.; Monteiro et al. 2011Monteiro RF, Forzza RC & Mantovani A (2011) Leaf structure of Bromelia and its significance for the evolution of Bromelioideae (Bromeliaceae). Plant Systematycs and Evolution 293: 53-64.; Zotz 2013Zotz G (2013) The systematic distribution of vascular epiphytes - a critical update. Botanical Journal of the Linnean Society 171: 453-481.) and ecology of Bromeliaceae (Dickison 2000Dickison WC (2000) Integrative Plant Anatomy. Academic Press, Harcourt. 533p.; Bonnet & Queiroz 2006Bonnet A & Queiroz MH (2006) Estratificação vertical de bromélias epifíticas em diferentes estádios sucessionais da Floresta Ombrófila Densa, Ilha de Santa Catarina, Santa Catarina, Brasil. Revista Brasileira de Botânica 29: 217-228. ; Voltolini & Santos 2011Voltolini CH & Santos M (2011) Variações na morfoanatomia foliar de Aechmea lindenii (E. Morren) Baker var. lindenii (Bromeliaceae) sob distintas condições ambientais. Acta Botanica Brasilica 25: 2-10.; Males & Griffiths 2017Males J & Griffiths H (2017) Leaf economic and hydraulic divergences underpin ecological differentiation in the Bromeliaceae. Plant, Cell & Environment. doi: 10.1111/pce.12954
https://doi.org/10.1111/pce.12954...
). In this context, the aim of this study was to investigate adaptive strategies of B. euphemiae, in both terrestrial and epiphytic phases. Our hypothesis is that in epiphytic phase there are more traits related to high incidence of light and to water retention, once the roots are not into the ground.

Material and Methods

Study area

This study was carried out within the dry forest formation of restinga located at Paulo César Vinha State Park, a coastal plain of nearly 1,500 ha in Espírito Santo state, Brazil (20º33’-20º38’S, 40º23’-40º26’W). Weather of region is Aw type according to Köppen classification (1948)Köppen W (1948) Climatología: con un estudio de los climas de la Terra. Fondo de Cultura Económica, Mexico. 496p., with annual temperature averaging 23.3º, annual rainfall of 1,307 mm and relative humidity of 80%. Such climate is characterized by existence of rainy summers and dry winters (Fabris 1995Fabris LC (1995) Composição florística e fitossociológica de uma faixa de floresta arenosa litorânea do Parque Estadual de Setiba, Município de Guarapari, ES. Dissertação de Mestrado. Universidade Estadual Paulista, Rio Claro. 195p.).

Botanical material

There were sampled mature leaves, collected on median areas of both rosette and roots that presented larger diameters, from five adult individuals in terrestrial phase and five individuals in epiphytic phase of Billbergia euphemiae (Fig. 1). We deposited the voucher of the species samples in VIES herbarium at Federal University of Espírito Santo, identified with the register number VIES 37156 in 12/09/2012 by collector B.B. Zorger s.n.

Figure 1
a-c. Individuals of Billbergia euphemiae in dry forest formation of restinga in Paulo César Vinha State Park, ES, Brazil – a,b. terrestrial phase; c. epiphytic phase. Arrow indicates stolon of propagation.

Morphological measures analysis

We measured length (cm), area (cm2), dry mass per area - LMA (g cm-2) and foliar succulence (g cm-2) - obtained by fresh mass minus foliar dry mass of foliar area divided by foliar area - one leaf per plant, totalling five leaves. We also measured the height from the ground (cm) of each sampled individual the upper boundary of the photosynthetic tissue (i.e. except inflorescence, seeds or fruits) (Pérez-Harguindeguy et al. 2013Pérez-Harguindeguy N, Díaz S, Garnier E , Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, De Vos AC, Buchmann N, Funes G, Quétier F, Hodgson JG, Thompson K, Morgan HD, Ter Steege H, van der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti MV, Conti G, Staver AC, Aquino S & Cornelissen JHC (2013) New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61: 167-234.). Length, width and height were measured by a measuring tape. The leaf area was measured using an Area Meter LI-COR 3100 (Lincoln, USA). To obtain dry mass, leaves were weight after collecting them. As for dry mass, samples were weight after drying in the oven at 60 ºC until obtain constant mass (Garnier et al. 2001Garnier E, Shipley B, Roumet C & Laurent G (2001) A standardized protocol for the determination of specific leaf area and leaf dry matter content. Functional ecology 15: 688-695.).

Determination of leaf angle

We measured leaf angle (º) in relation to the ground in one leaf from each individual, totalling five measurements, using a clinometer (James & Bell 2000James SA & Bell DT (2000) Leaf orientation, light interception and stomatal conductance of Eucalyptus globulus ssp. globulus leaves. Tree Physiology 20: 815-823.).

Anatomical and histochemical analysis

We fixed leaves and roots from five individuals in FAA 50 (a mixture of formaldehyde, ethanol and acetic acid) (Johansen 1940Johansen D (1940) Plant microtechnique. McGraw-Hill, New York. 523p.) and stored in 70% ethanol. We made transversal sections by freehand, with razor blades, in median foliar third and 1 cm from the top of the root. We did the colouring process with safrablau solution, set them between the blade and the coverslip with glycerine (Kraus & Arduin 1997Kraus JE & Arduin M (1997) Manual básico de métodos em morfologia vegetal. EDUR, Rio de Janeiro. 198p.). On the leaves, we quantified leaf thickness (µm), chlorenchyma, and water-storage parenchyma thickness. We also analysed stomata and scales densities (nº mm-2) in both surfaces of epidermis through epidermal impressions, using a drop of cyanoacrylate ester adhesive (Super Bonder®) on a histological blade (Wilson et al. 1981Wilson CKL, Pusey PL & Otto BE (1981) Plant epidermal sections and imprints using cyanoacrylate adhesives. Canadian Journal of Plant Science 61: 781-783.). In roots, we measured the diameter (µm) of metaxylem conducting elements and thickness of root, velamen, outer cortex or exoderm, inner cortex, poles numbers of protoxylem, and then identified presence/absence of epidermal hair and intercellular spaces on inner cortex. For each analysed parameter, we made eight measures in every sample (leaf and root) of five terrestrial individuals and from five epiphytes individuals. We measured all of them through a capture image system linked to Nikon E200 (Tokyo, Japan) microscope using Tsview v.6.1.3.2 software (Tucsen Imaging Technology Co. Limited). Results were documented using photomicrographs.

For histochemical analysis, freehand sections of roots were submitted to the reagent phloroglucinol in acid medium (Sass 1951Sass JE (1951) Botanical Microtechnique. 2nd ed. Ames, The Iowa State College Press, Iowa. 228p.) to verify possible lignified walls in cells of velamen.

Determination of photosynthetic pigments contents

We made the photosynthetic pigments extraction according to Arnon’s method (1949)Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24: 1-15. that uses acetone 80% as extractor. Therefore, we macerated 0.200 g of fresh plant material in 25 mL of acetone. We made the whole process with samples maintained under low temperatures in a dark chamber using green light 40 W. We made extracts measurements using a Genesys 10 S UV-Vis Thermo Scientific spectrophotometer on 480, 645 and 663 nm absorbencies. To define photosynthetic pigments contents (µmol g-1 MF) we used the equations of Hendry & Grime (1993)Hendry GAF & Grime JP (1993) Methods in comparative plant ecology. Chapman & Hall, London. 252p.:

Chlorophyll a = 12 . 7 . A 663 2 . 69 . A 645 × 1 . 119 Chlorophyll b = 22 . 9 . A 645 4 . 68 . A 663 × 1 . 102 Carotenoids = A 480 + 0 . 114 . A 663 0 . 638 . A 645 × V / 112 . 5 . FM

Where: A480= a 480 nm; A645= absorbance on 645 nm; A663= absorbance on 663 nm; V = sample volume (mL) and FM = sample fresh mass (g).

Determination of photosynthetically active radiation (PAR)

We measured the Photosynthetically Active Radiation (µmol g-1 MF) at the occurrence area of terrestrial and epiphytic individuals using a FieldScout Quantum Light Meters reader (Plainfield, USA). We made five measurements at 9:00 AM, 11:00 AM and 13:00 PM, maintaining the equipment close to the individuals collected in each life phase and then we calculated the arithmetic mean of each one.

Data analysis

Data obtained through analysis of morphology, foliar angle, anatomy, photosynthetic pigments contents and photosynthetically active radiation were submitted to Shapiro-Wilk’s test for normality. Once all data showed normal distribution, means were compared by t-test on STATISTICA 10 software (Statsoft 2006Statsoft Inc. (2006) Statistica (data analysis software system), version 10.0. Available at <http://www.statsoft.com/Products/STATISTICA-Features> Access on 16 July 2017.
http://www.statsoft.com/Products/STATIST...
).

Results

Epiphytic phase of Billbergia euphemiae showed lower height; leaves with lowers length, width and area (Tab. 1). About photosynthetic pigments content, it was observed higher values of chlorophyll a/b ratio (Tab. 1). In relation to anatomic aspects, B. euphemiae in the epiphytic phase shown lower water-storage parenchyma thickness, lower leaf thickness and higher stomata and scales densities on abaxial epidermis, in relation to terrestrial phase (Fig. 2; Tab. 1). The following attributes showed no changes between terrestrial and epiphytic phases: foliar angle, succulence, LMA, chlorophyll a, chlorophyll b, total chlorophyll, PAR and carotenoids, as well as, chlorenchyma thickness and adaxial scales (Tab. 1).

Table 1
Comparative between means ± standard deviation (mean ± SD) of Billbergia euphemiae individuals traits in terrestrial and epiphytic phase in dry forest of restinga in Paulo César Vinha State Park, ES, Brazil. Means with different letters indicates significant differences by t-test in level of 5% (p < 0.05) of probability.

Figure 2
a-f. Transverse sections of Billbergia euphemiae – a-b. leaves – a. terrestrial phase; b. epiphytic phase; c-f. roots – c,e. terrestrial phase; d,f. epiphytic phase. The arrow indicates epivelamen. (oc = outer cortex; ic = inner cortex; ws = water-storage parenchyma; ch = chlorenchyma; ve = velamen). Scale bars = 50 μm.

Individual roots in the epiphytic phase showed higher total root thickness, thicker velamen with higher number of cell layers, lower thickness of outer cortex with lower number of cell layers, higher number of cellular layers of inner cortex and higher number of protoxylem poles, in relation to terrestrial phase (Fig. 2; Tab. 1). Both terrestrial and epiphytic individuals have root hair on peripheral layer of velamen cell (epivelamen). On the other hand, only inner cortex in the terrestrial phase presented intercellular spaces. The metaxylem diameter was the same in both phases (Fig. 2; Tab. 1).

Results of histochemical analysis were negative for detection of lignified walls in velamen cells.

Discussion

Results indicate that Billbergia euphemiae individuals present part of attributes related to water conservation in epiphytic phase. It may be observed through the reduction of morphological measures, scales densities on abaxial epidermis, velamen thickness and number of poles on protoxylem. These attributes can be related to lower water and nutrients availability, since the roots of epiphytes plants are not into the ground (Benzing 2000Benzing DH (2000) Bromeliaeae: profile of an adaptative radiation. Cambridge University Press, Cambridge. 690p.).

The lower height found in B. euphemiae individuals of epiphytic phase, that propagated on phorophyte from stolon, may be explained by lower water and nutrients availability, which may contributes to lower cellular extension and photosynthetic efficiency (Lloyd & Farquhar 1996Lloyd J & Farquhar GD (1996) The CO2dependence of photosynthesis, plant growth responses to elevated atmospheric CO2 concentrations and their interaction with ground nutrient status. 1. General principles and forest ecosystems. Functional Ecology 10: 4-32.; Jaleel et al. 2009Jaleel CA, Manivannan P, Wahid A, Farooq M, Al-Juburi HJ, Somasundaram F & Panneerselvam R (2009) Drought stress in plants: a review on morphological characteristics and pigments composition. International Journal of Agricultural and Biology 11: 100-105.). In addition, the smaller height found may be a direct consequence of the smaller leaf size in the epiphytic phase. Lower length, width and leaf area in that phase can be seen as mechanisms for water retention (Reinert 1998Reinert F (1998) Epiphytes: photosynthesis, water balance and nutrients. Oecologia Brasiliensis 4: 87-108.). Smaller and straighter leaves are submitted to less resistance of air boundary layer which favours the faster cooling of the leaf and avoid water loss by transpiration (Parkhurst & Loucks 1972Parkhurst DF & Loucks OL (1972) Optimal leaf size in relation to environment. Journal of Ecology 60: 505-537.; Givnish & Vermeij 1976Givnish TJ & Vermeij GJ (1976) Sizes and shapes of liane leaves. American Naturalist 100: 743-778.). This is a common trait in plants that are submitted to lower water availability, like individuals of B. euphemiae in epiphytic phase (Benzing 2000Benzing DH (2000) Bromeliaeae: profile of an adaptative radiation. Cambridge University Press, Cambridge. 690p.).

About the photosynthetic pigments contents only chlorophyll a/b changed between terrestrial and epiphytic phases. It means that in epiphytes, chlorophyll b is degraded faster in relation to chlorophyll a (Kramer & Kozlowski 1979Kramer PJ & Kozlowski TT (1979) Physiology of woody plants. Academic Press, New York. 811p. ; Ishida et al. 1999Ishida A, Toma T & Marjenah (1999) Leaf gas exchange and chlorophyll fluorescence in relation to leaf angle, azimuth, and canopy position in the tropical pioneer tree, Macaranga conifera. Tree Physiology 19: 117-124. ). It may happen due to a disorder of photosystem II caused by hydric stress (Souza et al. 2004Souza RP, Machado EC, Silva JAB, Lagôa AMMA & Silveira JAG (2004) Photosynthetic gas exchange, chlorophyll fluorescence and some associated metabolic changes in cowpea (Vigna unguiculata) during water stress and recovery. Environmental and Experimental Botany 51: 45-56.). Other traits - foliar angle, LMA, succulence, chlorenchyma thickness, chlorophyll a, chlorophyll b, total chlorophyll and carotenoids - did not show changes in both terrestrial and epiphytic phase. As the light is similar in both habitats, even other factors like water and nutrients may not be strong enough to influence those foliar traits.

The higher stomata density in epiphytic phase enable the increase of CO2absorption and is normally associated to a lower stomatal pore size that reduce water loss by transpiration through the rapid stomata closing (Abrams et al. 1992Abrams MD, Kloeppel BD & Kubiske ME (1992) Ecophysiological and morphological responses to shade and drought in two contrasting ecotypes of Prunus setorina. Tree Physiology 10: 343-355.; Aasamaa et al. 2001Aasamaa K, Sober A & Rahi M (2001) Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Australian Journal Plant Physiology 28: 765-774.; Hetherington & Woodward 2003Hetherington AM & Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424: 901-908.). Furthermore, greater stomatal density may lead to greater transpiration if the stomatal opening and stomatal control in this species is less rigid, as found in plants under higher temperatures (Hetherington & Woodward 2003Hetherington AM & Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424: 901-908.). This generally allows for greater leaf transpiration and, consequently, cooling of leaves (Hetherington & Woodward 2003Hetherington AM & Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424: 901-908.; Cavallero et al. 2011Cavallero L, Galetti L, López D, McCargo J & Barberis IM (2011) Morphological variation of the leaves of Aechmea distichantha Lem. plants from contrasting habitats of a Chaco forest: a trade-off between leaf area and mechanical support. Revista Brasileira de Biociências 9: 455-464.; Voltolini & Santos 2011Voltolini CH & Santos M (2011) Variações na morfoanatomia foliar de Aechmea lindenii (E. Morren) Baker var. lindenii (Bromeliaceae) sob distintas condições ambientais. Acta Botanica Brasilica 25: 2-10.; Pereira et al. 2013Pereira TAR, da Silva LC, Azevedo AA, Francino DMT, Coser TS & Pereira JD (2013) Leaf morpho-anatomical variations in Billbergia elegans and Neoregelia mucugensis (Bromeliaceae) exposed to low and high solar radiation. Botany 91: 327-334.). However, we did not observe in this study variation in solar radiation between habitats, which could cause variation in temperature to support this hypothesis. The density of epidermal scales in abaxial surface was also higher in epiphytic individuals and contributes to water and nutrients absorption in such phase (Dickison 2000Dickison WC (2000) Integrative Plant Anatomy. Academic Press, Harcourt. 533p.). On the other hand, there was no difference of scales in adaxial surface, which may suggest an evolutionary conservation of this trait in B. euphemiae (de Bello et al. 2015de Bello F, Berg MP, Dias ATC, Diniz-Filho JAF, Götzenberger L, Hortal J, Ladle RJ & Lepš J (2015) On the need for phylogenetic ‘corrections’ in functional trait-based approaches. Folia Geobotanica 50: 349-357.).

The lower thickness of water-storage parenchyma in epiphytic phase differs from what has been found in literature (Benzing 2000Benzing DH (2000) Bromeliaeae: profile of an adaptative radiation. Cambridge University Press, Cambridge. 690p.) and does not show itself as a character related to the conservation of water. The data founded corroborates with Scarano et al. (2002)Scarano FR, Duarte HM, Rôças G, Barreto SMB, Amado EF, Reinert F, Wendt T , Mantovani A , Lima HRP & Barros CF (2002) Acclimation or stress symptom? An integrated study of intraspecific variation in the clonal plant Aechmea bromeliifolia, a widespread CAM tank- bromeliad. Botanical Journal of the Linnean Society 140: 391-401. results, which in turn showed that leaves of Aechmea bromellifolia under high stress (individuals under high intensity of light and not submitted to flood events) have lower thickness of water-storage parenchyma in relation to individuals in more favourable habitats.

In epiphytes and terrestrial roots, epivelamen exhibit root hairs, which can be seen as an strategy for water and nutrients absorption (Segecin & Scatena 2004Segecin S & Scatena VL (2004) Morfoanatomia de rizomas e raízes de Tillandsia L. (Bromeliaceae) dos Campos Gerais, PR. Acta Botânica Brasilica 18: 253-260. ; Silva & Scatena 2011Silva IV & Scatena VL (2011) Anatomia de raízes de nove espécies de Bromeliaceae (Poales) da região amazônica do estado de Mato Grosso, Brasil. Acta Botânica Brasilica 25: 618-627. ). Despite terrestrial bromeliads, roots have been described to have the exclusive function of fixation (Tomlinson 1969Tomlinson PB (1969) Commelinales - Zingiberales. In: Metcalf CR (ed.) Anatomy of the monocotyledons. Vol. 3. Anatomy of the monocotyledons. Oxford Clarendon Press, London. Pp. 193-294.), roots of B. euphemiae in both phases are capable of practicing not only fixation, but also support and possibly absorption functions. However, even with the presence of root hairs, the absorptions efficiency, probably, is lower in relation to roots fixed into the ground. It happens with the epiphytes due to fast water drainage (Tomlinson 1969Tomlinson PB (1969) Commelinales - Zingiberales. In: Metcalf CR (ed.) Anatomy of the monocotyledons. Vol. 3. Anatomy of the monocotyledons. Oxford Clarendon Press, London. Pp. 193-294.).

Individuals in epiphytic phase showed a thicker velamen. Such trait indicates that water loss is avoided via cortex and nutrients retention (Benzing 2000Benzing DH (2000) Bromeliaeae: profile of an adaptative radiation. Cambridge University Press, Cambridge. 690p.). Although, velamen confers mechanical protection and capacity of move water and nutrients in a fast and effective way for root system during the rain (Zotz & Winkler 2013Zotz G & Winkler U (2013) Aerial roots of epiphytic orchids: velamen radicum and its role in water and nutrient uptake. Oecologia 171: 733-74.). Water and nutrients absorption through the roots can be explained for lignin absence in velamen cellular walls, as shown by negative result with phloroglucinol, indicating be a characteristic that improve the water input in plants (Parrilla-Diaz & Ackerman 1990Parrilla-Diaz AT & Ackerman JD (1990) Epiphyte roots: anatomical correlates to environmental parameters in Puerto Rico orchids. Orquidea (Mex.) 12: 105-116.).

In both roots was possible to distinguish outer and inner cortex, as observed in Billbergia zebrina (Martins et al. 2016Martins JPR, Martins AD, Pires MF, Junior RAB, Reis RO, Dias GDMG & Pasqual M (2016) Anatomical and physiological responses of Billbergia zebrina (Bromeliaceae) to copper excess in a controlled microenvironment. Plant, Cell, Tissue and Organ Culture 126: 43-57.). Outer cortex is normally pluriestratified and lignified in Bromeliaceae group and avoids water loss (Tomlinson 1969Tomlinson PB (1969) Commelinales - Zingiberales. In: Metcalf CR (ed.) Anatomy of the monocotyledons. Vol. 3. Anatomy of the monocotyledons. Oxford Clarendon Press, London. Pp. 193-294.). Although, according literature, the outer cortex is thicker and lignified in epiphytes plants (Dycus & Knudson 1957Dycus AM & Knudson L (1957) The role of the velamen of the aerial roots of orchids. Botanical Gazette 119: 78-87.; Sanford & Adanlawo 1973Sanford WW & Adanlawo I (1973) Velamen and exodermis characters of West African epiphytic orchids in relation to taxonomic grouping and habitat tolerance. Botanical Journal of the Linnean Society 66: 307-321.), we observe that it is more developed in terrestrial phase than in epiphytic. One explication is that terrestrial phase individuals in restinga can be likely to soaked soil, during the rainy station (Scarano et al. 2002Scarano FR, Duarte HM, Rôças G, Barreto SMB, Amado EF, Reinert F, Wendt T , Mantovani A , Lima HRP & Barros CF (2002) Acclimation or stress symptom? An integrated study of intraspecific variation in the clonal plant Aechmea bromeliifolia, a widespread CAM tank- bromeliad. Botanical Journal of the Linnean Society 140: 391-401.); and thicker outer cortex can work as an exaptation for prevention of suffocation, and input of microorganisms more prone in terrestrial phase (Hadley & Williamson 1972Hadley G & Williamson B (1972) Features of mycorrhizal infection in some Malayan orchids. New Phytologist 71: 1111-1118.; Benzing et al. 1983Benzing DH, Friedman WE, Peterson G & Renfrow A (1983) Shootlessness, velamentous roots, and the pre-eminence of Orchidaceae in the epiphytic biotope. American Journal of Botany 70: 121-133.; Parrilla-Diaz & Ackerman 1990Parrilla-Diaz AT & Ackerman JD (1990) Epiphyte roots: anatomical correlates to environmental parameters in Puerto Rico orchids. Orquidea (Mex.) 12: 105-116.). The number of cell layers in inner cortex was higher in epiphytic phase in relation to terrestrial phase, while in inner cortex of terrestrial phase were observed intercellular spaces. These spaces can transport water for capillarity turning the process more efficient (Tomlinson 1969Tomlinson PB (1969) Commelinales - Zingiberales. In: Metcalf CR (ed.) Anatomy of the monocotyledons. Vol. 3. Anatomy of the monocotyledons. Oxford Clarendon Press, London. Pp. 193-294.) or transport air (O2and CO2), as speculated by Benzing et al. (1983)Benzing DH, Friedman WE, Peterson G & Renfrow A (1983) Shootlessness, velamentous roots, and the pre-eminence of Orchidaceae in the epiphytic biotope. American Journal of Botany 70: 121-133., which can be important to respiration in water soaked soils in terrestrial phase. We observed protoxylem poles in higher number in epiphytic phase individuals, despite metaxylem elements are similar in diameter. This fact added to velamen-exoderm set, corroborates with Tomlinson (1969)Tomlinson PB (1969) Commelinales - Zingiberales. In: Metcalf CR (ed.) Anatomy of the monocotyledons. Vol. 3. Anatomy of the monocotyledons. Oxford Clarendon Press, London. Pp. 193-294. who affirms that these elements groups are typical from individuals in epiphytic phase. Such traits can be an answer to the water and nutrients transportation need and substances to other plant organs (Tomlinson 1969Tomlinson PB (1969) Commelinales - Zingiberales. In: Metcalf CR (ed.) Anatomy of the monocotyledons. Vol. 3. Anatomy of the monocotyledons. Oxford Clarendon Press, London. Pp. 193-294.), once plants in epiphytic phase face a problem of fast water flow from phorophyte. The similarity of metaxylem diameters measures can be related to evolutionary conservatism of this trait in B. euphemiae.

In conclusion, we hypothesis was partially accepted, once a substantial part of traits improved the water conservation in epiphytic phase. Furthemore, we shown that B. euphemiae worked as a good hemiepiphyte plant model showing that plants belonging to this group can show plasticity in most of functional traits in response to water availability, a strategy that can contribute to survivor of these plants in environment under changes (e.g., climate changes and/or variations caused by human interference that lead to lower water availability). However, we indicate that part of traits in this study can reflect biotic interactions, defence to microorganisms, as well as, can be conserved within the phylogeny.

  • Area Editor: Dra. Simone Teixeira

Acknowledgements

We thank to Federal University of Espírito Santo (UFES) for financial support and to Paulo César Vinha State Park for logistic contribution during the study execution, which was developed to obtain the undergraduate degree in Biological Sciences of the first author.

References

  • Aasamaa K, Sober A & Rahi M (2001) Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Australian Journal Plant Physiology 28: 765-774.
  • Abrams MD, Kloeppel BD & Kubiske ME (1992) Ecophysiological and morphological responses to shade and drought in two contrasting ecotypes of Prunus setorina Tree Physiology 10: 343-355.
  • Ackerly DD (2003) Community assembly, niche conservatism, and adaptive evolution in changing environments. International Journal of Plant Sciences 164: S165-S184.
  • Aoyama EM & Sajo MG (2003) Estrutura foliar de Aechmea Ruiz & Pav. subgênero Lamprococcus (Beer) Baker e espécies relacionadas. Revista Brasileira de Botânica 26: 461-473.
  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris Plant Physiology 24: 1-15.
  • Benzing DH, Friedman WE, Peterson G & Renfrow A (1983) Shootlessness, velamentous roots, and the pre-eminence of Orchidaceae in the epiphytic biotope. American Journal of Botany 70: 121-133.
  • Benzing DH (2000) Bromeliaeae: profile of an adaptative radiation. Cambridge University Press, Cambridge. 690p.
  • BFG - The Brazil Flora Group (2018) Brazilian Flora 2020: innovation and collaboration to meet Target 1 of the Global Strategy for Plant Conservation (GSPC). Rodriguésia 69: 1513-1527.
  • Bonnet A & Queiroz MH (2006) Estratificação vertical de bromélias epifíticas em diferentes estádios sucessionais da Floresta Ombrófila Densa, Ilha de Santa Catarina, Santa Catarina, Brasil. Revista Brasileira de Botânica 29: 217-228.
  • Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Advances in Genetics 13: 115-155.
  • Cavallero L, Galetti L, López D, McCargo J & Barberis IM (2011) Morphological variation of the leaves of Aechmea distichantha Lem. plants from contrasting habitats of a Chaco forest: a trade-off between leaf area and mechanical support. Revista Brasileira de Biociências 9: 455-464.
  • Crayn DM, Winter K & Smith JAC (2004) Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae. Proceedings of the National Academy of Sciences 101: 3703-3708.
  • de Bello F, Berg MP, Dias ATC, Diniz-Filho JAF, Götzenberger L, Hortal J, Ladle RJ & Lepš J (2015) On the need for phylogenetic ‘corrections’ in functional trait-based approaches. Folia Geobotanica 50: 349-357.
  • Dickison WC (2000) Integrative Plant Anatomy. Academic Press, Harcourt. 533p.
  • Dycus AM & Knudson L (1957) The role of the velamen of the aerial roots of orchids. Botanical Gazette 119: 78-87.
  • Fabris LC (1995) Composição florística e fitossociológica de uma faixa de floresta arenosa litorânea do Parque Estadual de Setiba, Município de Guarapari, ES. Dissertação de Mestrado. Universidade Estadual Paulista, Rio Claro. 195p.
  • Ferreira LMSL, Bellitani MC & Silva LB (2007) Anatomia Foliar de Orthophytum mucugense Wand. e Conceição (Bromeliaceae). Revista Brasileira de Biociências 59: 825-827.
  • Fontoura T, Costa A & Wendt T (1991) Preliminary checklist of Bromeliaceae of Rio de Janeiro state, Brazil. Selbyana 12: 1-45.
  • Garnier E, Shipley B, Roumet C & Laurent G (2001) A standardized protocol for the determination of specific leaf area and leaf dry matter content. Functional ecology 15: 688-695.
  • Givnish TJ & Vermeij GJ (1976) Sizes and shapes of liane leaves. American Naturalist 100: 743-778.
  • Givnish TJ , Barfuss MHJ, Van Ee B, Riina R, Schulte K, Horres R, Gonsiska PA, Jabaily RS, Crayn DM , Smith JAC , Winter K , Brown GK, Evans TM, Holst BK, Luther H, Till W, Zizka G, Berry PE & Sytsma KJ (2011) Phylogeny, adaptive radiation, and historical biogeography in Bromeliaceae: insights from an eight-locus plastid phylogeny. American Journal of Botany 98: 872-895.
  • Goetze M, Schulte K , Palma-Silva C, Zanella CM, Büttow MV, Capra F & Bered F (2016) Diversification of Bromelioideae (Bromeliaceae) in the Brazilian Atlantic rainforest: a case study in Aechmea subgenus Ortgiesia. Molecular phylogenetics and evolution 98: 346-357.
  • Granados-Sánchez D, López-Ríos GF, Hernández-García MA & Sánchez-González A (2003) Ecologia de las plantas epífitas. Revista Chapingo. Serie ciencias forestales y del ambiente 9: 101-111.
  • Hadley G & Williamson B (1972) Features of mycorrhizal infection in some Malayan orchids. New Phytologist 71: 1111-1118.
  • Hendry GAF & Grime JP (1993) Methods in comparative plant ecology. Chapman & Hall, London. 252p.
  • Hetherington AM & Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424: 901-908.
  • Holbrook NM & Putz FE (1996a) Plants that climb up and plants that climb down: the physiology of tropical vines and hemiepiphytes. In: Smith AP, Mulkey SS & Chazdon RL (eds.) Tropical Forest Plant Ecophysiology. Chapman atid Hall Publishing Co., New York. Pp. 363-394.
  • Holbrook NM & Putz FE (1996b) From epiphyte to tree: differences in leaf structure and leaf water relations associated with the transition in growth form in eight species of hemiepiphytes. Plant, Cell and Environment 19: 631-642.
  • Ishida A, Toma T & Marjenah (1999) Leaf gas exchange and chlorophyll fluorescence in relation to leaf angle, azimuth, and canopy position in the tropical pioneer tree, Macaranga conifera Tree Physiology 19: 117-124.
  • Jaleel CA, Manivannan P, Wahid A, Farooq M, Al-Juburi HJ, Somasundaram F & Panneerselvam R (2009) Drought stress in plants: a review on morphological characteristics and pigments composition. International Journal of Agricultural and Biology 11: 100-105.
  • James SA & Bell DT (2000) Leaf orientation, light interception and stomatal conductance of Eucalyptus globulus ssp. globulus leaves. Tree Physiology 20: 815-823.
  • Johansen D (1940) Plant microtechnique. McGraw-Hill, New York. 523p.
  • Köppen W (1948) Climatología: con un estudio de los climas de la Terra. Fondo de Cultura Económica, Mexico. 496p.
  • Kramer PJ & Kozlowski TT (1979) Physiology of woody plants. Academic Press, New York. 811p.
  • Kraus JE & Arduin M (1997) Manual básico de métodos em morfologia vegetal. EDUR, Rio de Janeiro. 198p.
  • Kress WJ (1986) The systematic distribution of vascular epiphytes: an update. Selbyana 9: 2-22.
  • Lawton RO & Williams-Linera G (1996) Hemiepiphyte-host relationships: research problems and prospects. Selbyana 17: 71-74.
  • Lloyd J & Farquhar GD (1996) The CO2dependence of photosynthesis, plant growth responses to elevated atmospheric CO2 concentrations and their interaction with ground nutrient status. 1. General principles and forest ecosystems. Functional Ecology 10: 4-32.
  • Luther H E (2012) An alphabetical list of bromeliad binomials. 13ª ed. Marie Selby Botanical Gardens and Bromeliad Society International, Sarasota. 44p.
  • Lüttge U (2008) Physiological ecology of tropical plants. Springer, Berlin. 458p.
  • Magnago LFS, Pereira OJ, Matos FAR & Souza PF (2007) Caracterização Fitofisionômica da Restinga na Morada do Sol, Vila Velha, ES. Revista Brasileira de Biociências 5: 456-458.
  • Males J & Griffiths H (2017) Leaf economic and hydraulic divergences underpin ecological differentiation in the Bromeliaceae. Plant, Cell & Environment. doi: 10.1111/pce.12954
    » https://doi.org/10.1111/pce.12954
  • Martin CE (1994) Physiological ecology of the Bromeliaceae. Botanical Review 60: 1-82.
  • Martinelli G, Vieira CM, Gonzalez M, Leitman P, Piratininga A, Costa A F & Forzza RC (2008) Bromeliaceae da Mata Atlântica brasileira: lista de espécies, distribuição e conservação. Rodriguésia 59: 209-258
  • Martins JPR, Martins AD, Pires MF, Junior RAB, Reis RO, Dias GDMG & Pasqual M (2016) Anatomical and physiological responses of Billbergia zebrina (Bromeliaceae) to copper excess in a controlled microenvironment. Plant, Cell, Tissue and Organ Culture 126: 43-57.
  • Monteiro RF, Forzza RC & Mantovani A (2011) Leaf structure of Bromelia and its significance for the evolution of Bromelioideae (Bromeliaceae). Plant Systematycs and Evolution 293: 53-64.
  • Moreira ASFP, Lemos-Filho JP, Zotz G & Isaias RMS (2009) Anatomy and photosynthetic parameters of roots and leaves of two shade-adapted orchids, Dichaea cogniauxiana Shltr. and epidendrum secundum Jacq. Flora 204: 604-611
  • Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladares F & van Kleunen M (2010) Plant phenotypic plasticity in a changing climate. Trends in Plant Science 15: 684-692.
  • Parkhurst DF & Loucks OL (1972) Optimal leaf size in relation to environment. Journal of Ecology 60: 505-537.
  • Parrilla-Diaz AT & Ackerman JD (1990) Epiphyte roots: anatomical correlates to environmental parameters in Puerto Rico orchids. Orquidea (Mex.) 12: 105-116.
  • Pereira TAR, da Silva LC, Azevedo AA, Francino DMT, Coser TS & Pereira JD (2013) Leaf morpho-anatomical variations in Billbergia elegans and Neoregelia mucugensis (Bromeliaceae) exposed to low and high solar radiation. Botany 91: 327-334.
  • Pereira TAR, Oliveira TS, Silva LC & Azevedo AA (2011) Comparative leaf anatomy of four species of Bromelioideae (Bromeliaceae) occurring in the Atlantic Forest, Brazil. Botany 89: 243-253.
  • Pérez-Harguindeguy N, Díaz S, Garnier E , Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, De Vos AC, Buchmann N, Funes G, Quétier F, Hodgson JG, Thompson K, Morgan HD, Ter Steege H, van der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti MV, Conti G, Staver AC, Aquino S & Cornelissen JHC (2013) New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61: 167-234.
  • Proença SL & Sajo MG (2007) Anatomia foliar de bromélias ocorrentes em áreas de Cerrado do estado de São Paulo, Brasil. Acta Botanica Brasilica 21: 657-673.
  • Proença SL & Sajo MG (2008) Rhizome and root anatomy of 14 species of Bromeliaceae. Rodriguésia 59: 113-128.
  • Rada F & Jaimez R (1992) Comparative ecophysiology and anatomy of terrestrial and epiphytic Anthurium bredemeyeri Schott in a Tropical Andean Cloud Forest. Journal of Experimental Botany 43: 723-727.
  • Reinert F (1998) Epiphytes: photosynthesis, water balance and nutrients. Oecologia Brasiliensis 4: 87-108.
  • Sanford WW & Adanlawo I (1973) Velamen and exodermis characters of West African epiphytic orchids in relation to taxonomic grouping and habitat tolerance. Botanical Journal of the Linnean Society 66: 307-321.
  • Sass JE (1951) Botanical Microtechnique. 2nd ed. Ames, The Iowa State College Press, Iowa. 228p.
  • Scarano FR, Duarte HM, Rôças G, Barreto SMB, Amado EF, Reinert F, Wendt T , Mantovani A , Lima HRP & Barros CF (2002) Acclimation or stress symptom? An integrated study of intraspecific variation in the clonal plant Aechmea bromeliifolia, a widespread CAM tank- bromeliad. Botanical Journal of the Linnean Society 140: 391-401.
  • Segecin S & Scatena VL (2004) Morfoanatomia de rizomas e raízes de Tillandsia L. (Bromeliaceae) dos Campos Gerais, PR. Acta Botânica Brasilica 18: 253-260.
  • Silva IV & Scatena VL (2011) Anatomia de raízes de nove espécies de Bromeliaceae (Poales) da região amazônica do estado de Mato Grosso, Brasil. Acta Botânica Brasilica 25: 618-627.
  • Souza RP, Machado EC, Silva JAB, Lagôa AMMA & Silveira JAG (2004) Photosynthetic gas exchange, chlorophyll fluorescence and some associated metabolic changes in cowpea (Vigna unguiculata) during water stress and recovery. Environmental and Experimental Botany 51: 45-56.
  • Statsoft Inc. (2006) Statistica (data analysis software system), version 10.0. Available at <http://www.statsoft.com/Products/STATISTICA-Features> Access on 16 July 2017.
    » http://www.statsoft.com/Products/STATISTICA-Features
  • Ting TP, Hann J, Holbrook NM , Putz FE , Sternberg LSL, Price D & Goldstein G (1987) Photosynthesis in hemiepiphytic species of Clusia and Ficus. Oecologia 74: 339-346.
  • Tomlinson PB (1969) Commelinales - Zingiberales. In: Metcalf CR (ed.) Anatomy of the monocotyledons. Vol. 3. Anatomy of the monocotyledons. Oxford Clarendon Press, London. Pp. 193-294.
  • Violle C, Navas M-L, Vile D, Kazakou E, Fortunel C, Hummel I & Garnier E (2007) Let the concept of trait be functional! Oikos 116: 882-892.
  • Voltolini CH & Santos M (2011) Variações na morfoanatomia foliar de Aechmea lindenii (E. Morren) Baker var. lindenii (Bromeliaceae) sob distintas condições ambientais. Acta Botanica Brasilica 25: 2-10.
  • Wilson CKL, Pusey PL & Otto BE (1981) Plant epidermal sections and imprints using cyanoacrylate adhesives. Canadian Journal of Plant Science 61: 781-783.
  • Zotz G (2013) The systematic distribution of vascular epiphytes - a critical update. Botanical Journal of the Linnean Society 171: 453-481.
  • Zotz G & Winkler U (2013) Aerial roots of epiphytic orchids: velamen radicum and its role in water and nutrient uptake. Oecologia 171: 733-74.

Publication Dates

  • Publication in this collection
    20 Dec 2019
  • Date of issue
    2019

History

  • Received
    15 Feb 2018
  • Accepted
    30 July 2018
Instituto de Pesquisas Jardim Botânico do Rio de Janeiro Rua Pacheco Leão, 915 - Jardim Botânico, 22460-030 Rio de Janeiro, RJ, Brasil, Tel.: (55 21)3204-2148, Fax: (55 21) 3204-2071 - Rio de Janeiro - RJ - Brazil
E-mail: rodriguesia@jbrj.gov.br