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Bianca Butter Zorger1,3, Hiulana Pereira Arrivabene1 & Camilla Rodriguésia 70: e00592018. 2019 http://rodriguesia.jbrj.gov.br DOI: http://dx.doi.org/10.1590/2175-7860201970091 Original Paper Adaptive morphoanatomy and ecophysiology of Billbergia euphemiae, a hemiepiphyte Bromeliaceae Bianca Butter Zorger1,3, Hiulana Pereira Arrivabene1 & Camilla Rozindo Dias Milanez1,2 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. 1 Universidade Federal do Espírito Santo, Centro de Ciências Humanas e Naturais, Depto. Ciências Biológicas, Av. Fernando Ferrari 514, Goiabeira, 29075-910, Vitória, ES, Brazil. 2 ORCID: <https://orcid.org/0000-0002-9516-2031> 3 Author for correspondence: [email protected] 2 de 10 Zorger BB, Arrivabene HP & Milanez CRD Introduction (Crayn et al. 2004). Such adaptations probably enabled these individuals to occupy a wide Habitats under distinct selective pressures range of habitats, like those with low water and exert adaptative pressures that can lead individuals nutrients availability (Martin 1994), specially in of the same species to present different life Bromelioideae subfamily. This is one of eight strategies for their survival (Bradshaw 1965; subfamily of Bromeliaceae (Givnish et al. 2011; Ackerly 2003; Nicotra et al. 2010). Hemiepiphytes Goetze et al. 2016), with more of 500 species are known for being epiphytes that show a phase occurring in phytophysiognomies of Atlantic of life associated to the ground (Kress 1986). Forest (Martinelli et al. 2008). They can be classified as primary hemiepiphytes Billbergia euphemiae E. Morren, is a when individuals start their lives as epiphytes and secondary hemiepiphyte (Kress 1986; Granados- extend the roots to the ground, or as secondary Sánchez et al. 2003), native of Brazil, which hemiepiphytes, when individuals germinate in belongs to Bromelioideae subfamily (Bromelieae ground and adhere themselves on phorophytes tribe) (BFG 2018). Such species occur normally through propagation stolons (Granados-Sánchez in Atlantic Forest, including montane and et al. 2003). These plants exhibit contrasting submontane phytophysiognomies (Fontoura ecological strategies according to different phases 1991), and is typical of restinga areas (Magnago of life (Holbrook & Putz 1996a; Granados- et al. 2007). Its distribution is submitted to the Sánchez et al. 2003), which can be described influence of environmental factors variations, by variations of anatomical, morphological and such as luminosity, humidity, availability of physiological traits (Violle et al. 2007). nutrients in ground and salinity, as well as In the past decades, many studies shown biological factors, like reproduction and seed morphology and ecophysiology differences in dispersion (Lüttge 2008). Overall, leaf anatomy epiphytic and terrestrial species in relation to of Billbergia euphemiae include an uniseriate environment (edaphic, luminosity, moisture) and lignified epidermis with reduced lumen, (Parrilla-Diaz & Ackerman 1990; Rada & cutinized. The stomata are in the same level Jaimez 1992; Scarano et al. 2002), biotic factors of epidermis on abaxial surface of leaves and (Lawton & Williams-Linera 1996) and evolution arranged in longitudinal rows. Peltate scales (Benzing 2000) in different vegetative organs cover all surface in both surface of the epidermis, (Moreira et al. 2009). Although the epiphytism and disc cells do not differ from wing cells and has received general attention in literature, still have round shaped. This specie has water storage few studies have explored adaptive strategies in parenchyma, and subjacent, chlorenchyma with hemiepiphytes (Ting et al. 1987; Holbrook & aeration channels and collateral vascular bundles Putz 1996b). In addition, among such studies in single series in the lower half of the leaf blade much are restricts to genus Ficus sp. (Holbrook (Pereira et al. 2011). & Putz 1996b), still being unclear functional In this context, understanding anatomy, and ecological consequences of hemiepiphytism morphology and physiology of hemiepiphytes when take into account species belonging to other is important for knowing how these plants botanic family, as Bromeliaceae. behave according to environmental conditions Epiphytes consist in a representative in different phases of life. Moreover, this study group in Bromeliaceae family, an ecologically allow to complement a big range of studies that diverse family, exhibiting high species richness hemiepiphytes anatomy focused on taxonomy among vascular plants in the neotropics (Kress (Aoyama & Sajo 2003; Ferreira et al. 2007; 1986; Zotz 2013), having estimated 3,352 Monteiro et al. 2011; Zotz 2013) and ecology species belonging to 58 genus (Luther 2012). of Bromeliaceae (Dickison 2000; Bonnet & Furthermore, Bromeliaceae is a group known Queiroz 2006; Voltolini & Santos 2011; Males for having several adaptations to limiting & Griffiths 2017). In this context, the aim of this conditions (Benzing 2000). Some examples of study was to investigate adaptive strategies of those adaptations are presence of epidermal B. euphemiae, in both terrestrial and epiphytic scales (Segecin & Scatena 2004; Proença phases. Our hypothesis is that in epiphytic phase & Sajo 2007; Pereira et al. 2013), velamen there are more traits related to high incidence of (Benzing 2000; Proença & Sajo 2008) and CAM light and to water retention, once the roots are metabolism (Crassulacean Acid Metabolism) not into the ground. Rodriguésia 70: e00592018. 2019 Morphoanatomy and ecophysiology of Billbergia euphemiae 3 de 10 Material and Methods (Pérez-Harguindeguy et al. 2013). Length, width Study area and height were measured by a measuring tape. The leaf area was measured using an Area Meter This study was carried out within the dry LI-COR 3100 (Lincoln, USA). To obtain dry mass, forest formation of restinga located at Paulo César leaves were weight after collecting them. As for Vinha State Park, a coastal plain of nearly 1,500 dry mass, samples were weight after drying in the ha in Espírito Santo state, Brazil (20o33’–20o38’S, oven at 60 oC until obtain constant mass (Garnier 40o23’–40o26’W). Weather of region is Aw type according to Köppen classification (1948), with et al. 2001). annual temperature averaging 23.3o, annual rainfall of 1,307 mm and relative humidity of 80%. Such Determination of leaf angle o climate is characterized by existence of rainy We measured leaf angle ( ) in relation to the summers and dry winters (Fabris 1995). ground in one leaf from each individual, totalling five measurements, using a clinometer (James & Botanical material Bell 2000). There
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