Abstracts
The specific leaf area (SLA) has been related to environmental disturbances, showing a positive correlation between the disturbances intensities and SLA in a plant community. These studies, however, assessed the responses of plant community as a whole, neglecting species attributes, such as the position in the vertical stratum of forests. Considering the importance of SLA to understand forest ecological processes, this study aimed to determine the influence of the disturbance regime on the SLA of understory species, considering that, unlike for communities as a whole, an increase in the disturbance intensity implies a decrease in SLA of understory species. This study was conducted in nine understories of seasonal forests in Brazil. The most abundant species were selected and their SLA were evaluated. The variability of SLA among populations in different forests was analyzed by Student’s t-tests. The SLA of the understories (SLAU) was also compared by an adaptation of the Community-weighted mean index. The comparison of species SLA showed significant differences among the populations of understories under different disturbance regime, showing a decrease in SLA with an increase in the disturbance intensity. Similar results were found for the SLA of understories communities (SLAU), corroborating our hypothesis. The correlation between a reduction in species SLA and in SLA of understory with an increase in disturbance intensity, contradicted the trend observed in the literature for the community as a whole. This study highlights the importance of the evaluation of SLA in understories, as an indicator of the successional stage of communities.
community-weighted mean index; conservation; intraspecific variability; semideciduous seasonal forests; specific leaf area
A área foliar específica (SLA) tem sido relacionada a distúrbios ambientais, apresentando uma correlação positiva entre a intensidade de perturbação e a SLA da comunidade vegetal. Estes estudos, no entanto, avaliaram as respostas da comunidade vegetal como um todo, negligenciando os atributos por espécies, tais como a posição vertical no estrato florestal. Considerando a importância da SLA para entender os processos ecológicos das florestas, este estudo teve como objetivo determinar a influência do regime de perturbação na SLA de espécies de sub-bosque, cuja hipótese é que, ao contrário de comunidades como um todo, um aumento na intensidade de perturbação implica na diminuição da SLA de espécies de sub-bosque. Este estudo foi realizado em nove sub-bosque de florestas estacionais no Brasil. As espécies mais abundantes foram selecionados e suas SLA foram avaliadas. A variabilidade de SLA entre as populações em diferentes florestas foi analisada pelo teste t de Student. O SLA dos sub-bosque (SLAu) também foi comparado por uma adaptação do índice de média ponderada da comunidade. A comparação de SLA das espécies mostraram diferenças significativas entre as populações de sub-bosque sob um regime de distúrbios diferentes, mostrando um decréscimo na SLA com um aumento na intensidade de perturbação. Resultados semelhantes foram encontrados para o SLA dos sub-bosque (SLAu), corroborando nossa hipótese. A correlação entre a redução no SLA espécies e SLA do sub-bosque com um aumento na intensidade de perturbação contradiz a tendência observada na literatura para a comunidade como um todo. Este estudo destaca a importância da avaliação de SLA em sub-bosque, como um indicador do estágio sucessional das comunidades.
índice de média ponderada da comunidade; conservação; variabilidade intra-específica; florestas estacionais semideciduais; área foliar específica
1 Introduction
A functional trait is an attribute with a potential influence on the establishment,
survival or fitness of a species in a natural environment (Reich et al., 2003Reich, PB., Wright, IJ., Cavender-Bares, J., Craine, JM., Oleksyn,
J., Westoby, M. and Walters, MB., 2003. The evolution of plant functional
variation: Traits, spectra, and strategies. International Journal of Plant
Sciences, vol. 164, no. S3, p. S143-S164.
http://dx.doi.org/10.1086/374368.
http://dx.doi.org/10.1086/374368...
). Quantifying changes in these traits is
important to understand the patterns of species distribution and to predict
vegetation responses to environmental changes (Silva and Batalha, 2009Silva, IA. and Batalha, MA., 2009. Phylogenetic overdispersion of
plant species in southern Brazilian savannas. Brazilian journal of biology =
Revista brasileira de biologia, vol. 69, no. 3, p. 843-849.
http://dx.doi.org/10.1590/S1519-69842009000400011.
PMid:19802443
http://dx.doi.org/10.1590/S1519-69842009...
; Freitas et
al., 2012Freitas, JR., Cianciaruso, MV. and Batalha, MA., 2012. Functional
diversity, soil features and community functioning: a test in a cerrado site.
Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 72, no. 3,
p. 463-470. http://dx.doi.org/10.1590/S1519-69842012000300008.
PMid:22990816
http://dx.doi.org/10.1590/S1519-69842012...
).
Variations in leaf functional traits, especially in specific leaf area (SLA), have
guided many studies of functional ecology, which have addressed important ecological
correlations, such as relative growth rate and the photosynthetic efficiency of a
species (Reich et al., 2003Reich, PB., Wright, IJ., Cavender-Bares, J., Craine, JM., Oleksyn,
J., Westoby, M. and Walters, MB., 2003. The evolution of plant functional
variation: Traits, spectra, and strategies. International Journal of Plant
Sciences, vol. 164, no. S3, p. S143-S164.
http://dx.doi.org/10.1086/374368.
http://dx.doi.org/10.1086/374368...
; Zhang et al., 2012Zhang, JL., Poorter, L. and Cao, KF., 2012. Productive leaf
functional traits of Chinese savanna species. Plant Ecology, vol. 213, no. 9, p.
1449-1460. http://dx.doi.org/10.1007/s11258-012-0103-8.
http://dx.doi.org/10.1007/s11258-012-010...
). Of all the environmental
factors affecting leaf functional leaf traits, light is perhaps one of the most
studied in the literature (Pearcy, 2007Pearcy, RW., 2007. Responses of Plants to Heterogeneous Light
Environments. In PUGNAIRE, F. and VALLADARES, F. (Eds.). Functional plant
ecology. New York: Taylor & Francis Group. p. 213-258.
http://dx.doi.org/10.1201/9781420007626.ch7.
http://dx.doi.org/10.1201/9781420007626....
;
Hulshof and Swenson, 2010Hulshof, CM. and Swenson, NG., 2010. Variation in leaf functional
trait values within and across individuals and species: an example from a Costa
Rican dry forest. Functional Ecology, vol. 24, no. 1, p. 217-223.
http://dx.doi.org/10.1111/j.1365-2435.2009.01614.x.
http://dx.doi.org/10.1111/j.1365-2435.20...
; Mallik et al., 2013Mallik, AU., Kreutzweiser, DP., Spalvieri, CM. and Mackereth, RW.,
2013. Understory plant community resilience to partial harvesting in riparian
buffers of central Canadian boreal forests. Forest Ecology and Management, vol.
289, p. 209-218.
http://dx.doi.org/10.1016/j.foreco.2012.09.039.
http://dx.doi.org/10.1016/j.foreco.2012....
). Plants growing under
high light exposure generally show thicker leaves with a lower SLA (Cornelissen et al., 2003 Cornelissen, JHC., Lavorel, S., Garnier, E., Díaz, S., Buchmann,
N., Gurvich, DE., Reich, PB., Steege, H., Morgan, HD., Heijden, MGA., Pausas,
JG. and Poorter, H., 2003. A handbook of protocols for standardised and easy
measurement of plant functional traits worldwide. Australian Journal of Botany,
vol. 51, no. 4, p. 335-380. http://dx.doi.org/10.1071/BT02124.
http://dx.doi.org/10.1071/BT02124...
). Shade leaves show a
low foliar construction cost, since they are less thick and with lower
concentrations of photosynthetic enzymes per area, which increases their SLA (Westoby et al., 2002Westoby, M., Falster, DS., Moles, AT., Vesk, PA. and Wright, IJ.,
2002. Plant ecological strategies: some leading dimensions of variation between
species. Annual Review of Ecology and Systematics, vol. 33, no. 1, p. 125-159.
http://dx.doi.org/10.1146/annurev.ecolsys.33.010802.150452.
http://dx.doi.org/10.1146/annurev.ecolsy...
).
Recently, the SLA has been related to another important environmental factor: the
disturbance intensity. Most studies show a positive correlation between the
intensity or frequency of disturbances and SLA in a plant community (Reich et al., 2003Reich, PB., Wright, IJ., Cavender-Bares, J., Craine, JM., Oleksyn,
J., Westoby, M. and Walters, MB., 2003. The evolution of plant functional
variation: Traits, spectra, and strategies. International Journal of Plant
Sciences, vol. 164, no. S3, p. S143-S164.
http://dx.doi.org/10.1086/374368.
http://dx.doi.org/10.1086/374368...
; Garnier et al., 2004Garnier, E., Cortez, J., Billes, G., Navas, ML., Roumet, C.,
Debussche, M., Laurent, G., Blanchard, A., Aubry, D., Bellmann, A., Neill, C.
and Toussaint, JP., 2004. Plant functional markers capture ecosystem properties
during secondary succession. Ecology, vol. 85, no. 9, p. 2630-2637.
http://dx.doi.org/10.1890/03-0799.
http://dx.doi.org/10.1890/03-0799...
; Wright
et al., 2004Wright, IJ., Reich, PB., Westoby, M., Ackerly, DD., Baruch, Z.,
Bongers, F., Cavender-Bares, J., Chapin, T., Cornelissen, JHC., Diemer, M.,
Flexas, J., Garnier, E., Groom, PK., Gulias, J., Hikosaka, K., Lamont, BB., Lee,
T., Lee, W., Lusk, C., Midgley, JJ., Navas, ML., Niinemets, U., Oleksyn, J.,
Osada, N., Poorter, H., Poot, P., Prior, L., Pyankov, VI., Roumet, C., Thomas,
SC., Tjoelker, MG., Veneklaas, EJ. and Villar, R., 2004. The worldwide leaf
economics spectrum. Nature, vol. 428, no. 6985, p. 821-827.
http://dx.doi.org/10.1038/nature02403. PMid:15103368
http://dx.doi.org/10.1038/nature02403...
; Fortunel et al.,
2009Fortunel, C., Garnier, E., Joffre, R., Kazakou, E., Quested, H.,
Grigulis, K., Lavorel, S., Ansquer, P., Castro, H., Cruz, P., Dolezal, J.,
Eriksson, O., Freitas, H., Golodets, C., Jouany, C., Kigel, J., Kleyer, M.,
Lehsten, V., Leps, J., Meier, T., Pakeman, R., Papadimitriou, M., Papanastasis,
VP., Quétier, F., Robson, M., Sternberg, M., Theau, JP., Thébault, A. and
Zarovali, M., 2009. Leaf traits capture the effects of land use changes and
climate on litter decomposability of grasslands across Europe. Ecology, vol. 90,
no. 3, p. 598-611. http://dx.doi.org/10.1890/08-0418.1.
PMid:19341132
http://dx.doi.org/10.1890/08-0418.1...
). However, most of these studies focus on responses to grass, herbs
and shrubs and are concentrated in temperate environments (Fortunel et al., 2009Fortunel, C., Garnier, E., Joffre, R., Kazakou, E., Quested, H.,
Grigulis, K., Lavorel, S., Ansquer, P., Castro, H., Cruz, P., Dolezal, J.,
Eriksson, O., Freitas, H., Golodets, C., Jouany, C., Kigel, J., Kleyer, M.,
Lehsten, V., Leps, J., Meier, T., Pakeman, R., Papadimitriou, M., Papanastasis,
VP., Quétier, F., Robson, M., Sternberg, M., Theau, JP., Thébault, A. and
Zarovali, M., 2009. Leaf traits capture the effects of land use changes and
climate on litter decomposability of grasslands across Europe. Ecology, vol. 90,
no. 3, p. 598-611. http://dx.doi.org/10.1890/08-0418.1.
PMid:19341132
http://dx.doi.org/10.1890/08-0418.1...
). Moreover, the studies assessed the
responses of the plant community as a whole, neglecting species attributes, such as
the position in the vertical stratum of forests.
In tropical forest understories, an environment that is typically shaded, the
irradiance available to plants might represent only 1-2% of the total incoming
radiation to the canopy (Poorter et al.,
2006Poorter, L., Bongers, L. and Bongers, F., 2006. Architecture of 54
moist-forest tree species: traits, trade-offs, and functional groups. Ecology,
vol. 87, no. 5, p. 1289-1301.
http://dx.doi.org/10.1890/0012-9658(2006)87[1289:AOMTST]2.0.CO;2.
PMid:16761607
http://dx.doi.org/10.1890/0012-9658(2006...
), and then, the plant species might exhibit different responses.
Thus, the increase in irradiance on understories, caused by disturbances, can result
in distinct functional leaf responses compared to those in the entire community,
with a selection pressure towards an increase in the SLA (Schieving and Poorter, 1999Schieving, F. and Poorter, H., 1999. Carbon gain in a multispecies
canopy: the role of specific leaf area and photosynthetic nitrogen-use
efficiency in the tragedy of the commons. The New Phytologist, vol. 143, no. 1,
p. 201-211. http://dx.doi.org/10.1046/j.1469-8137.1999.00431.x.
http://dx.doi.org/10.1046/j.1469-8137.19...
; Cornelissen et al., 2003 Cornelissen, JHC., Lavorel, S., Garnier, E., Díaz, S., Buchmann,
N., Gurvich, DE., Reich, PB., Steege, H., Morgan, HD., Heijden, MGA., Pausas,
JG. and Poorter, H., 2003. A handbook of protocols for standardised and easy
measurement of plant functional traits worldwide. Australian Journal of Botany,
vol. 51, no. 4, p. 335-380. http://dx.doi.org/10.1071/BT02124.
http://dx.doi.org/10.1071/BT02124...
).
Evaluate the patterns of responses of functional traits for each stratum of
vegetation can assist in understanding responses of forest communities to
environmental changes related to the disturbance. The understory, especially, is the
most sensitive stratum to environmental perturbations (Mulkey and Pearcy, 1992Mulkey, SS. and Pearcy, RW., 1992. Interactions between acclimation
and photoinhibition of photosynthesis of a tropical forest understorey herb,
Alocasia macrorrhiza, during simulated canopy gap formation. Functional Ecology,
vol. 6, no. 6, p. 719-729. http://dx.doi.org/10.2307/2389969.
http://dx.doi.org/10.2307/2389969...
). This, considering the importance of
SLA as a guide to understanding forest changes, this paper aimed to determine the
influence of the disturbance regime in the study areas on the SLA of understory
species, considering that, unlike the communities as a whole, the increase in the
intensity of disturbance implies a decrease in SLA in species from this stratum.
2 Methods
2.1 Research areas and species selection
This study used the database from previous phytosociological tree community
studies (DBH ≥ 5 cm) in ten areas of seasonal semideciduous forests in Central
Brazil, totaling a sample of 10 ha (Table
1) (Lopes et al., 2012Lopes, SDF., Schiavini, I., Oliveira, AP. and Vale, VS., 2012. An
Ecological Comparison of Floristic Composition in Seasonal Semideciduous Forest
in Southeast Brazil: Implications for Conservation. International Journal of
Forestry Research, vol. 2012, p. 1-14.
http://dx.doi.org/10.1155/2012/537269.
http://dx.doi.org/10.1155/2012/537269...
).
These studies evaluated the structure and floristic diversity of the areas
comparing density, basal area and frequency of community species from
methodology of sample plots (25 plots per area). The botanical classification of
these studies was based on the Angiosperm Phylogenetic Group (APG III, 2009Angiosperm Phylogeny Group - APG III, 2009. An update of the
Angiosperm Phylogeny Group classification for the order and families of
flowering plants: APG III. Botanical Journal of the Linnean Society, vol. 161,
p. 105-121.). Species sampled from the
ten areas used in this study were classified by Lopes et al. (2014)LOPES, SF., VALE, VS., SCHIAVINI, I., PRADO JUNIOR, JA., OLIVEIRA,
AP., and ARANTES, CS., 2014. Canopy stratification in tropical seasonal forests:
how the functional traits of community change among the layers. Bioscience
Journal, vol. 30, no. 5, p. 1551-1562. according to their position in the stratum
community: canopy species, intermediary stratum species (under-canopy) and
understory species, using a nonparametric methodology of quartiles and medians
of heights of community and species. For this study, we used just the species
classified as understory species (Prado Junior
et al., 2014PRADO JUNIOR, JA., LOPES, SF., VALE, VS., ARANTES, CS., OLIVEIRA,
AP., and SCHIAVINI, I., 2014. Floristic patterns in understoreys under different
disturbance severities in seasonal forests. Journal of Tropical Forest Science,
vol. 26, no. 4, p. 458-468.). Since this paper aimed to study tree community, with
DBH ≥ 5 cm standardized for seasonal semidecidual forests (Felfili et al., 2011FELFILI, JM., EISENLORH, PV., MELO, MMRF., ANDRADE, LA., and
MEIRA-NETO, JAA., 2011. Fitossociologia no Brasil: métodos e estudos de casos.
Viçosa: Universidade Federal de Viçosa. 556 p. vol. 1.), herbaceous and shrubby species that
are present in understory “lato sensu” were not included in
sample. Thus, tested hypothesis are applicable just for tree community in
understory.
Classification and description of nine sites of seasonal semideciduous forests according to disturbance intensity (adapted from Lopes et al., 2013LOPES, SF., PRADO JUNIOR, JA., VALE, VS., and SCHIAVINI, I., 2013. Impactos ambientais antrópicos como modificadores da estrutura e funcionalidade de florestas estacionais semideciduais no Triângulo Mineiro, Brasil. Caminhos de Geografia, vol. 14, no. 47, p. 233-242.).
Lopes et al. (2013)LOPES, SF., PRADO JUNIOR, JA., VALE, VS., and SCHIAVINI, I., 2013. Impactos ambientais antrópicos como modificadores da estrutura e funcionalidade de florestas estacionais semideciduais no Triângulo Mineiro, Brasil. Caminhos de Geografia, vol. 14, no. 47, p. 233-242. classified the areas according to disturbance severity (Table 2) from an impact matrix, in which were considered structural parameters such as abundance of pioneer species, canopy height, presence of large gaps or internal trails and selective logging, among others. Areas under lower disturbance severity have forests in advanced succession stages, fragments higher than 70 ha, with lower edge effect, absence of cattle and selective logging (Lopes et al., 2013LOPES, SF., PRADO JUNIOR, JA., VALE, VS., and SCHIAVINI, I., 2013. Impactos ambientais antrópicos como modificadores da estrutura e funcionalidade de florestas estacionais semideciduais no Triângulo Mineiro, Brasil. Caminhos de Geografia, vol. 14, no. 47, p. 233-242.). It present low number of pioneer species (below 10% of trees), high canopy (trees commonly higher than 25 m). Areas under intermediary disturbance, as well as the lower impact areas, present high canopy and low number of pioneer species, but are small fragments (lower than 30 ha), under a matrix strongly disturbed, have internal trails and livestock, which increases the trampling and grazing in the area, increasing its degradation (Lopes et al., 2013LOPES, SF., PRADO JUNIOR, JA., VALE, VS., and SCHIAVINI, I., 2013. Impactos ambientais antrópicos como modificadores da estrutura e funcionalidade de florestas estacionais semideciduais no Triângulo Mineiro, Brasil. Caminhos de Geografia, vol. 14, no. 47, p. 233-242.). Areas under higher disturbance severity are under a matrix strongly disturbed, presenting a large edge effect. They present the lowers canopies (lower than 17 m), higher number of pioneer species (near 25% of trees), have many internal trails and presence of cattle and selective logging (Lopes et al., 2013LOPES, SF., PRADO JUNIOR, JA., VALE, VS., and SCHIAVINI, I., 2013. Impactos ambientais antrópicos como modificadores da estrutura e funcionalidade de florestas estacionais semideciduais no Triângulo Mineiro, Brasil. Caminhos de Geografia, vol. 14, no. 47, p. 233-242.). For more details on sampling methodology and impact matrix description of ten areas can be found in Lopes et al. (2013).LOPES, SF., PRADO JUNIOR, JA., VALE, VS., and SCHIAVINI, I., 2013. Impactos ambientais antrópicos como modificadores da estrutura e funcionalidade de florestas estacionais semideciduais no Triângulo Mineiro, Brasil. Caminhos de Geografia, vol. 14, no. 47, p. 233-242.
Comparison between the mean SLA of species that occurred in at least two areas under different disturbance intensities.
Only the understory species with higher absolute densities were selected, until
they comprised at least 70% of the total density of this stratum. According to
Cornelissen et al. (2003) Cornelissen, JHC., Lavorel, S., Garnier, E., Díaz, S., Buchmann,
N., Gurvich, DE., Reich, PB., Steege, H., Morgan, HD., Heijden, MGA., Pausas,
JG. and Poorter, H., 2003. A handbook of protocols for standardised and easy
measurement of plant functional traits worldwide. Australian Journal of Botany,
vol. 51, no. 4, p. 335-380. http://dx.doi.org/10.1071/BT02124.
http://dx.doi.org/10.1071/BT02124...
, the most
representative species can be considered as those that summarize about 70-80% of
the total abundance in the community.
2.2 Functional leaf traits
Fully expanded leaves were harvested from adults with no obvious symptoms of
pathogen or herbivore attack. Twenty leaves were collected from each of 10
individuals by species in each study area. Leaves were packed in sealed plastic
bags to remain turgid until the measurement of leaf traits in the laboratory.
Leaves were scanned with a metric scale and subsequently, the leaf area (LA) was
calculated using the program ImageJ (NIH,
2014National Institutes of Health – NIHImageJ. Version 1.342014Available
from: <http://imagej.nih.gov/ij/>
http://imagej.nih.gov/ij/...
). The leaves were placed in an oven at 60 °C for 72 h before
measurement of leaf dry mass (DM). The SLA was calculated as the ratio LA
(mm²)/DM (mg).
For species with compound leaves, leaf traits were calculated for the leaf as a
whole, and not for the leaflets. According to Hulshof and Swenson (2010)Hulshof, CM. and Swenson, NG., 2010. Variation in leaf functional
trait values within and across individuals and species: an example from a Costa
Rican dry forest. Functional Ecology, vol. 24, no. 1, p. 217-223.
http://dx.doi.org/10.1111/j.1365-2435.2009.01614.x.
http://dx.doi.org/10.1111/j.1365-2435.20...
, the variability among leaflets is much
greater than that for whole leaves and, therefore, should be evaluated for the
leaf as a whole.
2.3 Influence of disturbance intensity in specific leaf area (SLA)
The SLA of species collected in at least two understories under different
disturbance intensities were compared by Student's t-tests. To evaluate the
influence of disturbance intensity on the SLA of the understory community
(SLAU) was used an adaptation from the Community-weighted mean
index (Garnier et al., 2004Garnier, E., Cortez, J., Billes, G., Navas, ML., Roumet, C.,
Debussche, M., Laurent, G., Blanchard, A., Aubry, D., Bellmann, A., Neill, C.
and Toussaint, JP., 2004. Plant functional markers capture ecosystem properties
during secondary succession. Ecology, vol. 85, no. 9, p. 2630-2637.
http://dx.doi.org/10.1890/03-0799.
http://dx.doi.org/10.1890/03-0799...
). This index
evaluates not only the mean of the species functional traits, but also the
relative contribution (abundance) of each species. The SLAU was
obtained using the Formula 1:
Where: pi = relative contribution of species i to the maximum abundance of the community; n = number of species evaluated; SLAi = SLA value of species i.
3 Results
3.1 The influence of disturbance intensity on specific leaf area (SLA)
For intraspecific analyses, from seven species sampled in at least two understories under different disturbance intensities, five species (Ardisia ambigua, Cheiloclinium cognatum, Siparuna guianensis, Siphoneugena densiflora and Trichilia catigua) differed significantly with a decrease in SLA on more disturbed understories (Table 2). Chrysophyllum gonocarpum had a higher SLA, with an increase of disturbance and Cordiera sessilis not differ significantly with the disturbance intensity (Table 2).
For interspecific analyses, there was a trend towards a reduction in the mean with an increase in disturbance intensity, particularly among understories under low and high disturbance (Figure 1 and Appendix 1 Appendix 1 Values of SLAsb of nine understories of semideciduous seasonal forests, obtained from the functional traits index. NI = number of individuals, NI/N = species relative density, SLA = specific leaf area (mm2.mg–1). Understories Species NI NI/N SLA NI/N × SLA Area 1 Chrysophyllum gonocarpum 30 0.25 12.91 3.25 Eugenia involucrata 28 0.24 16.52 3.89 Ardisia ambigua 13 0.11 14.62 1.6 Inga marginata 10 0.08 18.17 1.53 Chomelia pohliana 7 0.06 35.05 2.06 Allophylus racemosus 6 0.05 18.92 0.95 Acalypha gracilis 6 0.05 24.28 1.22 Quararibea turbinata 5 0.04 22.09 0.93 Calyptranthes widgreniana 4 0.03 13.21 0.44 Cheiloclinium cognatum * 3 0.03 12.85 0.32 Trichilia pallida * 3 0.03 22.06 0.56 Cordiera sessilis * 2 0.02 12.07 0.2 Eugenia subterminalis * 2 0.02 13.19 0.22 TOTAL 119 17.17 Area 2 Galipea jasminiflora 142 0.66 22.71 15.07 Trichilia catigua 28 0.13 14.59 1.91 Eugenia subterminalis 18 0.08 13.19 1.11 Eugenia ligustrina 17 0.08 14.86 1.18 Calyptranthes widgreniana * 3 0.01 13.21 0.19 Chomelia pohliana * 3 0.01 35.05 0.49 Maytenus floribunda * 1 < 0.01 10.56 0.05 Hirtella gracilipes * 1 < 0.01 17.03 0.08 Trichilia pallida * 1 < 0.01 22.06 0.10 TOTAL 214 20.18 Area 3 Siparuna guianensis 97 0.52 17.95 9.26 Cheiloclinium cognatum 36 0.19 12.83 2.46 Siphoneugena densiflora 18 0.10 10.39 0.99 Trichilia pallida 17 0.09 22.06 1.99 Cordiera sessilis 15 0.08 11.63 0.93 Trichilia catigua * 3 0.02 14.30 0.23 Campomanesia velutina * 2 0.01 23.03 0.25 TOTAL 188 16.11 Area 4 Siparuna guianensis 106 0.65 20.01 13.01 Cheiloclinium cognatum 32 0.20 13.68 2.69 Cordiera sessilis 11 0.07 12.01 0.81 Coussarea hydrangeifolia 11 0.07 19.6 1.32 Faramea hyacinthina * 2 0.01 12.66 0.16 Byrsonima laxiflora * 1 0.01 16.85 0.10 TOTAL 163 18.09 Area 5 Siparuna guianensis 131 0.66 17.41 11.4 Guapira opposita 29 0.15 24.36 3.53 Cordiera sessilis 9 0.05 11.93 0.54 Faramea hyacinthina 9 0.05 12.66 0.57 Cheiloclinium cognatum * 7 0.04 12.85 0.45 Trichilia catigua * 5 0.03 14.30 0.36 Eugenia ligustrina * 3 0.02 14.86 0.22 Coussarea hydrangeifolia * 3 0.02 20.02 0.30 Campomanesia velutina * 3 0.02 23.03 0.35 Chrysophyllum gonocarpum * 1 0.01 13.56 0.07 TOTAL 200 17.79 Area 6 Cheiloclinium cognatum 153 0.68 12.86 8.78 Siparuna guianensis 40 0.18 18.01 3.22 Siphoneugena densiflora 19 0.08 9.37 0.79 Cordiera sessilis * 3 0.01 12.07 0.16 Chomelia pohliana * 3 0.01 35.05 0.47 Trichilia catigua * 2 0.01 14.30 0.13 Trichilia pallida * 2 0.01 22.06 0.20 Allophylus sericeus * 1 < 0.01 18.92 0.08 Acalypha gracilis * 1 < 0.01 24.28 0.11 TOTAL 224 13.94 Area 7 Maytenus floribunda 25 0.18 11.06 2.09 Cordiera sessilis 25 0.18 11.51 2.09 Chrysophyllum gonocarpum 21 0.15 14.25 2.17 Hirtella gracilipes 21 0.15 17.03 2.59 Siparuna guianensis 14 0.10 16.20 1.64 Byrsonima laxiflora 8 0.06 16.85 0.98 Trichilia catigua 7 0.05 12.84 0.65 Ardisia ambigua 6 0.04 13.5 0.59 Eugenia involucrata * 3 0.02 16.52 0.36 Coussarea hydrangeifolia * 3 0.02 20.02 0.44 Campomanesia velutina * 2 0.01 23.03 0.33 Siphoneugena densiflora * 1 0.01 9.91 0.07 Trichilia pallida * 1 0.01 22.06 0.16 Chomelia pohliana * 1 0.01 35.05 0.25 TOTAL 138 14.32 Area 8 Cordiera sessilis 173 0.68 12.86 8.72 Campomanesia velutina 45 0.18 23.03 4.06 Maytenus floribunda 28 0.11 9.83 1.08 Siparuna guianensis * 4 0.02 18.84 0.30 Coussarea hydrangeifolia * 2 0.01 20.02 0.16 Cheiloclinium cognatum * 1 < 0.01 12.85 0.05 Allophylus sericeus * 1 < 0.01 18.92 0.07 Trichilia pallida * 1 < 0.01 22.06 0.09 TOTAL 225 14.53 Area 9 Cordiera sessilis 125 0.51 10.55 5.38 Cheiloclinium cognatum 79 0.32 11.73 3.78 Siphoneugena densiflora 13 0.05 8.79 0.47 Siparuna guianensis 13 0.05 18.95 1.01 Coussarea hydrangeifolia * 11 0.04 20.02 0.9 Trichilia pallida * 3 0.01 22.06 0.27 Maytenus floribunda * 1 < 0.01 10.56 0.04 TOTAL 245 11.85 * Is used to indicate the type of SLAs, with data obtained from other areas. ). The SLAU values obtained by the functional traits index ranged from 20.18 mm2.mg–1 (SLAA4, Area 4) to 11.85 mm2.mg–1 (SLAA5, Area 5). The less disturbed understories had a mean SLAU above 17 mm2 .mg–1 and the most disturbed understory had a SLAU below 15 mm2.mg–1. The greatest variation between the values of SLAU was observed for understories under medium disturbance intensity, where the highest was SLAA7 (18.09 mm2.mg–1) and the lowest, SLAA10 (13.94 mm2.mg–1).
Functional traits index (SLAU) of the nine areas of semideciduous forest sampled according to its classification as for disturbance intensity. Values correspond to values obtained in Appendix 1.
The species Siparuna guianensis (mean SLA = 18.84 mm2.mg–1) in Area 6, 7, 9 and Galipea jasminiflora mean SLA = 22.71 mm2.mg–1) in Area 4, represent more than half of the individuals in these areas, increasing their SLAU. In Area 1, from 13 species, six had a mean SLA greater than 18 mm2.mg–1 however, these represented only 31% of the relative density in this area. The high density (68%) of Cheiloclinium cognatum (mean SLA = 12.85 mm2.mg–1) was the main species responsible for the low SLAA10 in Area 10. In the three understories under a high intensity of disturbance (SLAA3,5,8), the species Cordiera sessilis (mean SLA = 12.07 mm2.mg–1), Cheiloclinium cognatum and Maytenus floribunda (mean SLA = 10.56 mm2.mg–1) had the highest relative densities in these areas, and a low SLAU. Although the values of SLAU differed substantially among the understories, species co-occurring with low and high SLA were observed in all of them, independently of the disturbance intensity.
4 Discussion
Species-specific leaf area in all understories (SLAU) and for the majority
of all species, decreased with an increase in the disturbance intensity,
corroborating our hypothesis. These results contradict those in the literature
(Reich et al., 2003Reich, PB., Wright, IJ., Cavender-Bares, J., Craine, JM., Oleksyn,
J., Westoby, M. and Walters, MB., 2003. The evolution of plant functional
variation: Traits, spectra, and strategies. International Journal of Plant
Sciences, vol. 164, no. S3, p. S143-S164.
http://dx.doi.org/10.1086/374368.
http://dx.doi.org/10.1086/374368...
; Garnier et al., 2004Garnier, E., Cortez, J., Billes, G., Navas, ML., Roumet, C.,
Debussche, M., Laurent, G., Blanchard, A., Aubry, D., Bellmann, A., Neill, C.
and Toussaint, JP., 2004. Plant functional markers capture ecosystem properties
during secondary succession. Ecology, vol. 85, no. 9, p. 2630-2637.
http://dx.doi.org/10.1890/03-0799.
http://dx.doi.org/10.1890/03-0799...
; Wright et al., 2004Wright, IJ., Reich, PB., Westoby, M., Ackerly, DD., Baruch, Z.,
Bongers, F., Cavender-Bares, J., Chapin, T., Cornelissen, JHC., Diemer, M.,
Flexas, J., Garnier, E., Groom, PK., Gulias, J., Hikosaka, K., Lamont, BB., Lee,
T., Lee, W., Lusk, C., Midgley, JJ., Navas, ML., Niinemets, U., Oleksyn, J.,
Osada, N., Poorter, H., Poot, P., Prior, L., Pyankov, VI., Roumet, C., Thomas,
SC., Tjoelker, MG., Veneklaas, EJ. and Villar, R., 2004. The worldwide leaf
economics spectrum. Nature, vol. 428, no. 6985, p. 821-827.
http://dx.doi.org/10.1038/nature02403. PMid:15103368
http://dx.doi.org/10.1038/nature02403...
; Fortunel
et al., 2009Fortunel, C., Garnier, E., Joffre, R., Kazakou, E., Quested, H.,
Grigulis, K., Lavorel, S., Ansquer, P., Castro, H., Cruz, P., Dolezal, J.,
Eriksson, O., Freitas, H., Golodets, C., Jouany, C., Kigel, J., Kleyer, M.,
Lehsten, V., Leps, J., Meier, T., Pakeman, R., Papadimitriou, M., Papanastasis,
VP., Quétier, F., Robson, M., Sternberg, M., Theau, JP., Thébault, A. and
Zarovali, M., 2009. Leaf traits capture the effects of land use changes and
climate on litter decomposability of grasslands across Europe. Ecology, vol. 90,
no. 3, p. 598-611. http://dx.doi.org/10.1890/08-0418.1.
PMid:19341132
http://dx.doi.org/10.1890/08-0418.1...
) and indicate a positive correlation of the community SLA
with disturbance intensity.
Interspecific studies comparing light-demanding pioneer and shade-tolerant species
show a higher SLA for the former as a consequence of their higher relative growth,
respiration rates and lower leaf longevity (Walters
and Reich, 1999Walters, MB. and Reich, PB., 1999. Low-light carbon balance and
shade tolerance in the seedlings of woody plants: do winter deciduous and
broad-leaved evergreen species differ? The New Phytologist, vol. 143, no. 1, p.
143-154. http://dx.doi.org/10.1046/j.1469-8137.1999.00425.x.
http://dx.doi.org/10.1046/j.1469-8137.19...
; Reich et al.,
2003Reich, PB., Wright, IJ., Cavender-Bares, J., Craine, JM., Oleksyn,
J., Westoby, M. and Walters, MB., 2003. The evolution of plant functional
variation: Traits, spectra, and strategies. International Journal of Plant
Sciences, vol. 164, no. S3, p. S143-S164.
http://dx.doi.org/10.1086/374368.
http://dx.doi.org/10.1086/374368...
). Thus, increases in the disturbance intensity increase the number
of forest pioneer species, probably the main cause for the increase in SLA in
disturbed communities. However, as we found in this study, these generalized
relationships might not be detected for understory species and should remain
tentative.
The light availability in the understory can influence the species SLA, since there
is a positive correlation between SLA and photosynthetic efficiency per leaf mass
(Evans and Poorter, 2001Evans, JR. and Poorter, H., 2001. Photosynthetic acclimation of
plants to growth irradiance: the relative importance of specific leaf area and
nitrogen partitioning in maximizing carbon gain. Plant, Cell & Environment,
vol. 24, no. 8, p. 755-767.
http://dx.doi.org/10.1046/j.1365-3040.2001.00724.x.
http://dx.doi.org/10.1046/j.1365-3040.20...
). Thus, the
increase in the SLA of understory species might favor their growth and reproduction
under low irradiation conditions of tropical forests, mostly in the form of unstable
beams of scattered light (sunflecks) (Chazdon and
Pearcy, 1991Chazdon, RL. and Pearcy, RW., 1991. The importance of sunflecks for
forest understory plants photosynthetic machinery appears adapted to brief,
unpredictable periods of radiation. Bioscience, vol. 41, no. 11, p. 760-766.
http://dx.doi.org/10.2307/1311725.
http://dx.doi.org/10.2307/1311725...
).
Leaves of the understory tend to be thinner, with a low biomass per unit of leaf
area, which increases the SLA, and therefore, the interception of light per unit
leaf biomass invested (Valladares and Niinemets,
2008Valladares, F. and Niinemets, U., 2008. Shade tolerance, a key plant
feature of complex nature and consequences. Annual Review of Ecology Evolution
and Systematics, vol. 39, no. 1, p. 237-257.
http://dx.doi.org/10.1146/annurev.ecolsys.39.110707.173506.
http://dx.doi.org/10.1146/annurev.ecolsy...
). This SLA increment in understory species is related to a
restricted investment into structural tissues such as the epidermis, which acts as a
protection mechanism for plants against photoinhibition (Pearcy, 2007Pearcy, RW., 2007. Responses of Plants to Heterogeneous Light
Environments. In PUGNAIRE, F. and VALLADARES, F. (Eds.). Functional plant
ecology. New York: Taylor & Francis Group. p. 213-258.
http://dx.doi.org/10.1201/9781420007626.ch7.
http://dx.doi.org/10.1201/9781420007626....
).
Schieving and Poorter (1999)Schieving, F. and Poorter, H., 1999. Carbon gain in a multispecies
canopy: the role of specific leaf area and photosynthetic nitrogen-use
efficiency in the tragedy of the commons. The New Phytologist, vol. 143, no. 1,
p. 201-211. http://dx.doi.org/10.1046/j.1469-8137.1999.00431.x.
http://dx.doi.org/10.1046/j.1469-8137.19...
simulated the
competition between plants of two similar genotypes in all traits, with the
exception of the SLA, in light gradient environments. These authors observed that
the genotype with the higher SLA also showed a higher carbon gain and replaced the
lower SLA genotype whenever light was limiting in the system.
The increase in light availability in disturbed forests understories, as a
consequence of the lower canopy height and gaps, causes physiological and
morphological responses to the understory species (Ishii and Asano, 2010Ishii, H. and Asano, S., 2010. The role of crown architecture, leaf
phenology and photosynthetic activity in promoting complementary use of light
among coexisting species in temperate forests. Ecological Research, vol. 25, no.
4, p. 715-722. http://dx.doi.org/10.1007/s11284-009-0668-4.
http://dx.doi.org/10.1007/s11284-009-066...
), which might involve a reduction in their SLA.
The greatest exposure to light favors the development of extra layers of palisade
tissue or the stretching of these layers, which results in an increase of biomass
per leaf area, and therefore, a reduction in SLA (Pearcy, 2007Pearcy, RW., 2007. Responses of Plants to Heterogeneous Light
Environments. In PUGNAIRE, F. and VALLADARES, F. (Eds.). Functional plant
ecology. New York: Taylor & Francis Group. p. 213-258.
http://dx.doi.org/10.1201/9781420007626.ch7.
http://dx.doi.org/10.1201/9781420007626....
).
When exposed to excessive light, damage to photosystem II, responsible for light
absorption for photosynthesis, occurs for understory species (Pearcy, 2007Pearcy, RW., 2007. Responses of Plants to Heterogeneous Light
Environments. In PUGNAIRE, F. and VALLADARES, F. (Eds.). Functional plant
ecology. New York: Taylor & Francis Group. p. 213-258.
http://dx.doi.org/10.1201/9781420007626.ch7.
http://dx.doi.org/10.1201/9781420007626....
). This process involves a dramatic reduction in
net photosynthesis, which reduces their competitive power (Poorter and Arets, 2003Poorter, L. and Arets, E., 2003. Light environment and tree
strategies in a Bolivian tropical moist forest: an evaluation of the light
partitioning hypothesis. Plant Ecology, vol. 166, no. 2, p. 295-306.
http://dx.doi.org/10.1023/A:1023295806147.
http://dx.doi.org/10.1023/A:102329580614...
; Pearcy, 2007Pearcy, RW., 2007. Responses of Plants to Heterogeneous Light
Environments. In PUGNAIRE, F. and VALLADARES, F. (Eds.). Functional plant
ecology. New York: Taylor & Francis Group. p. 213-258.
http://dx.doi.org/10.1201/9781420007626.ch7.
http://dx.doi.org/10.1201/9781420007626....
). Thus, the increase of disturbance and consequently, in
excessive light in understories, selects species with a thicker epidermis and higher
content of pigments such as xanthophyll, which assists in dissipating the excess
energy as heat (Koniger et al., 1995KÖniger, M., Harris, GC., Virgo, A. and Winter, K., 1995.
Xanthophyll-cycle pigments and photosynthetic capacity in tropical forest
species - a comparative field-study on canopy, gap and understory plants.
Oecologia, vol. 104, no. 3, p. 280-290.
http://dx.doi.org/10.1007/BF00328362.
http://dx.doi.org/10.1007/BF00328362...
; Cornelissen et al., 2003 Cornelissen, JHC., Lavorel, S., Garnier, E., Díaz, S., Buchmann,
N., Gurvich, DE., Reich, PB., Steege, H., Morgan, HD., Heijden, MGA., Pausas,
JG. and Poorter, H., 2003. A handbook of protocols for standardised and easy
measurement of plant functional traits worldwide. Australian Journal of Botany,
vol. 51, no. 4, p. 335-380. http://dx.doi.org/10.1071/BT02124.
http://dx.doi.org/10.1071/BT02124...
), to reduce
photoinhibition. This structural investment increases the biomass per unit leaf area
and thereby reduces the SLA in understories with high light exposure.
The large range in understory SLA might indicate the different resource exploration
in light capture (Reich et al., 2003Reich, PB., Wright, IJ., Cavender-Bares, J., Craine, JM., Oleksyn,
J., Westoby, M. and Walters, MB., 2003. The evolution of plant functional
variation: Traits, spectra, and strategies. International Journal of Plant
Sciences, vol. 164, no. S3, p. S143-S164.
http://dx.doi.org/10.1086/374368.
http://dx.doi.org/10.1086/374368...
). Even
in less-disturbed understories, natural gaps occur (Pearson et al., 2003Pearson, TRH., Burslem, DF., Goeriz, RE. and Dalling, JW., 2003.
Regeneration niche partitioning in neotropical pioneers: effects of gap size,
seasonal drought and herbivory on growth and survival. Oecologia, vol. 137, no.
3, p. 456-465. http://dx.doi.org/10.1007/s00442-003-1361-x.
PMid:12920642
http://dx.doi.org/10.1007/s00442-003-136...
), which increase the gradient of light in the
understory. This light gradient allows the occurrence of multiple strategies for
light capture, and the coexistence of a large number of species in forests
understories. Moreover, the occurrence of species with different functional traits
promotes functional stability in understories and increases its resilience (Folke et al., 2004Folke, C., Carpenter, S., Walker, B., Scheffer, M., Elmqvist, T.,
Gunderson, L. and Holling, CS., 2004. Regime shifts, resilience, and
biodiversity in ecosystem management. Annual Review of Ecology Evolution and
Systematics, vol. 35, no. 1, p. 557-581.
http://dx.doi.org/10.1146/annurev.ecolsys.35.021103.105711.
http://dx.doi.org/10.1146/annurev.ecolsy...
; Wright et al., 2004Wright, IJ., Reich, PB., Westoby, M., Ackerly, DD., Baruch, Z.,
Bongers, F., Cavender-Bares, J., Chapin, T., Cornelissen, JHC., Diemer, M.,
Flexas, J., Garnier, E., Groom, PK., Gulias, J., Hikosaka, K., Lamont, BB., Lee,
T., Lee, W., Lusk, C., Midgley, JJ., Navas, ML., Niinemets, U., Oleksyn, J.,
Osada, N., Poorter, H., Poot, P., Prior, L., Pyankov, VI., Roumet, C., Thomas,
SC., Tjoelker, MG., Veneklaas, EJ. and Villar, R., 2004. The worldwide leaf
economics spectrum. Nature, vol. 428, no. 6985, p. 821-827.
http://dx.doi.org/10.1038/nature02403. PMid:15103368
http://dx.doi.org/10.1038/nature02403...
), which allows the maintainance of its
ecological processes, even following changes in natural conditions.
The results of this study show that in communities under high disturbance intensity,
the functional response observed in the understories is a decrease in SLA for most
species and for the SLA of understory community. Thus, the evaluation of the SLA in
the understory level (SLAU) can be an important tool for the evaluation
of the conservation of the plant community. As the disturbances regional and even
global directly affect the functional traits of species (Craine et al., 2003Craine, JM., Wedin, DA., Chapin, FS. and Reich, PB., 2003.
Relationship between the structure of root systems and resource use for 11 North
American grassland plants. Plant Ecology, vol. 165, no. 1, p. 85-100.
http://dx.doi.org/10.1023/A:1021414615001.
http://dx.doi.org/10.1023/A:102141461500...
), evaluate the distribution patterns of
these traits in natural remnants may aid the understanding of ecological processes
and vegetation responses to future disturbances.
Acknowledgements
The authors would like to thank Fundo de Amparo a Pesquisa do Estado de Minas Gerais for financial support for this project (FAPEMIG process nº APQ-00694-08).
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Appendix 1 Values of SLAsb of nine understories of semideciduous seasonal forests, obtained from the functional traits index. NI = number of individuals, NI/N = species relative density, SLA = specific leaf area (mm2.mg–1).
Understories | Species | NI | NI/N | SLA | NI/N × SLA |
---|---|---|---|---|---|
Area 1 | Chrysophyllum gonocarpum | 30 | 0.25 | 12.91 | 3.25 |
Eugenia involucrata | 28 | 0.24 | 16.52 | 3.89 | |
Ardisia ambigua | 13 | 0.11 | 14.62 | 1.6 | |
Inga marginata | 10 | 0.08 | 18.17 | 1.53 | |
Chomelia pohliana | 7 | 0.06 | 35.05 | 2.06 | |
Allophylus racemosus | 6 | 0.05 | 18.92 | 0.95 | |
Acalypha gracilis | 6 | 0.05 | 24.28 | 1.22 | |
Quararibea turbinata | 5 | 0.04 | 22.09 | 0.93 | |
Calyptranthes widgreniana | 4 | 0.03 | 13.21 | 0.44 | |
Cheiloclinium cognatum * * Is used to indicate the type of SLAs, with data obtained from other areas. | 3 | 0.03 | 12.85 | 0.32 | |
Trichilia pallida * * Is used to indicate the type of SLAs, with data obtained from other areas. | 3 | 0.03 | 22.06 | 0.56 | |
Cordiera sessilis * * Is used to indicate the type of SLAs, with data obtained from other areas. | 2 | 0.02 | 12.07 | 0.2 | |
Eugenia subterminalis * * Is used to indicate the type of SLAs, with data obtained from other areas. | 2 | 0.02 | 13.19 | 0.22 | |
TOTAL | 119 | 17.17 | |||
Area 2 | Galipea jasminiflora | 142 | 0.66 | 22.71 | 15.07 |
Trichilia catigua | 28 | 0.13 | 14.59 | 1.91 | |
Eugenia subterminalis | 18 | 0.08 | 13.19 | 1.11 | |
Eugenia ligustrina | 17 | 0.08 | 14.86 | 1.18 | |
Calyptranthes widgreniana * * Is used to indicate the type of SLAs, with data obtained from other areas. | 3 | 0.01 | 13.21 | 0.19 | |
Chomelia pohliana * * Is used to indicate the type of SLAs, with data obtained from other areas. | 3 | 0.01 | 35.05 | 0.49 | |
Maytenus floribunda * * Is used to indicate the type of SLAs, with data obtained from other areas. | 1 | < 0.01 | 10.56 | 0.05 | |
Hirtella gracilipes * * Is used to indicate the type of SLAs, with data obtained from other areas. | 1 | < 0.01 | 17.03 | 0.08 | |
Trichilia pallida * * Is used to indicate the type of SLAs, with data obtained from other areas. | 1 | < 0.01 | 22.06 | 0.10 | |
TOTAL | 214 | 20.18 | |||
Area 3 | Siparuna guianensis | 97 | 0.52 | 17.95 | 9.26 |
Cheiloclinium cognatum | 36 | 0.19 | 12.83 | 2.46 | |
Siphoneugena densiflora | 18 | 0.10 | 10.39 | 0.99 | |
Trichilia pallida | 17 | 0.09 | 22.06 | 1.99 | |
Cordiera sessilis | 15 | 0.08 | 11.63 | 0.93 | |
Trichilia catigua * * Is used to indicate the type of SLAs, with data obtained from other areas. | 3 | 0.02 | 14.30 | 0.23 | |
Campomanesia velutina * * Is used to indicate the type of SLAs, with data obtained from other areas. | 2 | 0.01 | 23.03 | 0.25 | |
TOTAL | 188 | 16.11 | |||
Area 4 | Siparuna guianensis | 106 | 0.65 | 20.01 | 13.01 |
Cheiloclinium cognatum | 32 | 0.20 | 13.68 | 2.69 | |
Cordiera sessilis | 11 | 0.07 | 12.01 | 0.81 | |
Coussarea hydrangeifolia | 11 | 0.07 | 19.6 | 1.32 | |
Faramea hyacinthina * * Is used to indicate the type of SLAs, with data obtained from other areas. | 2 | 0.01 | 12.66 | 0.16 | |
Byrsonima laxiflora * * Is used to indicate the type of SLAs, with data obtained from other areas. | 1 | 0.01 | 16.85 | 0.10 | |
TOTAL | 163 | 18.09 | |||
Area 5 | Siparuna guianensis | 131 | 0.66 | 17.41 | 11.4 |
Guapira opposita | 29 | 0.15 | 24.36 | 3.53 | |
Cordiera sessilis | 9 | 0.05 | 11.93 | 0.54 | |
Faramea hyacinthina | 9 | 0.05 | 12.66 | 0.57 | |
Cheiloclinium cognatum * * Is used to indicate the type of SLAs, with data obtained from other areas. | 7 | 0.04 | 12.85 | 0.45 | |
Trichilia catigua * * Is used to indicate the type of SLAs, with data obtained from other areas. | 5 | 0.03 | 14.30 | 0.36 | |
Eugenia ligustrina * * Is used to indicate the type of SLAs, with data obtained from other areas. | 3 | 0.02 | 14.86 | 0.22 | |
Coussarea hydrangeifolia * * Is used to indicate the type of SLAs, with data obtained from other areas. | 3 | 0.02 | 20.02 | 0.30 | |
Campomanesia velutina * * Is used to indicate the type of SLAs, with data obtained from other areas. | 3 | 0.02 | 23.03 | 0.35 | |
Chrysophyllum gonocarpum * * Is used to indicate the type of SLAs, with data obtained from other areas. | 1 | 0.01 | 13.56 | 0.07 | |
TOTAL | 200 | 17.79 | |||
Area 6 | Cheiloclinium cognatum | 153 | 0.68 | 12.86 | 8.78 |
Siparuna guianensis | 40 | 0.18 | 18.01 | 3.22 | |
Siphoneugena densiflora | 19 | 0.08 | 9.37 | 0.79 | |
Cordiera sessilis * * Is used to indicate the type of SLAs, with data obtained from other areas. | 3 | 0.01 | 12.07 | 0.16 | |
Chomelia pohliana * * Is used to indicate the type of SLAs, with data obtained from other areas. | 3 | 0.01 | 35.05 | 0.47 | |
Trichilia catigua * * Is used to indicate the type of SLAs, with data obtained from other areas. | 2 | 0.01 | 14.30 | 0.13 | |
Trichilia pallida * * Is used to indicate the type of SLAs, with data obtained from other areas. | 2 | 0.01 | 22.06 | 0.20 | |
Allophylus sericeus * * Is used to indicate the type of SLAs, with data obtained from other areas. | 1 | < 0.01 | 18.92 | 0.08 | |
Acalypha gracilis * * Is used to indicate the type of SLAs, with data obtained from other areas. | 1 | < 0.01 | 24.28 | 0.11 | |
TOTAL | 224 | 13.94 | |||
Area 7 | Maytenus floribunda | 25 | 0.18 | 11.06 | 2.09 |
Cordiera sessilis | 25 | 0.18 | 11.51 | 2.09 | |
Chrysophyllum gonocarpum | 21 | 0.15 | 14.25 | 2.17 | |
Hirtella gracilipes | 21 | 0.15 | 17.03 | 2.59 | |
Siparuna guianensis | 14 | 0.10 | 16.20 | 1.64 | |
Byrsonima laxiflora | 8 | 0.06 | 16.85 | 0.98 | |
Trichilia catigua | 7 | 0.05 | 12.84 | 0.65 | |
Ardisia ambigua | 6 | 0.04 | 13.5 | 0.59 | |
Eugenia involucrata * * Is used to indicate the type of SLAs, with data obtained from other areas. | 3 | 0.02 | 16.52 | 0.36 | |
Coussarea hydrangeifolia * * Is used to indicate the type of SLAs, with data obtained from other areas. | 3 | 0.02 | 20.02 | 0.44 | |
Campomanesia velutina * * Is used to indicate the type of SLAs, with data obtained from other areas. | 2 | 0.01 | 23.03 | 0.33 | |
Siphoneugena densiflora * * Is used to indicate the type of SLAs, with data obtained from other areas. | 1 | 0.01 | 9.91 | 0.07 | |
Trichilia pallida * * Is used to indicate the type of SLAs, with data obtained from other areas. | 1 | 0.01 | 22.06 | 0.16 | |
Chomelia pohliana * * Is used to indicate the type of SLAs, with data obtained from other areas. | 1 | 0.01 | 35.05 | 0.25 | |
TOTAL | 138 | 14.32 | |||
Area 8 | Cordiera sessilis | 173 | 0.68 | 12.86 | 8.72 |
Campomanesia velutina | 45 | 0.18 | 23.03 | 4.06 | |
Maytenus floribunda | 28 | 0.11 | 9.83 | 1.08 | |
Siparuna guianensis * * Is used to indicate the type of SLAs, with data obtained from other areas. | 4 | 0.02 | 18.84 | 0.30 | |
Coussarea hydrangeifolia * * Is used to indicate the type of SLAs, with data obtained from other areas. | 2 | 0.01 | 20.02 | 0.16 | |
Cheiloclinium cognatum * * Is used to indicate the type of SLAs, with data obtained from other areas. | 1 | < 0.01 | 12.85 | 0.05 | |
Allophylus sericeus * * Is used to indicate the type of SLAs, with data obtained from other areas. | 1 | < 0.01 | 18.92 | 0.07 | |
Trichilia pallida * * Is used to indicate the type of SLAs, with data obtained from other areas. | 1 | < 0.01 | 22.06 | 0.09 | |
TOTAL | 225 | 14.53 | |||
Area 9 | Cordiera sessilis | 125 | 0.51 | 10.55 | 5.38 |
Cheiloclinium cognatum | 79 | 0.32 | 11.73 | 3.78 | |
Siphoneugena densiflora | 13 | 0.05 | 8.79 | 0.47 | |
Siparuna guianensis | 13 | 0.05 | 18.95 | 1.01 | |
Coussarea hydrangeifolia * * Is used to indicate the type of SLAs, with data obtained from other areas. | 11 | 0.04 | 20.02 | 0.9 | |
Trichilia pallida * * Is used to indicate the type of SLAs, with data obtained from other areas. | 3 | 0.01 | 22.06 | 0.27 | |
Maytenus floribunda * * Is used to indicate the type of SLAs, with data obtained from other areas. | 1 | < 0.01 | 10.56 | 0.04 | |
TOTAL | 245 | 11.85 |
-
(With 1 figure)
Publication Dates
-
Publication in this collection
May 2015
History
-
Received
16 July 2013 -
Accepted
21 Jan 2014