Chlorophyll fluorescence varies more across seasons than leaf water potential in drought-prone plants

BRUNO H.P. ROSADO EDUARDO A. DE MATTOS About the authors

ABSTRACT

Among the effects of environmental change, the intensification of drought events is noteworthy, and tropical vegetation is predicted to be highly vulnerable to it. However, it is not clear how tropical plants in drought-prone habitats will respond to this change. In a coastal sandy plain environment, we evaluated the response of six plant species to water deficits across seasons, the relationship between their morpho-physiological traits, and which traits would be the best descriptors of plants' response to drought. Regardless of leaf succulence and phenology, responses between seasons were most strongly related to chlorophyll fluorescence. In this study we have demonstrated that a better comprehension of how tropical species from drought-prone habitats cope with changes in water availability can be based on seasonal variation in leaf water potential and chlorophyll fluorescence. Temporal variation in leaf water potential and chlorophyll fluorescence was found useful for differentiating between groups of sandy soil species that are responsive or unresponsive to water availability. However, chlorophyll fluorescence appeared to be a more sensitive descriptor of their seasonal and short-term responses.

Key words:
drought; functional traits; plant-water relations; photoinhibition; seasonal habitats

RESUMO

Entre os efeitos da mudança ambiental, a intensificação dos eventos de seca é notável e a vegetação tropical é apontada como altamente vulnerável a ela. No entanto, não está claro como plantas tropicais em habitats propensos à seca responderão a essa mudança. Em um ambiente de planície costeira arenosa, avaliamos a resposta de seis espécies vegetais à deficit de água ao longo das estações, a relação entre as suas características morfo-fisiológicas, e quais características seriam as melhores descritoras de resposta das plantas à seca. Independentemente de suculência foliar e fenologia, respostas entre as estações foram mais fortemente relacionadas a fluorescência da clorofila. Neste estudo demonstramos que a melhor compreensão de como espécies tropicais de habitats propensos a seca lidam com mudanças na disponibilidade de água pode ser baseada na variação sazonal de potencial hídrico e fluorescência da clorofila. Esta variação temporal de potencial hídrico e fluorescência da clorofila foram úteis para diferenciar grupos de espécies que são responsivas ou não responsivas à disponibilidade de água. Ressalta-se que a fluorescência da clorofila foi o descritor mais sensível de respostas das espécies tanto em termos sazonais quanto em curto prazo.

Palavras-chave:
seca; característica funcional; relações hídricas em plantas; fotoinibição; habitats sazonais

INTRODUCTION

In the current scenario of large-scale environmental change, the search for functional traits which will allow us to predict the response of communities and species to changes in conditions and resources has been identified as one of the 100 fundamental questions in ecology (Sutherland et al. 2013Sutherland WJ et al. 2013. Identification of 100 funda­mental ecological questions. J Ecol 101: 58-67.). Among the effects of environmental change, the intensification of drought events is noteworthy (McDowell et al. 2008McDowell N et al. 2008. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol178: 719-739., 2011McDowell NG, Beerling DJ, Breshears DD, Fisher RA, Raffa KF and Stitt M. 2011. The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol Evol (Personal edition) 26: 523-532.), and several studies have identified plant physiological traits that may be descriptors for the responses of plants to water availability (Bartlett et al. 2012Bartlett MK, Scoffoni C and Sack L. 2012. The deter­minants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis. Ecol Lett 15: 393-405., Choat et al. 2012Choat B et al. 2012. Global convergence in the vulnerability of forests to drought. Nature 491: 752-755., Bhaskar and Ackerly 2006Bhaskar R and Ackerly D. 2006. Ecological relevance of minimum seasonal water potential. Physiol Plantarum 127: 353-359.). In tropical environments seasonality is largely reflected in changes in water availability (Franco 2002Franco AC. 2002. Ecophysiology of Woody Plants. In: Oliveira PS and Marques RJ (Eds), The Cerrados of Brazil - Ecology and Natural History of Neotropical Savanna, NY: Columbia Univ. Press, p. 388.), and temporal fluctuations in water availability are particularly important for plants growing in sandy environments, due to the low water retention capacity of sandy soils (Noy-Meir 1972Noy-Meir I. 1972. Desert ecosystems: environment and producers. Ann Rev Ecol Syst 4: 25-51.). Although several studies of plant responses to drought in tropical dry forests and savannas have been published (Bucci et al. 2005Bucci SJ, Goldstein G, Meinzer FC, Franco AC, Campanello P and Scholz FG. 2005. Mechanisms contributing to seasonal homeostasis of minimum leaf water potential and predawn disequilibrium between soil and plant water potential in Neotropical savanna trees. Trees 19: 296-304., Franco 2002Franco AC. 2002. Ecophysiology of Woody Plants. In: Oliveira PS and Marques RJ (Eds), The Cerrados of Brazil - Ecology and Natural History of Neotropical Savanna, NY: Columbia Univ. Press, p. 388., Choat et al. 2006Choat B, Ball MC, Luly JG, Donnelly CF and Holtum JAM. 2006. Seasonal patterns of leaf gas exchange and water relations in dry rain forest trees of contrasting leaf phenology. Tree Physiol 26: 657-664., Méndez-Alonzo et al. 2012Méndez-Alonzo R, Paz H, Zuluaga RC, Rosell JA and Olson ME. 2012. Coordinated evolution of leaf and stem economics in tropical dry forest trees. Ecology 93: 2397-2406.), it is still unknown how tropical plants in other tropical drought-prone habitats (e.g. coastal sandy plains) will respond to drought, and which are the best traits for predicting this response.

Plants growing on sandy soils show higher water potential than those growing on clay soils, since sandy soils hold water at high water potential (Sperry et al. 2002Sperry JS, Hacke UG, Oren R and Comstock JP. 2002. Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ25: 251-263.). One important process that facilitates highly conservative water use is homeostasis of leaf water potential (ΨL) at midday across seasons (Bucci et al. 2005Bucci SJ, Goldstein G, Meinzer FC, Franco AC, Campanello P and Scholz FG. 2005. Mechanisms contributing to seasonal homeostasis of minimum leaf water potential and predawn disequilibrium between soil and plant water potential in Neotropical savanna trees. Trees 19: 296-304., Maseda and Fernández 2006Maseda PH and Fernández RJ. 2006. Stay wet or else: three ways in which plants can adjust hydraulically to their environment. J Exp Bot 57: 3963-3977.). The ability to maintain constant ΨL might be achieved by mechanisms such as greater stomatal control and hydraulic adjustments, which reduce transpiration (Maseda and Fernández 2006Maseda PH and Fernández RJ. 2006. Stay wet or else: three ways in which plants can adjust hydraulically to their environment. J Exp Bot 57: 3963-3977.). Species with less stomatal control may exhibit greater decreases in ΨL (Franks et al. 2007Franks PJ, Drake PL and Froend RH. 2007. Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance. Plant Cell Environ 30: 19-30., Maseda and Fernández 2006Maseda PH and Fernández RJ. 2006. Stay wet or else: three ways in which plants can adjust hydraulically to their environment. J Exp Bot 57: 3963-3977.). An important aspect of species that are able to maintain high ΨL is related to the avoidance of embolism (Sperry et al. 2002Sperry JS, Hacke UG, Oren R and Comstock JP. 2002. Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ25: 251-263., Maseda and Fernández 2006Maseda PH and Fernández RJ. 2006. Stay wet or else: three ways in which plants can adjust hydraulically to their environment. J Exp Bot 57: 3963-3977.). However, species with lower ΨL can maintain CO2 gas exchange for longer periods during drought, under low soil water availability and/or high air vapor pressure deficit (VPD). On the other hand, such species might be more susceptible to water loss (Maseda and Fernández 2006Maseda PH and Fernández RJ. 2006. Stay wet or else: three ways in which plants can adjust hydraulically to their environment. J Exp Bot 57: 3963-3977.). Importantly, the greater the degree of stomatal closure (associated with high ΨL), the dissipation of excitation energy by photosynthetic carbon assimilation will be more reduced (Maseda and Fernández 2006Maseda PH and Fernández RJ. 2006. Stay wet or else: three ways in which plants can adjust hydraulically to their environment. J Exp Bot 57: 3963-3977.). In addition, greater stomatal closure may result in an increase in carbon starvation due to a decrease in photosynthesis (McDowell et al. 2008McDowell N et al. 2008. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol178: 719-739., van der Molen et al. 2011Van Der Molen MK et al. 2011. Drought and ecosystem carbon cycling. Agr Forest Meteorol 151: 765-773.).

A further drawback of stomatal closure is that it may lead to light stress, i.e., photoinhibition caused by excess light that is not used in photosynthesis. Changes in the ratio of the yield of variable (Fv) and maximum (Fm) chlorophyll fluorescence in dark-acclimated leaves can be used to characterize the degree of photoinhibition in plants subjected to environmental stress (Baker 2008Baker NR. 2008. Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo. Annu Rev Plant Biol 59: 89-113.). A decrease in the Fv/Fm ratio indicates increased photoprotection, in which excess excitation energy is dissipated as heat, and to direct photodamage to photosystem II (PS II) centers (Krause 1988Krause GH. 1988. Photoinhibition of photosynthesis. An eva­luation of damaging and protective mechanisms. Phy­siol Plantarum 74: 566-574., Walker 1992Walker D. 1992. Excited leaves. New Phytol121: 325-345.). In addition, an increase in thermal dissipation in PS II is associated with a decrease in Fm and minimum chlorophyll fluorescence (F0), whereas damage to the reaction centers increases only F0 (Krause 1988Krause GH. 1988. Photoinhibition of photosynthesis. An eva­luation of damaging and protective mechanisms. Phy­siol Plantarum 74: 566-574., Porcar-Castell et al. 2008Porcar-Castell A, Juurola E, Nikinmaa E, Berninger F, Ensminger I and Hari P. 2008. Seasonal acclimation of photosystem II in Pinus sylvestris. I. Estimating the rate constants of sustained thermal energy dissipation and photochemistry. Tree Physiol28: 1475-1482.).

Rosado and de Mattos (2010Rosado BHP and DeMattos EA. 2010. Interspecific variation of functional traits in a CAM-tree dominated sandy coastal plain. J Veg Sci 21: 43-54.) observed varia­tions between wet and dry seasons in the pressure-volume relationship in species on the Brazilian coastal sandy plains, a species assemblage known as restingas. As expected for plants growing on dry sandy soils, they observed high values of ΨL at the turgor loss point (ΨTLP), less negative osmotic pressure, and a low bulk modulus of elasticity in restinga species (Rosado and de Mattos 2010Rosado BHP and DeMattos EA. 2010. Interspecific variation of functional traits in a CAM-tree dominated sandy coastal plain. J Veg Sci 21: 43-54.). However, most species have an average predawn Fv/Fm of less than 0.83 during the dry season, which indicates chronic photoinhibition. To date, how­ever, no information is available about the physiologi­cal responses of restinga plants to seasonal variation in water availability, or the possible relationship between such physiological responses and leaf phenology.

In this study we chose the two dominant species, which are able to maintain a high minimum ΨL during the dry season (Rosado and de Mattos 2010Rosado BHP and DeMattos EA. 2010. Interspecific variation of functional traits in a CAM-tree dominated sandy coastal plain. J Veg Sci 21: 43-54.), and four less dominant restinga species. These six species occur in a restinga in southeastern Brazil and exhibit a range of leaf succulence, from 147 to 1105 g m-2, and leaf phenology characteristics, from successive to concentrated leaf production in wet seasons (Rosado and de Mattos 2007Rosado BHP and DeMattos EA. 2007. Variação temporal de características morfológicas de folhas em dez espécies do Parque Nacional da Restinga de Jurubatiba, Macaé, RJ, Brasil. Acta Bot Bras 21: 741-752., 2010Rosado BHP and DeMattos EA. 2010. Interspecific variation of functional traits in a CAM-tree dominated sandy coastal plain. J Veg Sci 21: 43-54.). Leaf succulence reflects the amount of water stored in leaves and may act as a buffer for water loss (Lamont and Lamont 2000Lamont B and Lamont H. 2000. Utilizable water in leaves of 8 arid species as derived from pressure-volume curves and chlorophyll fluorescence. Physiol Plantarum110: 64-71.), and variations in leaf phenology are commonly associated with the ability to deal with water deficits (Reich and Borchert 1982Reich P and Borchert R. 1982. Phenology and ecophys­iology of tropical tree, Tabebuia neochrysantha (Bigno­niaceae). Ecology 63: 294-299., Borchert 1994Borchert R. 1994. Soil and stem water storage determine phenology and distribution of tropical dry forests trees. Ecology 75: 1437-1449.). We thus addressed the following hypotheses: 1) the six species have different strategies to maintain high ΨL across seasons based on distinct arrays of leaf phenology and leaf morpho-physiological traits; 2) seasonal responses of chlorophyll fluorescence are dependent on seasonal variation in ΨL and both ΨL and chlorophyll fluorescence are redundant in the description of species' seasonal responses to water availability. Although soil moisture availability is a function of input minus output of water and rooting depth, the number of rainless days (NRD) might be a useful surrogate for soil moisture availability, especially in sandy soils whose water retention capacity is low (Sperry et al. 2002Sperry JS, Hacke UG, Oren R and Comstock JP. 2002. Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ25: 251-263.). Given the low water retention capacity of sandy soils and the occurrence of dry spells in both wet and dry seasons (Cavalin and de Mattos 2007Cavalin PO and DeMattos EA. 2007. Spatio-temporal var­iation of photosynthetic pigments in the CAM tree Clusia hilariana Schlechtendal associated with dry spells during the rainy season in southeastern Brazil. Trees 21: 671-675.), coastal sandy plants may be differentially predisposed to water shortage during rainless days with varying VPD during wet and dry seasons. Our third hypothesis is therefore as follows: ΨL responds to higher VPD only when NRD is low, but responds to an increase in NRD, regardless of VPD.

MATERIALS AND METHODS

Study Area and Plant Species

Our study was conducted in the Restinga of Jurubatiba National Park, (14 140 ha), located in the northern part of the state of Rio de Janeiro, Brazil (extending north-south between 22º00'S and 22º23'S and east-west between 41º15'W and 41º35'W). The maximum temperature (around 30 °C) occurs in January and the minimum (around 20 °C) in July (Henriques et al. 1986Henriques RPB, Araujo DSD and Hay JD. 1986. Des­crição e classificação dos tipos de vegetação da restinga de Carapebús, Rio de Janeiro. Rev Bras Bot 9: 173-189.). The mean annual temperature is 22.6 ºC. The sandy soil is characterized by low water retention capacity, low nutrient content and low organic matter content. Average annual rainfall is 1100-1300 mm, with a monthly minimum of 41 mm in dry seasons and a monthly maximum of 189 mm in wet seasons (Araujo et al. 1998Araujo DSD, Scarano FR, Sá CFC, Kurtz BC, Zaluar HLT, Montezuma RCM and Oliveira RC. 1998. Comunidades vegetais do Parque Nacional da Restinga de Jurubatiba. In: Esteves FA (Ed), Ecologia das Lagoas Costeiras do Parque Nacional da Restinga de Jurubatiba e do Município de Macaé (RJ), Rio de Janeiro: NUPEM-UFRJ, p. 39-62.). The soil water deficit is highest during the months of July and August (Henriques et al. 1986Henriques RPB, Araujo DSD and Hay JD. 1986. Des­crição e classificação dos tipos de vegetação da restinga de Carapebús, Rio de Janeiro. Rev Bras Bot 9: 173-189.). Open Clusia scrub is the most common vegetation type, characterized by vegetation patches composed of shrubs and trees 0.5-8.0 m in height, surrounded by white bare sand that can reach 70 ºC on typical summer days. Clusia scrub covers 40% of the park and is dominated by two species: Clusia hilariana Schltdl. (Clusiaceae) and Protium icicariba (DC.) Marchand (Burseraceae) (Araujo et al. 2004Araujo DSD, Pereira MCA and Pimentel M. 2004. Flora e estrutura de comunidades na Restinga de Jurubatiba - Síntese dos conhecimentos com enfoque especial para a Formação Aberta de Clusia. In: Rocha CFD, Esteves FA and Scarano FR (Eds), Pesquisas de longa duração na restinga de Jurubatiba Ecologia, história natural e conservação, São Carlos: RiMa Editora, p. 59-76.). The annual rainfall in 2004 and 2005 was 1319 mm and 1388 mm, respectively. In the months studied, cumulative rainfall was 246 mm in 2004 and 770 mm in 2005, with September 2004 and August 2005 receiving the lowest rainfall (Fig. 1). The rainless period in September 2004 was 30 days long, whereas in August 2005 it lasted 15 days.

Figure 1
Daily rainfall (mm) during the period of study. The dashed lines indicated by black circles represent the months in which ΨL and chlorophyll a fluorescence were measured.

We selected six shrub species based on varia­tion in leaf succulence and phenology (Rosado and de Mattos 2007Rosado BHP and DeMattos EA. 2007. Variação temporal de características morfológicas de folhas em dez espécies do Parque Nacional da Restinga de Jurubatiba, Macaé, RJ, Brasil. Acta Bot Bras 21: 741-752.) in an area 300 m from the ocean: Clusia hilariana (average leaf succulence: 1105 g m -2) and Byrsonima sericea DC. (Malpighiaceae) (239 g m -2) are classified as successive leaf producers because they produce leaves throughout the year, while Protium icicariba (147 g m -2), Ocotea notata (Nees) Mez (Lauraceae) (169 g m -2), Eugenia umbelliflora Berg (Myrtaceae) (358 g m -2), and Erythroxylum ovalifolium Peyr. (Erythroxylaceae) (194 g m -2) concentrate their leaf production during the wet season. Erythroxylum is the only species that shows brevi-deciduous behavior. For simplicity, we will refer to each species by its genus name. Clusia is an obligatory CAM plant (Franco et al. 1996Franco AC, Haag-Kerwer A, Herzog B, Grams TEE, Ball E, DeMattos EA, Scarano FR, Garcia F, Mantovani A and Luttge U. 1996. The effect of light levels on daily patterns of chlorophyll fluorescence and organic acid accumulation in the tropical CAM tree Clusia hilariana. Trees 10: 359-365.), whereas all other species are C3 plants.

Leaf Water Potential and Chlorophyll Fluorescence

Leaf water potential was measured using a pres­sure chamber (Model 1000, PMS Instruments, USA) at predawn (Ψpd) and midday (Ψmd). The measurements were made using two completely exposed mature leaves from the north-facing side of the canopy of the same three individuals of each species throughout the study. For Erythroxylum measurements, samples were taken from terminal shoots because the leaves and petioles were too small to be used in the pressure chamber. When the difference in ΨL between two leaves of each individual was greater than 0.5 MPa, we measured a third leaf to estimate the average. From April 2004 to August 2005, measurements of ΨL were made during eight months chosen to represent the variation between the wet and the dry seasons. Twelve measurements were made at predawn and 18 at midday for each individual. To represent these data graphically we chose the days with the minimum values for each individual per month. The minimum values are good descriptors of species' responses to water deficits (Sperry et al. 2002Sperry JS, Hacke UG, Oren R and Comstock JP. 2002. Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ25: 251-263.) because they indicate the maximum xylem tension that a given species is able to tolerate while being able to maintain physiological activity (Bhaskar and Ackerly 2006Bhaskar R and Ackerly D. 2006. Ecological relevance of minimum seasonal water potential. Physiol Plantarum 127: 353-359.). At the same time, measurements of chlorophyll a fluorescence were performed using a pulse-amplitude modulated fluorometer with a fiber optic (FMS-2, Hansatech, UK), on the same two leaves from each individual. The fiber optic was kept at a constant distance and angle to the leaf surface using a leaf clip. The potential quantum yield of PSII, which is dependent on minimal (F0) and maximal fluorescence yield (Fm), was measured by applying a pulse of light strong enough to saturate all the PSII reaction centers after the leaf was dark-adapted for 30 min (de Mattos and Luttge 2001DeMattos EA and Luttge U. 2001. Chlorophyll fluo­rescence and organic acid oscillations during transition from CAM to C3-photosynthesis in Clusia minor L. (Clu­siaceae). Ann Bot 88: 457-463.). The Fv/Fm ratio was determined just before dawn (Fv/Fmpd) and at midday (Fv/Fmmd) by dark-adapting leaves for 30 min. Despite the usual high variability between leaves and individuals, we found it useful to use the absolute values of F0 and Fm to indicate temporal variation in photoprotec­tion or photodamage associated with stress (Porcar-Castell et al. 2008Porcar-Castell A, Juurola E, Nikinmaa E, Berninger F, Ensminger I and Hari P. 2008. Seasonal acclimation of photosystem II in Pinus sylvestris. I. Estimating the rate constants of sustained thermal energy dissipation and photochemistry. Tree Physiol28: 1475-1482.). The averages were calculated in the same way as for ΨL. On each sampling occasion we measured relative humidity and air temperature at 30 min intervals, starting at predawn and ending at midday.

Statistical Analyses

To test hypothesis 1, we evaluated the differences in Ψpd, Ψmd and Fv/Fmpd, Fv/Fmmd, and F0 and Fm between seasons and among species using a two-way repeated-measures ANOVA (P < 0.05). Ad­ditionally, to evaluate changes in the response of species (ecophysiological performance) between seasons, we constructed a correlation matrix using the mean values of each variable for each species in the wet and dry season, respectively. The wettest period comprised the months between November 2004 and February 2005. We analyzed the correlation matrix with a Principal Component Analysis (PCA) using program MULTIV (Pillar 1997Pillar VD. 1997. Multivariate exploratory analysis and rando­mization testing with MULTIV. Coenoses 12: 145-148.). We also used PCA to describe the associa­tion between ΨL and the chlorophyll variables (hypothesis 2).

To test hypothesis 3, we ran a multiple line­ar regression to determine the contribution of VPD and NRD to variation in Ψmd and Ψpd. We chose the highest VPD on each day when ΨL and Fv/Fm were measured at both predawn and midday, and NRD during the one, two, three or four weeks before the measurements were taken. We performed a separate multiple regression for each week because we used cumulative NRD. Two-way ANOVAs and multiple linear regressions were carried out in R 2.11.1 (http://www.R-project.org).

RESULTS

Leaf Water Potential

The physiological measurements from September 2004 were taken after 30 days of drought, and those from August 2005, after six days of drought (Fig. 1). The highest VPD values were observed during the dry seasons, i.e. September 2004 (46.1 Pa KPa -1) and August 2005 (36.5 Pa KPa -1) (Table I). The lowest VPD was observed on a cloudy day in July 2005 (12.3 Pa KPa -1).

The Ψpd and Ψmd values ranged from almost zero to around -1.70 MPa and from almost zero to -4.23 MPa, respectively. All species showed the greatest decline in Ψpd in September 2004 and August 2005 (Figs. 2a, 2b). In contrast to other species, Protium and Clusia showed constant values of Ψmd throughout the year, which were greater than those of other species (Tables II and III). Clusia showed a slightly lower Ψmd than Protium, but the difference was not significant. Clusia and Erythroxylum showed significantly lower values of Ψpd in the dry season in comparison to the wet season, but Erythroxylum was the only species with a significantly lower Ψmd in the dry season (Tables II and III). In July 2005, when measurements were made on a cloudy day, all species showed increases in Ψmd.

Figure 2
Seasonal variation at predawn, midday in leaf water potential (panels a and b) and chlorophyll a fluorescence (panels c and d, respectively). Species are represented as follows: closed squares - Byrsonima (■); closed triangles - Clusia (▲); closed circles -Erythroxylym (●); open squares - Eugenia (□); open diamonds - Ocotea (◊) and open circles - Protium (○).

Chlorophyll A Fluorescence

In all species, predawn and midday Fv/Fm varied in the ranges of 0.60-0.90 and 0.55-0.85, respectively. Byrsonima, Eugenia and Clusia showed a decline in Fv/Fmpd in September 2004. Eugenia had the lowest Fv/Fmpd value of all species (Table II, Fig. 2c). With the exception of Protium, all species showed a decline in Fv/Fmpd in the dry season (Tables II and III). A decline in Fv/Fmmd in all species was also observed in September 2004. Clusia and Protium showed the highest Fv/Fmmd in the wet season (0.80 and 0.79, respectively), while Eugenia showed the lowest (0.66) (Table II, Fig. 2d). The highest Fv/Fmmd values were observed for all species during July 2005. There were no significant differences between seasons for any species (Tables II and III).

The F0pd values varied from 180 to 450, with the lowest values observed in August 2005 (Fig. 3). Byrsonima, Clusia and Eugenia showed significant differences between seasons, with the highest values observed in September 2004 (Tables II and III). Eugenia showed the greatest variation in F0pd throughout the year (Fig. 3a). Fmpd varied from 800 to 2000 (Fig. 3b). With F0pd, Eugenia showed the greatest variation between seasons. Most species displayed a simultaneous marked decline in Fmpd in September 2004 and August 2005. Only Eugenia showed significant differences between seasons, with the lowest values of Fmpd measured in the dry season (Table II).

Figure 3
Seasonal variation in predawn basal (a) and maximum fluorescence yield (b) (F0pd and Fmpd respectively). Species symbols as for Figure 2.

Multiple linear regressions indicated that only NRD showed a negative relationship with Ψpd and Fv/Fmpd in Clusia, Erythroxylum and Eugenia. Both parameters were affected in Erythroxylum, while only to Ψpd or Fv/Fmpd responded to NRD in Clusia and Eugenia, respectively (Table IV). For midday measurements, only Ocotea showed a significant negative relationship between Fv/Fmmd and VPD (Table V).

The first two axes of the PCA explained 41.89% and 26.90% of the variation observed in the six traits, respectively (Table VI). The first axis was most strongly associated with Fv/Fmpd, Fmpd and F0pd. The second axis was most strongly associated with Ψpd and Ψmd. From the wet to the dry season, all species showed responses associated with the first axis of variation, being positively associated with F0pd and negatively with Fv/Fmpd, Fv/Fmmd and Fmpd. For Erythroxylum, however, the response was more closely associated with the second axis, with the response from wet to dry season being negatively related to Ψpd and Ψmd (Fig. 4).

Figure 4
PCA ordination of six species in two seasons on the basis of six traits: predawn (Ψpd) and midday leaf water potential (Ψmd), predawn (Fv/Fmpd), midday chlorophyll fluorescence (Fv/Fmmd), predawn basal (F0pd) and maximum fluorescence yield (Fmpd). Each species, in the wet and dry seasons (open and closed symbols, respectively) are represented as follows: Byrsonima (cross), Clusia (circles), Eugenia (hexagon), Erythroxylym (triangle), Protium (losangle) and Ocotea (square). Axis 1 and 2 represent 41.89% and 26.90% of total variance, respectively.

DISCUSSION

Most of the six species did not differ across seasons in their ability to maintain Ψmd. Although the dominant species, Clusia and Protium had higher values of Ψmd throughout, the other species, except for Erythroxylum, maintained similar values throughout the year, which were consistently lower than the dominant species. These values were maintained despite differences in leaf morphology and phenology. This agrees with reports indicating that the maintenance of Ψmd occurs in a series of ways, in contrast with the maintenance of constant hydraulic conductance, which occurs through changes in architectural traits such as leaf area per sapwood area (Meinzer et al. 1999Meinzer FC, Goldstein G, Franco AC, Bustamante M, Igler E, Jackson P, Caldas L and Rundel PW. 1999. Atmospheric and hydraulic limitations on transpiration in Brazilian cerrado woody species. Funct Ecol 13: 273-282., Bucci et al. 2005Bucci SJ, Goldstein G, Meinzer FC, Franco AC, Campanello P and Scholz FG. 2005. Mechanisms contributing to seasonal homeostasis of minimum leaf water potential and predawn disequilibrium between soil and plant water potential in Neotropical savanna trees. Trees 19: 296-304., Maseda and Fernández 2006Maseda PH and Fernández RJ. 2006. Stay wet or else: three ways in which plants can adjust hydraulically to their environment. J Exp Bot 57: 3963-3977., Franks et al. 2007Franks PJ, Drake PL and Froend RH. 2007. Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance. Plant Cell Environ 30: 19-30.). In Protium, for instance, the ability to maintain a higher Ψmd throughout the year might be mediated by a substantial reduction in leaf number during the dry season (Rosado and de Mattos 2010Rosado BHP and DeMattos EA. 2010. Interspecific variation of functional traits in a CAM-tree dominated sandy coastal plain. J Veg Sci 21: 43-54.). Regardless of the mechanisms involved, it is noteworthy that only the two dominant species exhibited higher and constant Ψmd, which suggests a higher safety margin for embolism (Sperry et al. 2002Sperry JS, Hacke UG, Oren R and Comstock JP. 2002. Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ25: 251-263.). Our findings support that in drought-prone habitats most species are able to maintain similar Ψmd between dry and wet seasons. However, only a small number of species are able to maintain a relatively high Ψmd, which may be an important trait related to the ability of these species to achieve dominance in sandy, drought-prone environments.

Are the Seasonal Responses of Chlorophyll Fluorescence Variables Related to the Seasonal Variation in ΨL?

Fv/Fmpd was lower in the restinga plants than the optimal value for most species, which indicates photoinhibition (Demmig-Adams and Adams 2006Demmig-Adams B and Adams WW. 2006. Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172: 11-21.). However, this was less pronounced than in plants from other harsh environments, where Fv/Fm may reach values below 0.5 (Bellot et al. 2004Bellot J, Maestre FT and Hernández N. 2004. Spatio-temporal dynamics of chlorophyll fluorescence in a semi-arid Mediterranean shrubland. J Arid Environ 58: 295-308., Zunzunegui et al. 2005Zunzunegui M, Barradas MCD, Ain-Lhout F, Clavijo A and Novo FG. 2005. To live or to survive in Doñana dunes: Adaptive responses of woody species under a Mediterranean climate. Plant Soil 273: 77-89., Ogaya et al. 2011Ogaya R, Peñuelas J, Asensio D and Llusià J. 2011. Chlorophyll fluorescence responses to temperature and water availability in two co-dominant Mediterranean shrub and tree species in a long-term field experiment simulating climate change. Environ Exp Bot 71: 123-127.). Nevertheless, there is a positive linear relationship between Fv/Fmpd and the leaf turnover rate for restinga species, which suggests that there are ecophysiological implications of even small decreases in Fv/Fmpd (Rosado and de Mattos 2010Rosado BHP and DeMattos EA. 2010. Interspecific variation of functional traits in a CAM-tree dominated sandy coastal plain. J Veg Sci 21: 43-54.). The greatest decreases in Fv/Fmpd and Fv/Fmmd occurred after a rainless period of 30 days in September 2004. These decreases were probably caused by low soil water potential and high radiation load, as observed for woody species in semi-arid Mediterranean shrubland in Spain (Bellot et al. 2004Bellot J, Maestre FT and Hernández N. 2004. Spatio-temporal dynamics of chlorophyll fluorescence in a semi-arid Mediterranean shrubland. J Arid Environ 58: 295-308.).

The reversible decline in Fv/Fm reflects the protective down-regulation of PS II, which may prevent damage to the reaction centers when there is excess excitation energy (Walker 1992Walker D. 1992. Excited leaves. New Phytol121: 325-345., Demmig-Adams and Adams 2006Demmig-Adams B and Adams WW. 2006. Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172: 11-21.). However, a comparison of changes in F0 and Fm indicates whether species are exhibiting increased thermal dissipation of excitation energy or deactivation of the PSII reaction centers (Krause 1988Krause GH. 1988. Photoinhibition of photosynthesis. An eva­luation of damaging and protective mechanisms. Phy­siol Plantarum 74: 566-574., Porcar-Castell et al. 2008Porcar-Castell A, Juurola E, Nikinmaa E, Berninger F, Ensminger I and Hari P. 2008. Seasonal acclimation of photosystem II in Pinus sylvestris. I. Estimating the rate constants of sustained thermal energy dissipation and photochemistry. Tree Physiol28: 1475-1482.). Thermal dissipation is associated with decreases in F0pd and Fmpd, as observed when the dry season of 2005 was approaching, whereas photodamage and deactivation only increase F0pd, as observed in September 2004 in most species. For Clusia, Byrsonima and Eugenia, F0pd increased to various degrees, yet always significantly during the dry season, with the highest values recorded for Eugenia. This indicates that these species were subjected to photodamage (Krause 1988Krause GH. 1988. Photoinhibition of photosynthesis. An eva­luation of damaging and protective mechanisms. Phy­siol Plantarum 74: 566-574.), as could be expected for plants exhibiting constant Ψmd, due to strong stomatal closure (McDowell et al. 2008McDowell N et al. 2008. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol178: 719-739.). Photoinhibition may have been alleviated during the cloudy day in July 2005, when all species showed the highest Fv/Fmmd. Cloudy days may also have decreased the strength of the general declining trend in F0pd throughout 2005, because the higher accumulated rainfall in 2005 (770 mm) in comparison with 2004 (246 mm) suggests that there were more cloudy days, which would reduce average light intensity.

Irrespective of leaf succulence and leaf phenology, with the exception of Erythroxylum, physiological changes of species across seasons were more strongly captured by chlorophyll fluorescence variables than to ΨL. The multivariate analysis showed that the responses of all species across seasons were positively associated with F0pd, which suggests the occurrence of photodamage during the dry season. However, the differential displacement of each species between seasons in the multivariate space indicates different degrees of susceptibility to photoinhibition, with Eugenia showing the strongest changes between seasons. The only species for which changes in fluorescence between seasons was also paralled by changes in Ψmd and Ψpd, was Erythroxylum. For Erythroxylum, the negative relationship between Ψmd and Ψpd was expected because of this species' higher wood density, which may decrease water transport to leaves (Rosado and de Mattos 2010Rosado BHP and DeMattos EA. 2010. Interspecific variation of functional traits in a CAM-tree dominated sandy coastal plain. J Veg Sci 21: 43-54.).

How does Variation in ΨL Differ in Response to NRD and VPD Throughout the Year?

The less responsive behavior of Byrsonima, Clusia and Protium to NRD and VPD indicates that these species have the ability to decouple from the main factors that drive daily and seasonal variation in water availability. In fact, Byrsonima and Protium show a strong midday depression of stomatal conductance in both wet and dry seasons (Lignani 2008Lignani LDB. 2008. Respostas Ecofisiológicas Contrastantes na Vegetação Aberta da Restinga de Jurubatiba, Macaé, RJ: Um estudo de caso em Protium icicariba (Burseraceae), uma espécie abundante, e Byrsonima sericea (Malpighia­ceae), uma espécie subordinada. Dissertação (Mestrado em Ecologia), Universidade Federal do Rio de Janeiro. (Unpublished).), and the CAM photosynthesis in Clusia (Franco et al. 1996Franco AC, Haag-Kerwer A, Herzog B, Grams TEE, Ball E, DeMattos EA, Scarano FR, Garcia F, Mantovani A and Luttge U. 1996. The effect of light levels on daily patterns of chlorophyll fluorescence and organic acid accumulation in the tropical CAM tree Clusia hilariana. Trees 10: 359-365.) may explain the lack of a midday response to NRD and VPD. In Clusia, the negative relationship between Ψpd and NRD might reflect nocturnal transpiration, typical in CAM species, which may lead to more negative Ψpd as NRD increases. In addition, the unresponsiveness of Ψmd and Ψpd to NRD and/or VPD in Byrsonima may be related to this species' higher leaf death rate and ΨTLP (Rosado and de Mattos 2010Rosado BHP and DeMattos EA. 2010. Interspecific variation of functional traits in a CAM-tree dominated sandy coastal plain. J Veg Sci 21: 43-54.). The less negative ΨTLP associated with a higher rate of leaf shedding may be an escape strategy for Byrsonima, allowing it to avoid the possible adverse effects of NRD and/or VPD on Ψmd and/or Ψpd (Rosado and de Mattos 2010Rosado BHP and DeMattos EA. 2010. Interspecific variation of functional traits in a CAM-tree dominated sandy coastal plain. J Veg Sci 21: 43-54.).

On the other hand, Eugenia, Erythroxylum and Ocotea responded strongly to NRD and/or VPD (Table IV). The negative relationship between NRD and Ψpd for Erythroxylum may indicate a lower capacity for xylem refilling during prolonged rainless periods because of the species' high wood density (Donovan et al. 2001Donovan LA, Linton MJ and Richards JH. 2001. Pre­dawn plant water potential does not necessarily equilibrate with soil water potential under well-watered conditions. Oecologia 129: 328-335., Rosado and de Mattos 2010Rosado BHP and DeMattos EA. 2010. Interspecific variation of functional traits in a CAM-tree dominated sandy coastal plain. J Veg Sci 21: 43-54.). Interestingly, predawn and midday Fv/Fm showed significant negative relationships with VPD and NRD, indicating that chlorophyll fluo­rescence may be more descriptive of the response of a species to water availability than ΨL.

Plants growing on sandy soils have a higher Ψpd than those growing on clay soils (Sperry et al. 2002Sperry JS, Hacke UG, Oren R and Comstock JP. 2002. Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ25: 251-263., Sperry and Hacke 2002Sperry JS, Hacke UG, Oren R and Comstock JP. 2002. Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ25: 251-263.). However, this is true only when the former have access to deeper soil water profiles and/or soil moisture is frequently replenished by rainfall (Fravolini et al. 2005Fravolini A, Hultine KR, Brugnoli E, Gazal R, English NB and Williams DG. 2005. Precipitation pulse use by an invasive woody legume: the role of soil texture and pulse size. Oecologia144: 618-627., Hultine et al. 2005Hultine KR, Koepke DF, Pockman WT, Fravolini A, Sperry JS and Williams DG. 2005. Influence of soil texture on hydraulic properties and water relations of a dominant warm-desert phreatophyte. Tree Physiol26: 313-323.). The Ψpd of restinga species growing where mean annual rainfall was 1100-1300 mm was higher than for other species occurring in sandy environments where the mean annual rainfall was around 450 mm (-0.1 to -1.70 MPa compared with -1.0 to -5.0 MPa, respectively) (Zunzunegui et al. 2005Zunzunegui M, Barradas MCD, Ain-Lhout F, Clavijo A and Novo FG. 2005. To live or to survive in Doñana dunes: Adaptive responses of woody species under a Mediterranean climate. Plant Soil 273: 77-89., Fravolini et al. 2005Fravolini A, Hultine KR, Brugnoli E, Gazal R, English NB and Williams DG. 2005. Precipitation pulse use by an invasive woody legume: the role of soil texture and pulse size. Oecologia144: 618-627., Hultine et al. 2005). In comparison with other seasonal environments, the variation in Ψpd observed in restinga plants, -0.1 to -0.43 MPa in the wet season and -0.19 to -1.70 MPa during the dry season, was not as marked. In Mediterranean plants, Ψpd varies from -0.1 to -0.86 MPa during spring and from -1.45 to -2.28 MPa during summer (Mediavilla and Escudero 2004Mediavilla S and Escudero A. 2004. Stomatal responses to drought of mature trees and seedlings of two co-occurring Mediterranean oaks. Forest Ecol Manag 187: 281-294., David et al. 2007David TS et al. 2007. Water-use strategies in two co-occurring Mediterranean evergreen oaks: surviving the summer drought. Tree Physiol27: 793-803.). In the Brazilian savannas, woody species show a significant decline in Ψpd, from values close to 0 MPa in the wet season to around -0.5 to -1.0 MPa during the dry season (Bucci et al. 2005Bucci SJ, Goldstein G, Meinzer FC, Franco AC, Campanello P and Scholz FG. 2005. Mechanisms contributing to seasonal homeostasis of minimum leaf water potential and predawn disequilibrium between soil and plant water potential in Neotropical savanna trees. Trees 19: 296-304.). It must be remembered, however, that it is not only soil properties, root access to the water table and/or rainfall patterns that affect Ψpd (Sperry et al. 2002Sperry JS, Hacke UG, Oren R and Comstock JP. 2002. Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ25: 251-263., Fravolini et al. 2005Fravolini A, Hultine KR, Brugnoli E, Gazal R, English NB and Williams DG. 2005. Precipitation pulse use by an invasive woody legume: the role of soil texture and pulse size. Oecologia144: 618-627.). Differences in Ψpd among species may also be related to processes such as hydraulic conductance and nocturnal transpiration (Donovan et al. 2001Donovan LA, Linton MJ and Richards JH. 2001. Pre­dawn plant water potential does not necessarily equilibrate with soil water potential under well-watered conditions. Oecologia 129: 328-335., Dawson et al. 2007Dawson TE, Burgess SSO, Tu KP, Oliveira RS, Santiago LS, Fisher JB, Simonin KA and Ambrose AR. 2007. Nighttime transpiration in woody plants from contrasting ecosystems. Tree Physiol27: 561-575.). For Clusia, the CAM behavior of nocturnal stomatal opening, as also observed in C3 plants that show nocturnal transpiration, could explain the low Ψpd, (Donovan et al. 2001Donovan LA, Linton MJ and Richards JH. 2001. Pre­dawn plant water potential does not necessarily equilibrate with soil water potential under well-watered conditions. Oecologia 129: 328-335.). On the other hand, in Erythroxylum, the only brevi-deciduous species in this study, a decrease in the rate of water delivery to the leaves because of the species' high wood density (~0.77 g cm -3; Rosado and de Mattos 2010Rosado BHP and DeMattos EA. 2010. Interspecific variation of functional traits in a CAM-tree dominated sandy coastal plain. J Veg Sci 21: 43-54.) could promote more negative Ψpd and Ψmd, as described in other studies (Donovan et al. 2001Donovan LA, Linton MJ and Richards JH. 2001. Pre­dawn plant water potential does not necessarily equilibrate with soil water potential under well-watered conditions. Oecologia 129: 328-335., Meinzer 2003Meinzer F. 2003. Functional Convergence in plant responses to the environment. Oecologia134: 1-11.).

In conclusion, temporal variation in ΨL and chlorophyll fluorescence was found useful for differentiating between groups of sandy soil species that are responsive or unresponsive to water availability. However, chlorophyll fluorescence appeared to be a more sensitive descriptor of their seasonal and short-term responses to NRD. The use of plant traits as proxies for the responses of communities to environmental change is gaining importance (Sutherland et al. 2013Sutherland WJ et al. 2013. Identification of 100 funda­mental ecological questions. J Ecol 101: 58-67.). In this study we have demonstrated that a better comprehension of how tropical species from drought-prone habitats cope with changes in water availability can be based on measurements of seasonal variation in ΨL and chlorophyll fluorescence. These findings reinforce the importance of ecophysiological knowledge when selecting functional traits for predicting responses to climate change (Rosado et al. 2013Rosado BHP, Dias ATC and DeMattos EA. 2013. Going back to basics: importance of ecophysiology when choosing functional traits for studying communities and ecosystems. Natureza & Conservação 11: 15-22.), and open important avenues for models specifically concerning species from dry environments. In addition, because we focused on species from the Atlantic rain forest complex that are able to occupy coastal sandy plains environments, our results contribute to the understanding of the environ­mental filtering that affects community assembly in resource-poor habitats.

ACKNOWLEDGMENTS

We are very grateful to P. Cavalin and M.I. Braz for their invaluable help with fieldwork. We thank the staff of NUPEM-UFRJ and the National Park for logistic support. We deeply thank both reviewers for good comments and suggestions that helped us improve the manuscript. The authors were supported by grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) and the Programa de Pesquisas Ecológicas de Longa Duração no Brasil (PELD-CNPq).

REFERENCES

  • Araujo DSD, Pereira MCA and Pimentel M. 2004. Flora e estrutura de comunidades na Restinga de Jurubatiba - Síntese dos conhecimentos com enfoque especial para a Formação Aberta de Clusia In: Rocha CFD, Esteves FA and Scarano FR (Eds), Pesquisas de longa duração na restinga de Jurubatiba Ecologia, história natural e conservação, São Carlos: RiMa Editora, p. 59-76.
  • Araujo DSD, Scarano FR, Sá CFC, Kurtz BC, Zaluar HLT, Montezuma RCM and Oliveira RC. 1998. Comunidades vegetais do Parque Nacional da Restinga de Jurubatiba. In: Esteves FA (Ed), Ecologia das Lagoas Costeiras do Parque Nacional da Restinga de Jurubatiba e do Município de Macaé (RJ), Rio de Janeiro: NUPEM-UFRJ, p. 39-62.
  • Baker NR. 2008. Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo. Annu Rev Plant Biol 59: 89-113.
  • Bartlett MK, Scoffoni C and Sack L. 2012. The deter­minants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis. Ecol Lett 15: 393-405.
  • Bellot J, Maestre FT and Hernández N. 2004. Spatio-temporal dynamics of chlorophyll fluorescence in a semi-arid Mediterranean shrubland. J Arid Environ 58: 295-308.
  • Bhaskar R and Ackerly D. 2006. Ecological relevance of minimum seasonal water potential. Physiol Plantarum 127: 353-359.
  • Borchert R. 1994. Soil and stem water storage determine phenology and distribution of tropical dry forests trees. Ecology 75: 1437-1449.
  • Bucci SJ, Goldstein G, Meinzer FC, Franco AC, Campanello P and Scholz FG. 2005. Mechanisms contributing to seasonal homeostasis of minimum leaf water potential and predawn disequilibrium between soil and plant water potential in Neotropical savanna trees. Trees 19: 296-304.
  • Cavalin PO and DeMattos EA. 2007. Spatio-temporal var­iation of photosynthetic pigments in the CAM tree Clusia hilariana Schlechtendal associated with dry spells during the rainy season in southeastern Brazil. Trees 21: 671-675.
  • Choat B, Ball MC, Luly JG, Donnelly CF and Holtum JAM. 2006. Seasonal patterns of leaf gas exchange and water relations in dry rain forest trees of contrasting leaf phenology. Tree Physiol 26: 657-664.
  • Choat B et al. 2012. Global convergence in the vulnerability of forests to drought. Nature 491: 752-755.
  • David TS et al. 2007. Water-use strategies in two co-occurring Mediterranean evergreen oaks: surviving the summer drought. Tree Physiol27: 793-803.
  • Dawson TE, Burgess SSO, Tu KP, Oliveira RS, Santiago LS, Fisher JB, Simonin KA and Ambrose AR. 2007. Nighttime transpiration in woody plants from contrasting ecosystems. Tree Physiol27: 561-575.
  • DeMattos EA and Luttge U. 2001. Chlorophyll fluo­rescence and organic acid oscillations during transition from CAM to C3-photosynthesis in Clusia minor L. (Clu­siaceae). Ann Bot 88: 457-463.
  • Demmig-Adams B and Adams WW. 2006. Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172: 11-21.
  • Donovan LA, Linton MJ and Richards JH. 2001. Pre­dawn plant water potential does not necessarily equilibrate with soil water potential under well-watered conditions. Oecologia 129: 328-335.
  • Franco AC. 2002. Ecophysiology of Woody Plants. In: Oliveira PS and Marques RJ (Eds), The Cerrados of Brazil - Ecology and Natural History of Neotropical Savanna, NY: Columbia Univ. Press, p. 388.
  • Franco AC, Haag-Kerwer A, Herzog B, Grams TEE, Ball E, DeMattos EA, Scarano FR, Garcia F, Mantovani A and Luttge U. 1996. The effect of light levels on daily patterns of chlorophyll fluorescence and organic acid accumulation in the tropical CAM tree Clusia hilariana Trees 10: 359-365.
  • Franks PJ, Drake PL and Froend RH. 2007. Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance. Plant Cell Environ 30: 19-30.
  • Fravolini A, Hultine KR, Brugnoli E, Gazal R, English NB and Williams DG. 2005. Precipitation pulse use by an invasive woody legume: the role of soil texture and pulse size. Oecologia144: 618-627.
  • Henriques RPB, Araujo DSD and Hay JD. 1986. Des­crição e classificação dos tipos de vegetação da restinga de Carapebús, Rio de Janeiro. Rev Bras Bot 9: 173-189.
  • Hultine KR, Koepke DF, Pockman WT, Fravolini A, Sperry JS and Williams DG. 2005. Influence of soil texture on hydraulic properties and water relations of a dominant warm-desert phreatophyte. Tree Physiol26: 313-323.
  • Krause GH. 1988. Photoinhibition of photosynthesis. An eva­luation of damaging and protective mechanisms. Phy­siol Plantarum 74: 566-574.
  • Lamont B and Lamont H. 2000. Utilizable water in leaves of 8 arid species as derived from pressure-volume curves and chlorophyll fluorescence. Physiol Plantarum110: 64-71.
  • Lignani LDB. 2008. Respostas Ecofisiológicas Contrastantes na Vegetação Aberta da Restinga de Jurubatiba, Macaé, RJ: Um estudo de caso em Protium icicariba (Burseraceae), uma espécie abundante, e Byrsonima sericea (Malpighia­ceae), uma espécie subordinada. Dissertação (Mestrado em Ecologia), Universidade Federal do Rio de Janeiro. (Unpublished).
  • Maseda PH and Fernández RJ. 2006. Stay wet or else: three ways in which plants can adjust hydraulically to their environment. J Exp Bot 57: 3963-3977.
  • McDowell N et al. 2008. Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol178: 719-739.
  • McDowell NG, Beerling DJ, Breshears DD, Fisher RA, Raffa KF and Stitt M. 2011. The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends Ecol Evol (Personal edition) 26: 523-532.
  • Mediavilla S and Escudero A. 2004. Stomatal responses to drought of mature trees and seedlings of two co-occurring Mediterranean oaks. Forest Ecol Manag 187: 281-294.
  • Meinzer F. 2003. Functional Convergence in plant responses to the environment. Oecologia134: 1-11.
  • Meinzer FC, Goldstein G, Franco AC, Bustamante M, Igler E, Jackson P, Caldas L and Rundel PW. 1999. Atmospheric and hydraulic limitations on transpiration in Brazilian cerrado woody species. Funct Ecol 13: 273-282.
  • Méndez-Alonzo R, Paz H, Zuluaga RC, Rosell JA and Olson ME. 2012. Coordinated evolution of leaf and stem economics in tropical dry forest trees. Ecology 93: 2397-2406.
  • Noy-Meir I. 1972. Desert ecosystems: environment and producers. Ann Rev Ecol Syst 4: 25-51.
  • Ogaya R, Peñuelas J, Asensio D and Llusià J. 2011. Chlorophyll fluorescence responses to temperature and water availability in two co-dominant Mediterranean shrub and tree species in a long-term field experiment simulating climate change. Environ Exp Bot 71: 123-127.
  • Pillar VD. 1997. Multivariate exploratory analysis and rando­mization testing with MULTIV. Coenoses 12: 145-148.
  • Porcar-Castell A, Juurola E, Nikinmaa E, Berninger F, Ensminger I and Hari P. 2008. Seasonal acclimation of photosystem II in Pinus sylvestris I. Estimating the rate constants of sustained thermal energy dissipation and photochemistry. Tree Physiol28: 1475-1482.
  • Reich P and Borchert R. 1982. Phenology and ecophys­iology of tropical tree, Tabebuia neochrysantha (Bigno­niaceae). Ecology 63: 294-299.
  • Rosado BHP and DeMattos EA. 2007. Variação temporal de características morfológicas de folhas em dez espécies do Parque Nacional da Restinga de Jurubatiba, Macaé, RJ, Brasil. Acta Bot Bras 21: 741-752.
  • Rosado BHP and DeMattos EA. 2010. Interspecific variation of functional traits in a CAM-tree dominated sandy coastal plain. J Veg Sci 21: 43-54.
  • Rosado BHP, Dias ATC and DeMattos EA. 2013. Going back to basics: importance of ecophysiology when choosing functional traits for studying communities and ecosystems. Natureza & Conservação 11: 15-22.
  • Sperry JS and Hacke UG. 2002. Desert shrub water relations with respect to soil characteristics and plant functional type. Funct Ecol16: 367-378.
  • Sperry JS, Hacke UG, Oren R and Comstock JP. 2002. Water deficits and hydraulic limits to leaf water supply. Plant Cell Environ25: 251-263.
  • Sutherland WJ et al. 2013. Identification of 100 funda­mental ecological questions. J Ecol 101: 58-67.
  • Van Der Molen MK et al. 2011. Drought and ecosystem carbon cycling. Agr Forest Meteorol 151: 765-773.
  • Walker D. 1992. Excited leaves. New Phytol121: 325-345.
  • Zunzunegui M, Barradas MCD, Ain-Lhout F, Clavijo A and Novo FG. 2005. To live or to survive in Doñana dunes: Adaptive responses of woody species under a Mediterranean climate. Plant Soil 273: 77-89.

Publication Dates

  • Publication in this collection
    29 Apr 2016
  • Date of issue
    2016

History

  • Received
    09 Jan 2015
  • Accepted
    03 Apr 2015
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