fernandes et al 2011_plant ecology

8/3/2019 Fernandes Et Al 2011_Plant Ecology

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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 narrowlydistributed and threatened species Coccoloba cereif-

era (Polygonaceae). About 33 to 60% of the leaves

on the 246 individuals surveyed were lost. The

disturbance also influenced 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. Con-

trarily, the endophyte richness decreased drastically

after the event (from 104 to 33 species), only 12% of

similar species remain. The hail storm strongly

influenced 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 alsoseverely 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 field

Serra do Cipo

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 precipi-

tation, affect the structure and functioning of ecosys-

tems (Walter 1985; Wolfe 1979; Woodward 1987) is a

question that still requires a better understanding.

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: [email protected]

A. Sanchez-Azofeifa

Department of Earth & Atmospheric Sciences, Centre

for Earth Observation Sciences, University of Alberta,

Edmonton, AB T6G 2R3, Canada

e-mail: [email protected]

123

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DOI 10.1007/s11258-011-9941-z


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Temperature changes brought on by global warming

can increase the occurrence of severe storms (McMas-

ter 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 inten-sity 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). Wil-lemse (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 largerhailstorms.

Hailstorms can cause severe damage to vegeta-

tion 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, flowers, 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 inflict severe damage to plants, but initially

imperceptible, damage to fruits, flowers, 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 assimila-

tion. It remains unclear, however, whether the

observed decrease in photosynthetic CO2 assimila-

tion 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 extinc-

tions of species that are restricted locally and

physiologically more vulnerable of a particularenvironment.

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 first

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 mountainssupport one of the richest floras of the world with a

high degree of endemism (Moreira et al. 2008;

Silva et al. 2008). In this high montane environ-

ment, 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 fields

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 influence

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 rich-

ness of the associated community of leaf endophyticfungi in C. cereifera would be negatively influenced

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 find any

previous study on this regard. We postulate that

alterations in the plant physiology and structure

would negatively affect the endophyte communityinhabited 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 Thennara-

san 2004; Toofanee and Dulymamode 2002). Dam-

aged leaves would present torn edges and holes that

would become sites of unregulated water loss and

modify physiological processes (Tartachnyk andBlanke 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. Thereserve 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 fields 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 flora of Serra do Cipo because of itspurple to bluish-colored sclerophyllous leaves (Gi-

ulietti 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 identified serious threats to

the survival of C. cereifera. The species is micro-

endemic (narrowly distributed) (Ribeiro and Fernan-

des 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 stillunknown 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 contin-

uous gene flow and habitat conservation (Moreira

et al. 2009). Any subpopulation loss or further habitat

fragmentation may represent an important threat tothe 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 reflected

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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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 first 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 field. The first

transect was located at S19816.8020 and W

043835.6400; the second transect at S19816.8260and

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

Fig. 1 Representative

photos of C. cereifera

(Polygonaceae) before

(a) and after (be) a severe

hailstorm in Serra do Cipo,

southeastern Brazil

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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 calcu-

lated 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 thepercentage 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 thenumber 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 youngones 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 polypheno-

lics present in the leaf epidermis of each leaf, a dual

excitation fluorimeter (Dualex Dual Excitation,prototype CNRS-LURE, France) was used in the

field. 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 spectropho-

tometric absorption analysis through spectrophotom-

eter 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, theleaf tissue sections were superficially 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 accord-

ing to their morphological traits, including aerial

mycelium form, colony and medium color, surface

texture, and margin characters. Endophytes were

identified when reproductive structures were found.

The number of morphospecies found in different leafages 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 wereparametric (chlorophyll, carotenoid, and polyphenol

content) and MannWhitney test for the non-para-

metric 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 indi-

cates 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 significantly responded

with an increase of more than 18% water content

(Fig. 2a). The temperature and relative humidity also

presented sharp temporal variations (Fig. 2b). Tem-

perature dropped 14C degrees with an associated

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increased in relative humidity (50%), all within a

timeframe of 15 min. An analysis of the incoming

and reflected light does not show significant 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, confirm 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 importanceof 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

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 observedwhen soil moisture

increased from ca. 10 to

28%. b Variation in

temperature and relative

humidity during the day of

the observed event.

Temperature significantly

dropped between 16:00 and

17:00, which was

complemented with a

significant increase in

relative humidity.

Temperature during and

after the time of the eventdropped 14C degrees and

relative humidity increased

by 50%

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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 individ-

uals studied also decreased after hail impact

(Table 1). In spite of that, the number of fungi

isolated and morphospecies diminished significantly

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 morpho-

species reported before the hailstorm were recorded

again after the hailstorm (IJaccard = 0.120). Four of

these were found in the same leaf age (IJac-card = 0.029), four in the same individuals (IJac-

card = 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

Fig. 3 a Temporal

variation in PAR and

b solar radiation during the

day of the event. No

significant changes are

observed pre and post event

mostly due to a low sun

angle

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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 concentra-

tion 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 ofC. 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

Table 1 Total number of endophyte fungi isolated, morpho-

species, and frequency of individuals with fungi per leaf age

(young, mature and old leaves) from C. cereifera (N= 20),

before and 21 days after of the hailstorm occurred in the Serra

do Cipo, southeastern Brazil

Endophytes Leaf age Leaf number Before hailstorm After hailstorm

Total number of isolated Young 20 6 1

Mature 20 11 13

Old 20 87 20

Total 60 104 34

Total number of morphospecies Young 20 6 1

Mature 20 11 12

Old 20 87 20

Total 60 104 33

Frequency of individual plants with fungi Young 20 0.10 0.05

Mature 20 0.25 0.25

Old 20 0.70 0.55

Total 60 0.80 0.70

Table 2 Means ( SE) of number of endophyte morphospe-

cies, number of endophytic fungi isolated, leaf total chloro-

phyll (mmol/m2

), carotenoid (mmol/m2

), and polyphenol

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

Leaf age Before hailstorm After hailstorm Test T Df P

Endophyte richness Young 0.27 0.01a 0.05 0.05a MannWhitney 420.5 18 [0.05

Mature 0.46 0.02a 0.60 0.31a MannWhitney 410.0 19 [0.05

Old 0.53 0.02a 1.00 0.27b MannWhitney 492.0 19 =0.02

Number of endophyte isolated Young 0.30 0.25a 0.05 0.05a MannWhitney 420.5 18 [0.05

Mature 0.55 0.26a 0.65 0.35a MannWhitney 410.0 19 [ 0.05

Old 4.35 1.21a 1.00 0.27b MannWhitney 492.0 19 =0.02Total Chlorophyll (mmol/m

2) Young 0.27 0.01a 0.43 0.03b Paired t 6.78 18 \0.001

Mature 0.46 0.02a 0.53 0.03b Paired t 2.30 19 \0.05

Old 0.53 0.02a 0.54 0.03a Paired t 0.38 19 [0.05

Carotenoid (mmol/m2) Young 9.10-4 0.02.10-4a 13.10-4 0.3.10-4b Paired t 19.02 18 \0.001

Mature 14.10-4 0.4.10-4a 20.10-4 0.6.10-4b Paired t 20.13 19 \0.001

Old 16.10-4 0.7.10-4a 24.10-4 0.8.10-4b Paired t 19.49 19 \0.001

Polyphenols (lmol/cm2) Young 1.72 0.025a 16.11 0.27b Paired t 52.17 18 \0.001

Mature 1.59 0.027a 14.33 0.34b Paired t 38.17 19 \0.001

Old 1.50 0.014a 16.72 0.46b Paired t 33.51 19 \0.001

Mean values followed by different letters in the same row indicate significant differences between before and after the hailstorm

(P\0.05)

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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 ahailstorm on native grassland in the northern Great

Plains of North America. However, in the rupestrian

field 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 ofLarrea

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 first fifteen minutes after hail injury,

there was a reduction of 33% in photosynthetic CO2assimilation and 16% decline in evapotranspiration in

apple leaves (Tartachnyk and Blanke 2002). Other-

wise, 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 coloniza-

tion 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 (sunflower). InC. cereifera, these secondary compounds increased

tenfold (Table 2). Although the effects of polyphen-

olics on endophytes is not clear at present, in the old

leaves the endophyte richness decreased after hail-

storm, 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 specieswith the restricted distribution pattern or similar

architectural types. Habitat restriction and rarity are

common features of the flora 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 pigmentsand 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 Scientific 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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