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Morphophysiological Plasticity in Epiphytic Research Article Tropical Conservation Science Voume 11: 1–10 Morphophysiological Plasticity in Epiphytic ! The Author(s) 2018 Reprints and permissions: Bromeliads Across a Precipitation Gradient sagepub.com/journalsPermissions.nav DOI: 10.1177/1940082918781926 in the Yucatan Peninsula, Mexico journals.sagepub.com/home/trc Manuel Jesu´s Cach-Pe´rez1,2,3, Jose´ Luis Andrade2, and Casandra Reyes-Garcı´a2 Abstract Plasticity may be a key factor to determine plant survival under a changing environment as a result of climate change or land use modification. Plasticity in physiological and morphological traits was evaluated in seven epiphytic Tillandsia species (Bromeliaceae) from six vegetation communities along a precipitation gradient in the Yucatan Peninsula, Mexico. Microenvironmental conditions (air temperature and humidity, light, and vapor pressure deficit), as well as Á titratable acidity, osmotic potential, relative water content, and succulence were characterized during wet, early dry, and dry seasons. We calculated the relative distances plasticity index using physiological data from the wet and dry seasons; morphological plasticity was also calculated for foliar trichome and stomatal traits from previously published data. We found high variation in microenvironmental conditions between seasons, particularly for the tropical dry deciduous forest. The dry season had a negative effect in all physiological variables (decrease from 40% to 59% for Á titratable acidity and 10% to 38% for relative water content). The highest plasticity was registered for T. balbisiana (physiological: 0.29, anatomical: 0.18) and the lowest for T. fasciculata and T. yucatana. Nonmetric multidimensional scaling analysis separated individuals distributed in the wettest vegetation types from those distributed in the driest vegetation types, irrespective of the species, showing convergent physiological strategies to confront environmental variation. We found higher plasticity in water use traits in atmospheric species, compared to tanks and higher plasticity in general in species with wide distribution compared to those with small distribution ranges. Keywords Bromeliaceae, photosynthesis, seasonality, Tillandsia, water relations Introduction distribution, due to their exposition to a wide range of environmental heterogeneity (Chaves, Leal, & Lemos- Plasticity can be defined as the ability of an organism to Filho, 2018; Sultan, 2001; Valladares et al., 2006). adjust its performance through changes in its morphology or its physiology in response to changes in environ- mental conditions (Navas & Garnier, 2002; Pigliucci, 1CONACYT—Departamento de Agricultura Sociedad y Ambiente, 2005; Valladares, Sanchez-Gomez, & Zavala, 2006; El Colegio de la Frontera Sur Unidad Villahermosa, Villahermosa, Tabasco, Valladares, Wright, Lasso, Kitajima, & Pearcy, 2000). Mexico 2 This response of individuals (plasticity) to environmental Unidad de Recursos Naturales, Centro de Investigacio´n Cientı´fica de Yucata´n, A.C., Me´rida, Yucata´n, Mexico changes influences their distribution and can contribute 3Laboratorio Nacional de Innovacio´n Ecotecnolo´gica para la Sustentabilidad, to plant fitness (Sultan, 2001). The calculation of a plas- Villahermosa, Tabasco, Mexico ticity index may be a way to measure the magnitude of Received 16 February 2018; Revised 8 May 2018; Accepted 9 May 2018 these physiological and morphological changes, which can help to understand the strategies followed by plants Corresponding Author: Casandra Reyes-Garcı´a, Unidad de Recursos Naturales, Centro de to cope with environmental variations. It has been Investigacio´n Cientı´fica de Yucata´n, A.C., Calle 43, No. 130, Col. Chuburna proposed that species with wide distribution will show de Hidalgo, C.P. 97205 Me´rida, Yucata´n, Me´xico. larger phenotypical plasticity than species with restricted Email: [email protected] Creative Commons Non Commercial CC BY-NC: This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License (http://www.creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage). 2 Tropical Conservation Science There is an increasing interest in plant plasticity given the performed with epiphytic bromeliad species growing urgency to predict the response of species to climate along environmental gradients (Cach-Pe´rez, Andrade, & change (Potvin & Tousignant, 1996; Rehfeldt, Wykoff, Reyes-Garcı´a, 2014; Griffiths & Maxwell, 1999; Griffiths & Ying, 2001). This would be important, for example, & Smith, 1983) and none of these have focused in char- if we consider that changes on species distribution acterizing plasticity, which can help predict possible under climate change are projected using correlations responses to climate change and possible impacts in the on bioclimatic models that can overestimate species different vegetation types where these species can be loss, because some key aspects can be ignored, such as found. plasticity (Hampe, 2004; Thuiller et al., 2005). The aim of this study was to determine the plasticity of The epiphytic habitat can be considered extreme due seven epiphytic bromeliads to variation in environmental to high environmental variability. The absence of roots in conditions within six contrasting vegetation types of the the soil make epiphytes dependent on atmospheric pre- Yucatan Peninsula, Mexico, along a precipitation gradi- cipitation (rain, dew, and fog) to acquire water and nutri- ent (from 500 to about 1,500 mm yÀ1). We expected that ents and highly sensitive to air humidity in order to species with a wider distribution, and located at the drier, maintain water balance (Benzing, 1990; Einzmann & more seasonal northwestern region of the Peninsula Zotz, 2016). Epiphytes have developed adaptations such would show higher plasticity compared with species as poikilohydry, leaf, stem, and root succulence, and cras- with limited distribution. We also expected tank species sulacean acid metabolism (CAM) to cope with variability to be less plastic than atmospheric species. We character- in water supply (Ng & Hew, 2000; Zotz & Hietz, 2001). In ized seasonal variations in physiological traits (Á titrat- the family Bromeliaceae in addition to CAM photosyn- able acidity, leaf relative water content [RWC], leaf thesis and succulent tissues, epiphytic species have foliar osmotic potential, and leaf succulence) under field condi- trichomes specialized in the absorption of water and tions and used published data on morphological traits nutrients and may also exhibit water reservoirs at the to obtain physiological and morphological plasticity base of its leaves (Benzing, 1990; Chaves, Leal, & de indexes. Lemos-Filho, 2015; Freschi et al., 2010; Kleingesinds et al., 2018; Martin, 1994). Regarding these traits, epi- phytic bromeliads have been classified in two main life Methods forms: atmospheric species (with lingulate to narrowly Field Sites triangular leaves, densely covered by trichomes) and tank species (with long and wide leaves that form a Measurements were performed for seven epiphytic bro- water reservoir in the center of the rosette; Benzing, meliad species from six contrasting vegetation types, 1980). These morphological differences have been which follow a precipitation gradient in the Yucatan linked to physiological strategies, as tank species main- Peninsula (Mexico; Figure 1): coastal sand dune scrub tain a more constant water source that partly isolates (2119 N, 8926 W; 500 mm mean annual precipitation), them from surrounding environmental conditions, the scrub and peten mangrove (2051 N, 9022 W; 675 mm seasonal variation in water and light use may be more mean annual precipitation), deciduous forest (2105 N, conservative, compared to the atmospheric species 8935 W; 900 mm mean annual precipitation), semidecid- (Kleingesinds et al., 2018; Reyes-Garcı´a, Mejia-Chang, uous forest (2005 N, 8932 W; 1,150 mm mean annual & Griffiths, 2012). These adaptations have allowed bro- precipitation), and semievergreen forest (1806 N, meliads to colonize habitats in a wide range of environ- 8948 W; 1,500 mm mean annual precipitation); the sites ments, from moist montane forests, coastal deserts, and are described in detail in Cach-Pe´rez et al. (2013). Andean paramos (Benzing, 2000). Several studies have demonstrated the high sensitivity Studied Species of epiphytic bromeliads to environmental changes (Andrade, 2003; Chilpa-Galva´n, Tamayo-Chim, For the physiological measurements, we selected seven Andrade, & Reyes-Garcı´a, 2013; De Sousa & Colpo, species of the 15 reported by Cach-Pe´rez et al. (2013) 2017; Graham & Andrade, 2004; Nowak & Martin, according to their distribution, abundance, and import- 1997; Reyes-Garcı´a & Griffiths, 2009; Reyes-Garcı´a, ance value index within each vegetation type. At each Griffiths, Rinco´n, & Huante, 2008; Reyes-Garcı´a, site, we surveyed a tank and an atmospheric species, in Mejı´a-Chang, Jones, & Griffiths, 2008; Valdez- order to contrast the strategies, except for the peten man- Herna´ndez, Gonza´lez-Salvatierra, Reyes-Garcı´a, grove where Tillandsia streptophylla Scheidw. was the Jackson, & Andrade, 2015; Zotz & Asshoff, 2010). only abundant species. The selected species were However, these studies have been carried out with par- Tillandsia brachycaulos Schltdl.,
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