Plant Ecol DOI 10.

1007/s11258-011-9941-z

Hail impact on leaves and endophytes of the endemic threatened Coccoloba cereifera (Polygonaceae)
G. Wilson Fernandes Yumi Oki Arturo Sanchez-Azofeifa Gabriela Faccion Helica C. Amaro-Arruda

Received: 16 July 2009 / Accepted: 10 June 2011 Springer Science+Business Media B.V. 2011

Abstract There is increasing evidence that some natural disturbances are increasing in frequency and intensity with global change, but the effects of these changes on plant populations is poorly understood. It is estimated that for every 1C increase in the summer mean minimum temperature, there is a 40% increase in hail damage. Severe hailstorms can cause large impacts on biological communities. In 2008, a strong hailstorm hit the speciose and endemic rupes trian vegetation in Serra do Cipo, Brazil. This event prompted us to record its effects on the narrowly distributed and threatened species Coccoloba cereifera (Polygonaceae). About 33 to 60% of the leaves on the 246 individuals surveyed were lost. The disturbance also inuenced some of the physiological traits of C. cereifera, increasing the concentration of photosynthetic pigments (chlorophyll and carotenoid)

and polyphenols in the leaves. The most pronounced increase of chlorophyll was in young leaves (ca. 60%). Carotenoid content increased by ca. 50% in all leaf ages, while polyphenols increased tenfold. Contrarily, the endophyte richness decreased drastically after the event (from 104 to 33 species), only 12% of similar species remain. The hail storm strongly inuenced all variables evaluated in this study, i.e., structure, physiology, and associated fungi. These results show that hailstorm had a dramatic and immediate impact on C. cereifera and may also severely affect other endemic or threatened plant species. Therefore, it is imperative that we broaden our knowledge on global climate change impacts for the conservation of native species. Keywords Endophytic fungi Disturbance Hailstorm Plant physiology Rupestrian eld Serra do Cipo

G. W. Fernandes (&) Y. Oki G. Faccion H. C. Amaro-Arruda Ecologia Evolutiva & Biodiversidade/DBG, ICB/Universidade Federal de Minas Gerais (UFMG), CP 486, Belo Horizonte, MG 30161-970, Brazil e-mail: gw.fernandes@gmail.com A. Sanchez-Azofeifa Department of Earth & Atmospheric Sciences, Centre for Earth Observation Sciences, University of Alberta, Edmonton, AB T6G 2R3, Canada e-mail: arturo.sanchez@ualberta.ca

Introduction There is increasing evidence that considerable impacts and damages on nature caused by unpredicted and intense climatic disturbances are becoming more frequent. Therefore, the way that global changes, such as abrupt alterations in the temperature and precipitation, affect the structure and functioning of ecosystems (Walter 1985; Wolfe 1979; Woodward 1987) is a question that still requires a better understanding.

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Temperature changes brought on by global warming can increase the occurrence of severe storms (McMaster 1999). Owing to the increased temperature in atmospheric layers near the earths surface, these layers retain more water vapor, and it is expected that the hydrological cycle will become more intensive. This may possibly increase the frequency and intensity of extreme events such as severe storms or hailstorms (Nobre 2001; Van Aalst 2006). The occurrence of hail is not an exclusive characteristic or trait of a given climate, but the result of a combination of several factors, such as topography, elevation, soil exposure and other conditions that favor glaze formation (Dale et al. 2001). In the most affected region, hailstorms are generated by the combination of thermoconvection, high frequency of jet streams at high altitude, with cold fronts at low levels and moist air advections (Vinet 2000). Willemse (1995) showed that there will be a 40% increase in hail damage for every 1C increase in the summer mean minimum temperature stated for some global change scenarios. Forecasts out for the Sydney Basin show that there may be a 26% increase in the number of large and hail events between 20012010 and 20112020 (Leslie et al. 2008). Each successive decade has, in aggregate, more severe hail events than the preceding decade. By 2050, the future climate scenario simulations indicate that this storm will be a common event and suggestive of even larger hailstorms. Hailstorms can cause severe damage to vegetation such as pronounced loss of leaf area and laceration of leaves (Dwyer et al. 1994; Jones and Aldwinkle 1990; Whiteside et al. 1988). Hail damage to foliage, owers, and tender stem tissues appears as bruising, shredding, defoliation, or physical mangling. The damage caused by the impact of hailstones on plant tissue can take many forms depending mainly on hail size, density per area, the speed of fall and duration of storm event, as well as the age and phenology of plant tissues. Some studies have shown that even small hailstones can inict severe damage to plants, but initially imperceptible, damage to fruits, owers, leaf buds, and seedlings in early stages (Leite et al. 2002; Schubert 1991). The direct impacts of hail on plants include lodging and breaking of stems, broken branches, threshing grain, leaf area loss and leaf damage (Berlato et al. 2000; Tartachnyk et al.

2007), however, tattered holes may be obvious only for larger leaves (Schubert 1991). In addition to the direct damage caused by hail, there are also indirect effects such as the reduction of photosynthetic active area as well as the facilitation of pathogen entrance due to damage caused by hailstone impact on branches and leaves (Berlato et al. 2000; Leite et al. 2002; Schubert 1991). For example, Tartachnyk and Blanke (2008) showed that prompt stomatal closure in leaf areas around hail damage occurred after hail impact, which led to a decline in evapotranspiration and a severe reduction in photosynthetic CO2 assimilation. It remains unclear, however, whether the observed decrease in photosynthetic CO2 assimilation was exclusively due to stomatal limitations preventing CO2 entry or limitations in primary photochemical processes. Owing to their devastating effects, most studies have focused on the impacts of hailstorms on agricultural systems, and as such that information can not be translated to wild species on to natural ecosystems. On the other hand, such information may be crucial for conservation efforts. An unpredictable event, such as a severe hailstorm, represents a strong disturbance event that may have large impacts on the biological community, and may even cause extinctions of species that are restricted locally and physiologically more vulnerable of a particular environment. In this article, we report on the impacts of a hailstorm on a wild plant species that occurs in a tropical montane environment in Brazil. Montane environments are expected to provide the rst evidence for global climate changes (Breshears et al. 2008; Pounds et al. 1999), and we expect that communities on those environments will experience the most intense and severe impacts of weather changes, including hailstorms. This is particularly relevant as some Brazilian southeastern mountains support one of the richest oras of the world with a high degree of endemism (Moreira et al. 2008; Silva et al. 2008). In this high montane environment, plants are already subjected to several stressors, including physical and biological factors such as intense solar radiation, high temperatures, and poor soil conditions (Negreiros et al. 2009). We focused our observations on the severely threatened endemic species Coccoloba cereifera

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(Polygonaceae), known only from a single, small, and fragmented population in the rupestrian elds of Serra do Cipo, southeastern Brazil (Moreira et al. 2008). This species has been studied and monitored for some time by our research group, and hence, offered an ideal opportunity to study effects of hailstorm damage on its features. Field observations indicated visible changes in the color pattern of leaves hit by hail stones; hence, providing evidence that hail damage might inuence the concentration of compounds responsible for leaf color patterns. Some studies have now shown increased concentration of polyphenolics on leaves damaged by the physical environments ( Biolley et al. 1998; Hunter and Forkner 1999; Jonasson et al. 1986; Penuelas et al. 1996; Ruhland et al. 2007). Finally, we tested the hypothesis that richness of the associated community of leaf endophytic fungi in C. cereifera would be negatively inuenced by hail stones. Unpublished studies (GWF et al.) revealed a rich community of endophytes associated with the leaves of C. cereifera. The interaction of endophytes and plants has been argued to be of major importance in some plant species and their loss or community change after hailing may be of major importance, however, we failed to nd any previous study on this regard. We postulate that alterations in the plant physiology and structure would negatively affect the endophyte community inhabited by them. These endophytes are broadly diverse in tropical plant species (Arnold and Herre 2003). In general, endophyte richness increases with leaf age in many ecological systems and varies according to the plant species and its tissues (Arnold and Herre 2003; Espinosa-Garcia and Langenheim 1990; Suryanarayanan and Thennarasan 2004; Toofanee and Dulymamode 2002). Damaged leaves would present torn edges and holes that would become sites of unregulated water loss and modify physiological processes (Tartachnyk and Blanke 2008), which could affect the endophyte community. Thus, to begin the understanding the susceptibility of this endemic species C. cereifera, as well as its physiological changes caused by hail impact, we evaluated (a) the damage caused on its population; and (b) changes on the structure and physiology of the leaves and the community of endophytes in C. cereifera after the hail event.

Materials and methods Field site and species description This study was carried out at a private reserve area in Serra do Cipo, km 108 of highway MG 010, at an altitude of 1,200 m, in southeastern Brazil. The reserve encompasses approximately 30% of the distributional range of C. cereifera (Ribeiro and Fernandes 1999; Moreira et al. 2008). This species is a narrowly distributed endemic species from the rupestrian elds of Serra do Cipo (Ribeiro and Fernandes 1999) (Fig. 1a), with a highly aggregated distribution; only found within a small area of 26 km2, between 1,100 and 1,300 m a.s.l. Although rare, C. cereifera is one of the most conspicuous plant species found in the extremely diverse and endemic ora of Serra do Cipo because of its purple to bluish-colored sclerophyllous leaves (Giulietti et al. 1987; Rizzini 1979). The leaves are short petiolate, with a bluish-purple color and exhibit a thick silver waxy layer on the lamina (Melo 2000). We have previously identied serious threats to the survival of C. cereifera. The species is microendemic (narrowly distributed) (Ribeiro and Fernandes 1999, 2000), its distribution area is crossed by a state highway (MG 010) (Viana et al. 2005), it has a rare reproduction system (trioecious) with still unknown impact on its ecology and natural history (Silva et al. 2008), the species is represented by a sole population (Moreira et al. 2008), and hosts some insect herbivores that may reach high population levels (Ribeiro et al. 2003). Although this narrowly endemic species possesses a high genetic diversity preventing a direct genetic risk of extinction, its survivorship might depend on efforts to keep continuous gene ow and habitat conservation (Moreira et al. 2009). Any subpopulation loss or further habitat fragmentation may represent an important threat to the maintenance of C. cereifera. Changes on climatic conditions in the study area are monitored using a set of optical phenology networks consisting of two incoming and reected photosynthetically active radiation (PAR) sensors, and two solar radiation sensors (Onset Corporation, Boston, MA, USA). The stations are complemented with soil moisture (20 cm depth) and temperature/ relative humidity sensor. Data are collected every

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Plant Ecol Fig. 1 Representative photos of C. cereifera (Polygonaceae) before (a) and after (be) a severe hailstorm in Serra do Cipo, southeastern Brazil

15 min using a Hobo Weather station data logger (Onset Corporation, Boston). Sampling To evaluate the impact of a hailstorm on C. cereifera, we carried out two studies. The observations were performed on October 06, 2008, 21 days after a severe hailstorm hit the study area. The rst study evaluated the extensive damage caused on the population of C. cereifera while the second one examined the impacts of hail on the physiology and

structure of the leaves and the community of endophytes from 20 individuals previously studied before the storm (June, 2008). In the study of hail damage, three transects of 20 9 50 m were randomly set in the eld. The rst transect was located at S19816.8020 and W 043835.6400 ; the second transect at S19816.8260 and W043835.6130 ; and the last transect at S 19816.7580 and W043835.6550 . The total number of individuals of C. cereifera and the number of branches on each individual plant were recorded in each transect. From each plant, one main branch was

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randomly chose and on these selected branches, we measured stem height, number of leaves damaged by hailstones, number of remaining leaves, and calculated the rate of leaf loss. The rate of leaf loss was calculated from the number of uprooted leaves in each branch divided by total number of leaves found before of the hailstorm. In addition, we estimated the percentage of leaf area loss (from remaining leaves) in each branch. The correlation between the height of the branches and the rate of leaf loss was performed with Spearman correlation. For the study on leaf traits and endophytic community from C. cereifera after the hailstorm, leaves at different positions on the branches from each of 20 individuals of C. cereifera previously studied in the same season (June, 2008) were selected as they could provide clear evidence of hail impacts. To estimate the impact, we initially evaluated the number of remaining leaves, number of leaves damaged by the hailstorm, and estimated leaf area loss on each individual. Leaves were selected according to their age as unfolded, young, mature, and old. The age classes can be visually distinguished based on leaf coloration. As C. cereifera leaves age, sclerophylly increases, wax accumulates on leaf lamina, and the color shifts from deep purple (unfolded) to bluish purple (young), turquoise, green (mature), and green (old). In some individuals hit by hails, unfolded leaves and young ones were not found, and were scored as lost due to the impact of hail stones (Fig. 1be). A total of 61 leaf samples were selected (two unfolded leaves, 19 young leaves, 20 mature leaves, and 20 old ones) and permanently numbered. In each one of these 61 leaf samples, we measured polyphenols, the percentage of leaf area loss, chlorophyll and carotenoid contents, and endophytic fungi richness. For the non-destructive assessment of polyphenolics present in the leaf epidermis of each leaf, a dual excitation uorimeter (Dualex Dual Excitation, prototype CNRS-LURE, France) was used in the eld. Afterward, leaves were collected and digitally photographed to calculate the leaf area loss using Photoshop 7.0. The 61 samples were then wrapped in aluminum foil and stored in a refrigerator (ca. 2C) for further analyses. Later (12 h) one 1 9 1 cm square of leaf tissue was taken from each leaf to assay chlorophyll and carotenoid content. Photosynthetic pigments

(total chlorophyll and carotenoid) were assessed using extraction and subsequent in vivo spectrophotometric absorption analysis through spectrophotometer Cirrus 80 MB, Femto, Brazil, following the Holden (1976) method. Another square of 1 9 1 cm of leaf tissue was removed to evaluate endophytic fungi richness. For endophytic fungi evaluation, the leaf tissue sections were supercially sterilized (Fisher et al. 1992). Fragments of each leaf region were placed onto potato-dextrose-agar (PDA) petri plates (supplemented with cloranphenicol 100 ppm to inhibit bacteria growth) and incubated at 25C for 10 days. The emerged fungi were separated according to their morphological traits, including aerial mycelium form, colony and medium color, surface texture, and margin characters. Endophytes were identied when reproductive structures were found. The number of morphospecies found in different leaf ages was recorded. Unfolded leaves were excluded from data analysis due to low sampling number (N = 2). The results of the rate of leaf area loss after hailstorm found among different leaf ages were statistically analyzed using One Way Repeated Measures Anova (SigmaStat 3.5). For comparisons of the parameters studied (richness and number of isolated of endophytes, chlorophyll, carotenoid, and polyphenol content) before and after hailstorm in each leaf age (young, mature, and old leaves) we used Paired t test when the data were parametric (chlorophyll, carotenoid, and polyphenol content) and MannWhitney test for the non-parametric data (richness and number of isolated of endophytes). Data are presented as means standard errors. The similarity of fungi species (Jaccard Index, Krebs 1998) found in the leaves of C. cereifera before and after the hailstorm was evaluated.

Results Analysis of the available meteorological data indicates that a large precipitation event took place immediately after the main hailstorm. A total of 18 mm of precipitation was observed within 15 min after the event. Soil moisture signicantly responded with an increase of more than 18% water content (Fig. 2a). The temperature and relative humidity also presented sharp temporal variations (Fig. 2b). Temperature dropped 14C degrees with an associated

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Plant Ecol Fig. 2 a Precipitation and response of soil moisture content after the hail event that took place at 16:30 on September 15th 2008 in Serra do Cipo, Brazil. A rapid response ca. 15 min after the event is observed when soil moisture increased from ca. 10 to 28%. b Variation in temperature and relative humidity during the day of the observed event. Temperature signicantly dropped between 16:00 and 17:00, which was complemented with a signicant increase in relative humidity. Temperature during and after the time of the event dropped 14C degrees and relative humidity increased by 50%

increased in relative humidity (50%), all within a timeframe of 15 min. An analysis of the incoming and reected light does not show signicant effects on underlying vegetation, likely due to the sun angle distribution at the time of the event (Fig. 3a, b). Increases in precipitation, humidity and soil moisture, coupled with the observed decrease in temperature (place quantities) during the timeframe between 16:00 and 17:00, conrm the occurrence of the hailstorm event. We observed 246 C. cereifera individuals in the three transects studied. All the individuals sampled had profound damage on stems and branches and considerable leaf loss (Fig. 1be). The average height

of the branches studied was 47.5 cm 2.1, while the rate of leaf loss of the individuals in the three transects was 41.6 1.6%. Leaf area loss was positively correlated with branch height, but was low (r = 0.14, P \ 0.03), indicating the importance of other unmeasured factors. The mean percentage of leaf damage on the 20 selected individuals was 35.2% 2.2, but there was no difference in the average percentage of leaf damage among leaf ages (P [ 0.05). Endophytes were reared from 14 out of the 20 individuals studied, while a total of 33 endophyte morphospecies were recorded on them (Table 1). Curiously, these were recovered from a total of 34

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Plant Ecol Fig. 3 a Temporal variation in PAR and b solar radiation during the day of the event. No signicant changes are observed pre and post event mostly due to a low sun angle

fungi isolates, indicating that nearly every isolate represented endophyte morphospecies (Table 1). The frequency of individuals with endophytes decreased after the hail event, from 80% to 70% individuals. Both the total number of isolates of fungi and morphospecies found in the leaves of the 20 individuals studied also decreased after hail impact (Table 1). In spite of that, the number of fungi isolated and morphospecies diminished signicantly after hail stone impact only for old leaves (P = 0.02; Table 2). No endophytes were recorded in unfolding leaves before or after the hailstorm. Endophyte community composition also changed after the

hailstorm. Only 17 out of the 33 endophyte morphospecies reported before the hailstorm were recorded again after the hailstorm (IJaccard = 0.120). Four of these were found in the same leaf age (IJaccard = 0.029), four in the same individuals (IJaccard = 0.029), and only one was found in the same individual and leaf age (IJaccard = 0.007). Hail promotes an increase of approximately 4360% in the chlorophyll and carotenoid contents in almost all leaf ages of C. cereifera (Table 2). The strongest increase of chlorophyll content was observed in young leaves (about 60%), while an increase of approximately 15% was recorded in

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Plant Ecol Table 1 Total number of endophyte fungi isolated, morphospecies, and frequency of individuals with fungi per leaf age (young, mature and old leaves) from C. cereifera (N = 20), Endophytes Total number of isolated Leaf age Young Mature Old Total Total number of morphospecies Young Mature Old Total Frequency of individual plants with fungi Young Mature Old Total before and 21 days after of the hailstorm occurred in the Serra do Cipo, southeastern Brazil Leaf number 20 20 20 60 20 20 20 60 20 20 20 60 Before hailstorm 6 11 87 104 6 11 87 104 0.10 0.25 0.70 0.80 After hailstorm 1 13 20 34 1 12 20 33 0.05 0.25 0.55 0.70

Table 2 Means ( SE) of number of endophyte morphospecies, number of endophytic fungi isolated, leaf total chlorophyll (mmol/m2), carotenoid (mmol/m2), and polyphenol Leaf age Endophyte richness Young Mature Old Number of endophyte isolated Young Mature Total Chlorophyll (mmol/m2) Old Young Mature Old Carotenoid (mmol/m2) Young Mature Old Polyphenols (lmol/cm2) Young Mature Old Before hailstorm 0.27 0.01a 0.46 0.02a 0.53 0.02a 0.30 0.25a 0.55 0.26a 4.35 1.21a 0.27 0.01a 0.46 0.02a 0.53 0.02a 9.10-4 0.02.10-4a 14.10
-4

content (lmol/cm2) for each of three leaf age classes (young, mature, and old) in C. cereifera, before and after an intense hailstorm in the Serra do Cipo, southeastern Brazil After hailstorm 0.05 0.05a 0.60 0.31a 1.00 0.27b 0.05 0.05a 0.65 0.35a 1.00 0.27b 0.43 0.03b 0.53 0.03b 0.54 0.03a 13.10-4 0.3.10-4b 20.10
-4

Test MannWhitney MannWhitney MannWhitney MannWhitney MannWhitney MannWhitney Paired t Paired t Paired t Paired t Paired t Paired t Paired t Paired t Paired t
-4

T 420.5 410.0 492.0 420.5 410.0 492.0 6.78 2.30 0.38 19.02 20.13 19.49 52.17 38.17 33.51

Df 18 19 19 18 19 19 18 19 19 18 19 19 18 19 19

P [0.05 [0.05 =0.02 [0.05 [ 0.05 =0.02 \0.001 \0.05 [0.05 \0.001 \0.001 \0.001 \0.001 \0.001 \0.001

0.4.10 a

-4

0.6.10 b

16.10-4 0.7.10-4a 1.72 0.025a 1.59 0.027a 1.50 0.014a

24.10-4 0.8.10-4b 16.11 0.27b 14.33 0.34b 16.72 0.46b

Mean values followed by different letters in the same row indicate signicant differences between before and after the hailstorm (P \ 0.05)

mature leaves. No statistical difference was found in the chlorophyll content of old leaves after and before the hailstorm. The carotenoid content increased about 4350% in all leaf ages. The polyphenol concentration in the leaves of C. cereifera after hailstorm increased tenfold than in the leaves before the hailstorm (P \ 0.001; Table 2).

Discussion An intense hailstorm caused severe damage on the sole known population of C. cereifera, an endangered species found in a mountain top in southeastern Brazil. Hail caused the loss of 42% of leaves while most of the remaining leaves and branches were also

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damaged (Fig. 1). The impact of hail depends on the physical properties of the both storm and hail stones, such as angle of impact, size of stones, and also on the structure and architecture of plants (Houston 1999; Mendez 2003). Peltzer and Wilson (2006) observed that grasses and lichens suffer higher rate of biomass loss (6076%) than shrubs (68%) after a hailstorm on native grassland in the northern Great Plains of North America. However, in the rupestrian eld of Serra do Cipo, shrub species suffered higher rate of leaf loss (5060%) compared with herbaceous species after a hailstorm (Fernandes et al. submitted). More generally, the effects of hailstorms on vegetation involve changes in the composition of species and their ability to respond to damage (Peltzer and Wilson 2006). The recovery after a severe hailstorm event may be slow or fast depending on the plant species, storage organs, phenology, etc. For instance, after a hailstorm, the branches of Larrea cuneifolia needed 207 days to recover to pre-storm dry weight (Mendez 2003). In our study, we were unable to obtain such data. However, observations about recovery time of establishment following hailstorm for native species are needed if we want to better understand the effect of hailstorms on native plant species and their conservation (Mendez 2003). This is of relevance as such climatic events are supposed to increase in the forthcoming decades due to climate change (Dale et al. 2001; McMaster 1999). Perhaps of major or crucial relevance is of that knowledge for speciose habitats where endemics thrive, such as in tropical mountain tops worldwide. The effect of hail on C. cereifera represents a mechanically induced disturbance. Physiological alterations such as changes in photosynthetic rate, chlorophyll, and secondary compound have been observed after hailstorms in some cultivated plant species (Jakopic et al. 2007; Tartachnyk and Blanke 2008). In the rst fteen minutes after hail injury, there was a reduction of 33% in photosynthetic CO2 assimilation and 16% decline in evapotranspiration in apple leaves (Tartachnyk and Blanke 2002). Otherwise, a series of photochemical process leads to the physiological recuperation of the plant (Tartachnyk and Blanke 2008). This is probably related to the increase in chlorophyll and carotenoid content that followed the hailstorm in our studied C. cereifera. The small lesions provoked by the physical impact of the hail stones represent open doors for the entry of

pathogens and insects even days after the event (Jones and Aldwinkle 1990). A way of preventing or diminishing these natural enemy impact or colonization is the increase in the synthesis of polyphenols (Harborne 1989; Hammerschmidt 2005). Indeed, Moriondo et al. (2003) reported an increase in polyphenolics in Helianthus annuus (sunower). In C. cereifera, these secondary compounds increased tenfold (Table 2). Although the effects of polyphenolics on endophytes is not clear at present, in the old leaves the endophyte richness decreased after hailstorm, and was coincident with polyphenol increase. Future experimental studies are called for to address this question. The knowledge about impact of hailstorm on the only known population of C. cereifera and its recovery is of crucial importance to the conservation of this species, and possibly to other many species with the restricted distribution pattern or similar architectural types. Habitat restriction and rarity are common features of the ora of many speciose tropical vegetations and at mountain tops worldwide. Furthermore, knowledge on hail impact on endemic and restricted species is of increasing interest due to the need to measure vulnerability and survivorship in harsh mountain environments where hail are expected to increase in the future. The results indicate that hailstorms may have the potential to modify plant metabolism (photosynthetic pigments and polyphenols content) and even the plants relationship with its associated microorganisms. The increased frequency and intensity of hailstorms reinforces the urgent need to better understand the complex changes caused by such events on those species in need of protectionespecially endemic species.
Acknowledgments The authors thank D. Goodsman, D. Negreiros, S. Castro and M. Storquio for their valuable assistance. This research was supported by National Counsel of Technological and Scientic Development (CNPq Proc. 476178/2008-8, 303352/2010-8, 474292/2010-0, 559279/2008` 6, 558250/2009-2, 151817/2008-1), Fundacao de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG Proc. APQ 01278-08, EDT 465/07, RDP-00048-10), Coordenacao de Aperfeicoamento de Pessoal de Nvel Superior (CAPES Proc. BEX 323710-9, Proc. 02/2009 DRI/CGCI), The Natural Sciences and Engineering Research Council of Canada (NSERC), and the Inter American Institute for Global Change Research (IAI) Collaborative Research Network Program CRN-II funded under the U.S. National Science Foundation Grant.

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