Hailstorm impact across plant taxa: Leaf fall in a mountain environment

Natural catastrophes in the planet increased over 400% from 1970 to 2005, causing severe impact on natural ecosystems, and are sought to increase in the forthcoming decades due to climate change driven events. However, the descriptions of the impacts caused by events as hailstorms on wild ecosystems are anecdotal in the tropical region. The occurrence of a severe hailstorm on a mountainous tropical environment in Brazil allowed, for the first time, to examine hailstorm impact on 32 plant species belonging to distinct families. The study was carried out in an area of rupestrian field located in Serra do Cipó, Minas Gerais State, Brazil. The impact of hail on the vegetation was evaluated by an index of damage and the damage level was related to plant species architectural features. Hail impact differed strongly among the species and was influenced by plant height, growth form, leaf traits and stem type. Hailstorms are natural disturbance phenomena that have differential impacts on plants species in rupestrian fields.


Introduction
Records of substantial impact and damage on nature caused by unexpected and intense climatic disturbances have been reported throughout history. However, the frequency and intensity of these events seem to have been intensifying in the last decades (Bauer-Messmer and Waldvogel, 1997) and human-induced climate change has been argued to be associated with it (Crompton and Aneney, 2008). Natural catastrophes in the planet increased over 400% from 1970to 2005(Zanetti and Schwarz, 2006 Figure 1). Global climatic simulation models indicate an increase of maximum and minimum temperature, modification in precipitation parameters (more intense precipitation or severe drought), increase of tropical cyclones and events related with El Niño, abrupt climate changes, increase in the frequency and intensity of several types of storms such as hurricanes, tornados, thunderstorms, windstorms and hailstorms (e.g., Carter et al., 1999). Hailstorms frequently occur during the spring and summer when the temperatures are higher and more water vapor is available in the atmosphere (Berlato et al., 2000;Nobre, 2001). These phenomena can take place when the rising of the temperature in the closer atmospheric zone layers retains more water vapor causing an acceleration of the hydrologic cycle that promotes severe storms (Nobre, 2001). However, the occurrence of hailstorms is due to multiple factors that involve topographic features, altitude, and temperature, among others (Dale et al., 2001). According to Nobre (2001) the frequency of extreme climatic events in South America is uncertain. It is expected, however, that due to the temperature increase in the atmospheric layers near the surface, an increase in the number of hailstorms in the region. Hail may cause significant impact on vegetation, but as plants live on different habitat conditions and present different traits and architecture, the impact is also expected to differ among them. The most visible impact is at the leaf level due to the loss of leaf area available to photosynthesis caused by the laceration of the leaf lamina or its complete removal (Dwyer et al., 1994). Depending on the ontogenetic development and phenology at the time of the hail event the reproductive structures, fruits and flowers, as well as growth modules (meristems) can be totally destroyed (Whiteside et al., 1988). Stems can also suffer intense damage or even complete re-moval by hailing. Moreover, small lesions can lead to sores and injures few days after the event and the sores caused by impact of hails on plants represent sites for the entrance of diverse pathogenic infections (Jones and Aldwinkle, 1990). At the stand level in a temperate forest environment, damage induced by hailstorms is highly variable depending on stand species composition, amount and extent of ice accumulation, and historical context (Irland, 1998). Peltzer and Wilson (2006) observed that grasses and lichens suffered much higher rate of biomass removal (60-76%) than shrubs (6-8%) after a hailstorm on native grassland in the northern Great Plains of North America. Effects on vegetation involve changes in the composition of species towards more resistant plants species, establishment of new leaves and the recovery of the stems (Peltzer and Wilson, 2006). The recovery after a severe hailstorm appears to be slow, as exemplified by Larrea cuneifolia that needed 207 days to recover the initial dry weight after a hail storm (Méndez, 2003). At a physiological or adaptation perspective, the knowledge of hailstorm impact on wild plant species is anecdotal at best. Otherwise, some physiological alterations such as changes in photosynthetic rate, chlorophyll and secondary compounds have been observed after hailing. The torn edges, caused by hailstorm, become predominant sites of unregulated water loss for the plant. Tartachnyk and Blanke (2008) showed that prompt stomata closure in the leaf area around the damage sites took place within 3 min after hail injury and led to a decline in evapotranspiration and a severe reduction in photosynthetic CO 2 assimilation. Recovery in both transpiration and photosynthesis commenced after 3h. It remained unclear, however, whether the observed decrease in photosynthetic CO 2 assimilation was due exclusively to stomatal limitation preventing entry of CO 2 into the leaf or, additionally, to limitations in primary photochemical processes. Hailstorms can also provoke alterations in the ecological dynamics of an ecosystem (Peltzer and Wilson, 2006) and consequently affect the ecological succession process, at least temporally according to impact and frequency of hailstorm. Most hailstorms hit regions where their impact is not recorded and, as a consequence, the knowledge on potential damage caused on plants in natural ecosystems remains unrecorded. In the tropics most studies are concentrated in crop species (Jakopic et al., 2007;Tartachnyk and Blanke, 2008). However, these plants might not offer reliable comparisons with wild species in their natural habitat conditions as through human selection, these plants present different architecture, and are selected for some attributes, generally not found on their wild relatives. On September 15 th , 2008, a strong hailstorm hit an area comprehended between 1000 and 1300 meters high in elevation in Serra do Cipó, southeastern Brazil ( Figure  2). The phenomenon was recorded on a small area in the elevation gradient of approximately 30-50 km² (19º 16' 45.7"S and 43º 35' 27.8" W). Despite the small area affected, the vegetation was visibly impacted by the storm. The event provided an unforeseen opportunity to study the response of native plants to this natural disturbance. The vegetation hit by the hailstorm, rupestrian field, is one of the richest on species in the tropics and has a high level of endemism and biodiversity (Giulietti et al., 1997). The rich community of herbaceous and woody species are mainly composed of sclerophyllous plants with tortuous trunks, are exposed to severe abiotic conditions that include strong winds, frequent fires, low humidity during the dry season, high temperature variation during the day, high light exposure, and extremely poor soils (Giulietti et al., 1997;Ribeiro and Fernandes, 2000).
In an attempt to provide the first data on the impact and relevance of hailstorm on the speciose and endemic plant community, we evaluated the level of impact of hails on 32 plant species and individual plant traits, such as plant height, growth form, leaf traits and stem type. We aimed to test the following hypotheses: (i) taller plant individuals suffer higher damage than shorter individuals because they are more exposed to hail, independent of plant species; (ii) herbaceous species are more vulnerable to the impact of hailing; and (iii) leaf traits, such as shape and arrangement, and type of stems influence on the intensity of leaf damage caused by hailstorm.

Site description
The field sample was carried out on September 19, 2008, four days after the hailstorm, in the Vellozia Reserve (19º 16' 45.7"S and 43º 35' 27.8" W), located in Serra do Cipó, southern portion of the Espinhaço Range, Minas Gerais State, Brazil. The vegetation of the study site is the rupestrian fields (rocky outcrops at high elevations) (for further details see Giulietti et al., 1997;Ribeiro and Fernandes, 2000).

Damage evaluation and pertinent plant characteristics
The effects of the hailstorm on the rupestrian field vegetation were evaluated on the 32 plant species most frequent in the studied area. Damage was categorized according to (i) damage level (classified according to field analysis of the impact), and (ii) survey of the habit and morphological traits of each plant species that could influence the degree of damage observed in the sample. In the field, up to 10 individuals of each species were examined considering the parameters: height of the individual and the level of damage (leaf loss). Damage level evaluation on leaves was done through an adaptation of the categories based on Dirzo and Dominguez (1995) as 0 = no leaf loss; 1 = 1-6%, 2 = 7-12%, 3 = 13-25%, 4 = 26-50%, 5 = 51-100%. The height and the leaf loss category of each individual were recorded. For each family, the individual frequency in each category of leaf damage after a hailstorm was calculated. To analyze the plant traits that could confer resistance to hail impact, we collect secondary information on each plant species studied from the literature on taxonomy and systematic botany, and obtained assistance from the Botanical Herbarium from Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais. The plant aspects analyzed were: family, growth habit (herb, shrub or tree), leaf traits, and stem type. Leaves were separated according to: leaf attachment (petiolate or sessile), leaf shape (single or compound), leaf arrangement on the stem (alternate and opposite) and leaf texture (membranous, chartaceous, coriaceous and succulent). Stem (woody, stipe, acaule, succulent) was classified as to type. From the data collected we evaluated the frequency of individuals with each plant feature relative to categories of leaf loss. For comparison among the height of the individuals (non-parametric data) observed in each categories of leaf loss, we used the non-parametric test of Kruskal-Wallis (Conover, 1980). The average ordinations (rank mean) were compared by the Dunn test. Chi-square tests (X²) were conducted for the comparison between the frequencies of individual with each plant feature relative to categories of leaf loss. The statistical tests were performed through the Sigma Stat for Windows version 3.5 (Copyright © 2006 Systat Software Inc).

Results
The 32 species analyzed (Table 1, n=10 individuals per species) belong to 20 plant families. The plant species in the familes Clusiaceae, Nyctaginaceae, Mimosoidae, and Erythroxylaceae were the most highly impacted, suffering leaf losses that ranged from 90 to 100%. No apparent physical damage was observed on individuals of the Bromeliaceae, Cactaceae and Rubiaceae ( Table 2). The data indicate that leaf loss varied according to some plant traits. The lowest rates of leaf loss caused by hailstorm were found on the shorter individuals ( Figure 3, P< 0.01) and on herbaceous species (X 2 = 71.5, degree of freedom (df) = 10, P = <0.001; Figure 4a). Individuals with petiolate leaves suffered greater loss of leaves than individuals with sessile leaves (ca. 60% of the sessile individuals suffered no damage) (X 2 = 79.0, df= 5, P = <0.001; Figure 4b). The shape and the arrangement of leaves also influenced leaf loss by hail. The individuals with compound leaves (X 2 = 19.1, df= 5, P = 0.002; Figure 4c) and opposite leaves (X 2 = 109.2, df= 5, P = <0.001; Figure 4d) had higher leaf loss. Species with succulent leaves showed no leaf loss while species with membranous leaves exhibited higher rates of leaf loss (X 2 = 125.2, df= 15, P = <0.001; Figure 4e). The degree of leaf loss was influenced by the type of the plant stem. The frequency of acaule individuals with no damage was high (around 67%), while woody plants with no damage only repre-sented 25% (X 2 = = 98.9, df= 15, P = <0.001; Figure 4f). The most severe damages were found on woody individuals (Figure 4f).

Discussion
Extreme events such as hailstorms cause severe damages on vegetation and produce pronounced leaf loss and laceration of leaves (Whiteside et al., 1988;Jones and Aldwinkle, 1990;Dwyer et al., 1994), as observed in this study. However, hail did not affect plant families homogeneously. In addition, a combination of traits as height, plant habitat, physical features (architecture, leaf hardness) of plant species influenced the degree of hail impact on wild plant species in this ecosystem. The shorter individuals and herbaceous species were the most resistant to hail. Shorter individuals exhibit lower biomass (Huston, 1997) and canopy area, and hence may lose fewer leaves with a minor probability of being hit by the hails. The herbaceous species found in the rupestrian field are species with tough or coriaceous leaves (Giulietti et al., 1997;Ribeiro and Fernandes, 2000). These traits may minimize leaf loss. For the rupestrian fields some leaf features (sessile, simple, alternate, and succulent leaves) appear to offer more protection against hail impact in this ecosystem. Hailstorms are often accompanied by strong winds and, according to leaf spatial features (attachment, shape, arrangement) and resistance (texture), individuals can suffer different levels of damages. Membranous leaves, due to their thin consistency and lesser thickness, are more vulnerable to damages compared to harder and thicker leaves (see Gonçalves and Lorenzi, 2007). For Cunningham et al. (1999), a greater epidermal thickness can allow more leaf resistance (physical reinforcement). Succulent leaves are thicker and have more features such as cuticle developed, which may provide greater protection against environmental damage.  (Peltzer and Wilson, 2006). The effects of hailstorms on vegetation may involve changes in the composition of species according to their ability to live out and respond to damage (Peltzer and Wilson, 2006). The frequency and relevance of such climatic events are thought to increase in the forthcoming decades due to climate change (McMaster, 1999;Dale et al., 2001), and the understanding of these events is of crucial importance for the speciose and fragile habitats generally found in mountain tops worldwide. Hailstorms represent forces that have the potential to change community structure. The knowledge about the impact hailstorm on speciose ecosystems, as the rupestrian fields, and its recovery is of fundamental importance. The vegetation of this threatened ecosystem is already under high pressure caused by invasive species, road construction, fire and urban expansion. Hailstorm may represent a phenomenon of importance that may become major if its frequency increases in the forthcoming years. Otherwise, data on hail impact on wild plant species are rare at best and, hence, there is an urgent need to gather whatever information is available at the moment so that one can attempt to formulate models to predict impact and wild plant species recovery after hailstorm. For the near upcoming future, biologists will be asked to detail their understanding on disturbances caused by climate changes, including how plants, ecosystems and interactions respond to them, and hailstorm might be an important phenomena to be added in the increasing list.