On-line version ISSN 2236-8906
Hoehnea vol.39 no.1 São Paulo Mar. 2012
Déficit hídrico interfere nos vasos do lenho de Croton floribundus Spreng. em diferentes tipos de vegetação, SP, Brasil
Eduardo Luiz Longui*; Diego Romeiro; Luana Naves Testoni; Osny Tadeu de Aguiar; Roque Cielo Filho; Israel Luiz de Lima; Sandra Monteiro Borges Florsheim
Instituto Florestal, Caixa Postal 1322, 02377-000 São Paulo, SP, Brasil
In this paper we showed that water deficit affects the wood vessels of Croton floribundus in five areas with different vegetation types: Rain Forest, Semi-deciduous Forest and Woody Savanna. We concluded that variations in the vessels are due especially to water deficit and the number of months with water deficit. Larger diameter vessels occurred in areas with higher water deficit, which may represent a strategy to optimize the water transport in favorable periods. Vessels with smaller diameters occur in areas with lower deficit, which may be related to lower minimum temperatures and frost occurrence, which like drought can cause vessel embolism. In Caetetus Ecological Station, a Semi-deciduous Forest (area of highest water deficit), we observed investments in efficiency and safety, with the occurrence of larger diameter vessels associated with one of the lowest vulnerability indexes and highest proportions of multiple vessels of four or more elements.
Key words: Ecological anatomy, mesomorphy, vulnerability, water availability
O déficit hídrico influenciou na formação dos vasos da madeira de Croton floribundus ocorrentes em cinco áreas com as seguintes vegetações: Floresta Ombrófila, Floresta Estacional Semidecidual e Cerradão. As variações dos vasos devem-se especialmente ao déficit hídrico e número de meses com déficit hídrico. Vasos de maior diâmetro ocorreram em áreas com maior déficit hídrico, o que pode indicar uma estratégia para otimizar o transporte de água em épocas favoráveis. Vasos com menores diâmetros ocorreram em áreas com menor déficit hídrico, possivelmente influenciados pelas menores temperaturas mínimas e a ocorrência de geadas, que semelhante a seca, causa a embolia dos vasos. Na Estação Ecológica de Caetetus, Floresta Estacional Semidecidual (área com maior déficit de água) observaram-se investimentos em eficiência e segurança, com a ocorrência de vasos de maior diâmetro associados a um dos menores índices de vulnerabilidade e maior proporção de vasos múltiplos de quatro ou mais elementos.
Palavras-chave: Anatomia ecológica, disponibilidade hídrica, mesomorfia, vulnerabilidade
In this study we aimed to identify variations in the vessel features of Croton floribundus Spreng. wood with respect to variations in climatic data, especially the water deficit. We hypothesized that vessels show features related to greater safety in water transport in dry environments and are related to water deficit.
Expanding knowledge about the influence of water deficit in Brazilian native trees is important, because the water deficiency is one of the main factors that limit plant growth due to its influence on photosynthesis, production of sugars employed in produce energy and the construction of cell walls. Thus, the efficient water transport in plants allows for increased photosynthetic uptake of CO2 for a given vascular investment and should improve fitness through enhanced growth and reproduction (Pittermann et al. 2005). The availability of water interferes in the formation of wood cells, especially vessel elements, the responsible cells for the water transport in angiosperms. In this context, trees have variations in size, frequency and vessel elements grouping as an adaptive response to the environment, tending to a greater efficiency or safety depending on water availability (Carlquist 2001).
Vessels with a smaller diameter are safer in water transport, while larger vessels are more efficient, which can increase the capacity of photosynthesis (Hacke et al. 2005, Carlquist 2001). According to Tyree et al. (1994), the law of Hagen-Poiseuille, which assesses the dynamics of fluids through cylindrical tubes, also serves to explain the water flow through the wood vessels, which can also be compared to pipes. According to the authors, one vessel with 40 µm diameter is as conductive as 16 vessels with 20 µm diameter each or as 256 vessels with 10 µm diameter each. Moreover, historically vessels with smaller diameters are associated with drier or colder environments (Baas 1982, Carlquist 2001). There is also a trend towards an increase in vessel grouping in areas of high water deficit (Carlquist & Hoekman 1985, Fahn et al. 1986).
Aiming to evaluate ecological trends and the susceptibility of wood vessels to develop embolism, Carlquist (2001) introduced some indexes as ecological indicators: vulnerability index (VI); mesomorphy index (MI) and vessel grouping index (VGI). Based on these indicators, it is determined that vulnerability index lower than one (< 1) reflect adaption to drier areas, while values greater than three (> 3) are found in plants living in areas with high water availability (Carlquist 2001). For mesomorphy index, values less than 100 indicate plants that grow in dry environments (xeric) or in regions with a dry period for several months in the year, while higher mesomorphy index values are found in species that grow in mesic environments (Carlquist 2001, Lens et al. 2003). For vessel grouping index, the value of one (> 1) indicates exclusively solitary vessels; beyond that, as higher the value, greater is the vessel grouping index. Therefore plants adapted to water stress environments have higher vessel grouping index (Carlquist 2001).
Due to the wide distribution and occurrence in different vegetation types, Croton floribundus Spreng. (Euphorbiaceae) becomes an interesting species for studies of ecological wood anatomy and evaluation of the ecological indexes mentioned. The species is pioneer, heliophyte, deciduous or semi-deciduous; has very fast growth and short life cycle, and does not tolerate low temperatures. C. floribundus naturally occurs in different vegetations in São Paulo State, as rain forest, semi-deciduous forest and woody savanna (Durigan et al. 1997, Lorenzi 2002, Carvalho 2003). These vegetations have distinct characteristics of precipitation, temperature and water deficit, enabling assessment of anatomical aspects under different environmental conditions, which in turn contributes to increase the ecological knowledge of this species.
Material and methods
Experimental areas - The samples was collected in five areas of the São Paulo State: 1. Cantareira State Park (CSP), 2. Carlos Botelho State Park (CBSP), 3. Itapeva Experimental Station (IES), 4. Assis Ecological Station (AES) and 5. Caetetus Ecological Station (CES) (figure 1, table 1).
Tree sampling - Wood samples were collected at breast height (DBH - 1.30 m) of three trees from each area with estimated heights between 5-8 m, totaling 15 trees. Samples were collected between April and July, the beginning of the drier season in all areas (figure 2). BBH, means of DBH and xylarium number of Croton floribundus trees are described on table 2. Anatomical analysis - Blocks of 1.5 cm3 were cut from each sample. The blocks were softened in boiling water and glycerin (4:1), and 15-20 µm thick sections were prepared on a sliding microtome. The transverse and longitudinal sections (A) were bleached with sodium hypochlorite (60%), washed in water, and stained with safranin (1%) (Johansen 1940). Macerations (B) were prepared according to the modified Franklin method (Berlyn & Miksche 1976). A and B were stained with aqueous safranin and mounted in a solution of water and glycerin (1:1). The terminology followed the IAWA list (IAWA Committee 1989).
Slides were prepared for the analysis and measurement of the following anatomical features: diameter, frequency and vessel element length, diameter of intervessel pits and vessel-ray pits. For each feature n = 25 was used initially, except for the pits, where n = 10 was adopted.
We investigated the vulnerability (VI), mesomorphy (MI) and vessel grouping index (VGI) (Carquist 2001). According to the formulas:
Where: VD: vessel diameter. VF: vessel frequency, VEL: Vessel element length. VG: Vessel grouping (solitary, multiples of 2, 3 and multiples of 4 or more vessels).
The percentage of vessel area was determined on transverse sections in 25 squares of 1 mm2 each, distributed among the sections of each sample.
All anatomical measures were performed on a microscope (Olympus CX 31) equipped with a camera (Olympus Evolt E330) and a computer with image analyzer software (Image-Pro 6.3). Statistical analysis - We initially performed descriptive statistical analysis and comparison between means and standard deviations to test the differences between the groups. With the results, "t-test sample size" were used to determine the number of measurements to the power 0.8. For comparison of each anatomical feature, based on the normal distribution of data, a parametric analysis of variance (One Way Analysis of Variance) was performed. When a significant difference was observed, Tukey test to identify pairs of significantly different means were used. Relation among vessel features, indexes and the climatic data were perfomed by linear regression.
Regardless of experimental area, the vessel elements have simple perforation plate; there are elements without and with tails at one or both ends (figure 3a). Intervessel pits with medium size, alternate (figure 3b); vessel-ray pits similar to intervessel pits (figure 3c). The specimens have diffuse pores (figures 5a-e).
There are quantitative differences among the sampling areas in all the anatomical features studied. Vessel diameter was wider in CES (figure 4a); shorter vessel element length and less frequent vessels in CSP (figure 4b-c), see transverse sections in figure 5.
All ecological indexes showed variation among the areas (figure 7a-c). The vessel grouping (figure 8) differed among study areas, mostly solitary vessels were observed only in IES samples. The lowest percentage of solitary vessels was noted in the samples of CBSP. The percentage of vessels multiples of two and three did not vary among the samples of different areas, whereas the highest percentage of vessels multiples of four or more occurred in the samples of CBSP, AES and CES (figure 8).
All significant relations were positive (table 3). The Vessel diameter was related with the mean temperature (MT), mean minimum temperature (MMT), water deficit (WD) and months with water deficit (MWD). The vulnerability index was related with MMT and MWD while the mesomorphy index was correlated with the MMT, WD and MWD.
The samples of this study were collected at the beginning of the dry season between April and June, so all samples examined were from between growth layers, i. e., formed before the cambium cessation when the plants had water available.
The qualitative vessels features corroborate Pollito (2004) for the presence of simple perforation plates and for the type of pits. The vessel diameter was related positively with temperature (table 3), indicating that higher temperatures, such as occur at CES, are associated with larger vessel sizes. Moreover, the positive relation between vessel diameters with water deficit (WD) and the number of months with water deficit (MWD) indicates that plants from areas with higher values of water deficit and number of months with water deficit develop vessels with a larger diameter (efficiency), a contrary result of many studies in ecological wood anatomy.
We suggest that our results may represent a strategy of these plants to optimize the water transport in months with adequate rainfall to grow. Plants of the CES, e.g., have four months with water deficit, in seven months of dry period in which there is no surplus water. Thus, these plants have only five months during the year to grow in appropriate water conditions (figure 2e).
Vessels with smaller diameters, safer and less efficient in water conduction, occurred in CBSP and IES. However, these two areas have the lowest values of water deficit and number of months with water deficit per year, with water available almost all year-round. Under these conditions we expected find vessels of larger diameter (more efficient); a possible explanation for the smaller vessel diameter in CBSP and IES are the lowest minimum temperatures and frost occurrence, which similar to an event such as drought, can cause vessel embolism (Carlquist 2001).
This result was reinforced by the positive relation between vessel diameter and minimum temperatures (table 3) indicating the largest diameter of the vessels in areas with higher MMT. Vessels with smaller diameters (safer) could represent a strategy to avoid xylem cavitation (Hacke et al. 2005), even without apparent risk of water deficits in the CBSP and IES. Martinez-Vilalta & Pockman (2002) observed that the cavitation induced by freezing is a limiting factor for the distribution of populations of Larrea tridentata (Sessé & Moc. ex DC.) Coville, which shows the potential importance of frost in the xylem anatomy.
To estimate the potential area of water transport, we measured the vessel area percentage in 1 mm2 . The highest values occurred in the IES, AES and CES. According to the climatic data, apparently, we did not observe any obvious feature shared by these three areas (table 1) because they are distinct in water deficit, precipitation and temperature.
These three areas have lower altitudes, but we do not believe that this feature should significantly influence the formation of wood in the direction of greater potential area of water transport. Additionally, CSP presents climatic characteristics related to water availability consistent with a greater area of vessels, despite showing the lowest value for this variable among study areas. One possible explanation for these results could be found from the analysis of soils, particularly water availability (Oliveira & Peichl 1986). Soils with low water availability, due to low water holding capacity or a higher position on the local topography, could counterbalance the small water deficit in the IES, inducing greater water transport than what would be expected based on the climatic characteristics of the study area. The mechanism of action could account for less potential of water transport observed in the CSP.
We did not observe any relation between the length and frequency of vessel elements of C. floribundus with the environmental variables. The lower frequency occurred in the CSP. In contrast, Longui et al. (2009a) found a higher vessel frequency in the CSP in Piptadenia gonoacantha (Mart.) J.F. Macbr. collected in CSP at CES. Studies show that vessel frequency is inversely proportional to vessel diameter (Baas et al. 2004). In the present study this relationship was not observed, because the vessel frequency did not change in four areas (except in CSP), but the diameter varied. These results show that the relation frequency / diameter differs between species and that only with regards the frequency is difficult to establish a generalized trend in the adaptation of vessels to the environment.
Apparently the pit diameter in C. floribundus does not show an eco-anatomical response related to environmental variables because the values revealed no trends among the five areas. According IAWA Committee (1989), C. floribundus pits have medium (7-10 µm) to large (> 10 µm) diameter. Dickison (2000) mentions that in addition to vessel diameter, the danger of embolism is mainly related to the pit features. Thus, small pits (Baas et al. 1982), with small size apertures (Tyree et al. 1994; Sperry & Hacke 2004) offer a strategy to reduce the occurrence of cavitation, regardless of vessel size. Luchi (2004), studying Croton urucurana Baill. in soils with different moisture levels, found larger pits in specimens of wetland.
The positive relations between the vulnerability index with months with water deficit and mean minimum temperature and between mesomorphy index with water deficit, months with water deficit and mean minimum temperature (table 3) indicate a greater efficiency in more restrictive areas to the availability of water.
As mentioned in the introduction, vulnerability index values < 1 reflect high safe, while values > 3 are found in plants with highly efficient water transport (Carlquist 2001). We interpret that lower vulnerability index, the greater xylem safety. The CES and CSP are the two areas with the highest months with water deficit and without water surplus. In both areas there were the two higher vulnerability index (figure 7a). This index reflects that wood of CES and CSP is more efficient in transport to water, but more vulnerable to embolism in relation to the other three areas. Longui et al. (2009a), in Piptadenia gonoacantha (Mart.) J.F.Macbr., noted higher vulnerability index at CES with respect to the CSP.
We emphasize that the plants of CBSP, IES and AES showed lower values of vessel grouping index, and CBSP the lowest percentage of solitary vessels although Carlquist & Hoekman (1985) and Fahn et al. (1986) report that there is a tendency for greater vessel grouping in environments with higher water deficit. This conflict between the largest vessels grouping in an environment without water deficit, such as CBSP, might be explained, as previously mentioned, by low temperatures and frost, contributing in part to the results found for the grouping.
With respect to mesomorphy index, which relates mesic and xeric conditions, in Brazilian forests are moisture gradients with different climatic conditions. Thus we consider that plants adapted to mesic conditions present higher mesomorphy index in areas with a more humid climate. However, in the present study, the largest mesomorphy index occurred at CES and the CSP, both areas with high water deficit; according to the above we expected lower mesomorphy index in these areas.
According to Carlquist (2001), the higher value of vessel grouping index, up to 1, is the better adaptation to water stress. We did not observe a clear trend for the vessel grouping index, because the two areas with high water deficit have significantly different vessel grouping index: CSP showed lower vessel grouping index compared to CES. However, CSP did not differ from IES and CES did not differ from CBSP, the other two areas did not present apparent water restriction (figure 2). Noshiro & Baas (2000) also found no relations between vessel grouping index and the average temperature and precipitation in species of the genus Cornus. In this study, vessel grouping index was not a good indicator of eco-anatomical responses.
Regarding the vessels grouping, considering only CSP and CES, the latter seems to have an advantage in wood safety with a higher percentage of vessel multiples of 4 or more than the former (figure 8), a feature that can compensate for the larger vessel diameter. Marcati et al. (2001), in a study of Copaifera langsdorffii Desf. in forest and savanna, mentioned that specimens from savanna showed greater vessel diameter than the specimens from the forest, but trees in the savanna were also found a higher vessel frequency.
In the present study, there was no relation between precipitation and vessel features. On the other hand, the water deficit and number of months with deficit shows five significant relations, suggesting greater attention to these environmental data in the interpretation of changes in the wood vessels.
Besides the influence of the environment, changes in vessel diameter can also be caused by the radial position and reflect the changes between juvenile and mature wood, being influenced by the maturity of the vascular cambium (Tsoumis 1968). In many species of Brazilian tree an increase in vessel diameter in the direction of bark is reported, e.g., Longui et al. (2009b) in Luehea divaricata Mart. and Lima et al. (2010) also in Croton floribundus with different samples from CSP.
Our hypothesis was partially confirmed, because were observed larger diameter vessels in areas with higher water deficit, this results is not common in literature. We suggested a strategy to optimize the use of water in favorable periods. Vessels with smaller diameters occurred in areas with lower water deficit, we infer a relationship with lower minimum temperatures and frost occurrence, which similar to drought event may cause vessel embolism. In Caetetus Ecological Station semi-deciduous forest (area of highest water deficit) we observed investments in efficiency (a) and safety (b): a) larger diameter vessels associated with b) one of the lowest vulnerability index and highest proportions of vessel multiples of four or more elements. These conclusions emphasize the importance of variations in diameter and frequency of vessel and vessel grouping to adjust the water transport under diverse environmental conditions.
We are very grateful to Dr. João Batista Baitello, Dr. Antônio Carlos Galvão de Melo for their contribution in fieldwork; and to Sonia Godói Campião for laboratory assistance.
Baas, P. 1982. Systematic, phylogenetic, and ecological wood anatomy - History and perspectives. In: P. BAAS (ed.). New perspectives in wood anatomy. Nijhoff/Junk, The Hague/Hingham, pp. 23-58. [ Links ]
Baas, P., Ewers, F.W., Davis, S.D. & Wheeler, E.A. 2004. Evolution of xylem physiology. In: I. Poole & A. Hemsley (eds.). Evolution of Plant Physiology. Elsevier Academic Press, London, pp. 273-295. [ Links ]
Berlyn, G.P. & Miksche, J.P. 1976. Botanical microtechnique and cytochemistry. The Iowa University Press, Iowa. [ Links ]
Carlquist, S. & Hoekman, D.A. 1985. Ecological wood anatomy of the woody Southern Californian flora. IAWA Bulletin 6:319-347. [ Links ]
Carlquist, S. 2001. Comparative wood anatomy: systematic, ecological and evolutionary aspects of dicotyledon wood. 2 ed. Springer Verlag, Berlin. [ Links ]
Carvalho, P.E.R. 2003. Espécies Arbóreas Brasileiras. Brasília: Embrapa Informação Tecnológica, Embrapa Florestas, Colombo. [ Links ]
CEPAGRI (Centro de pesquisas meteorológicas e climáticas aplicadas à agricultura). 2010. Clima dos Municípios Paulistas. http://www.cpa.unicamp.br/outras-informacoes/clima-dos-municipiospaulistas.html (acesso em 07.10.2010). [ Links ]
Dickison, W.C. 2000. Integrative plant anatomy. Academic Press, San Diego. [ Links ]
Durigan, G., Figliolia, M.B., Kawabata, M., Garrido, M.A.O. & Baitello, J.B. 1997. Sementes e mudas de árvores tropicais. Páginas e Letras, São Paulo. [ Links ]
Fahn, A., Werker, E. & Baas, P. 1986. Wood anatomy and identification of trees and shrubs from Israel and adjacent regions. The Israel Academy of Sciences and Humanities, Jerusalem. [ Links ]
Hacke, U.G., Sperry, J.S. & Pittermann, J. 2005. Efficiency versus safety tradeoffs for water conduction in angiosperm vessels versus gymnosperm tracheids. In: N.M. Holbrook & M.A. Zwienniecki (eds.). Vascular transport in plants. Elsevier Inc., Amsterdam, pp. 333-354. [ Links ]
Iawa Committee. 1989. IAWA list of microscopic features for hardwood identification. IAWA Bulletin 10:219-332. [ Links ]
Johansen, D.A. 1940. Plant microtechnique. McGraw-Hill Book, New York. [ Links ]
Lens, F., Gasson, P. Smets & E. Jansen, S. 2003. Comparative wood anatomy of Epacrids (Styphelioideae, Ericaceae s.l). Annals of Botany 91:835-856. [ Links ]
Lima, I.L., Zanon, B.R., Longui, E.L. & Florsheim, S.M.B. 2010. Variação radial da densidade básica e dimensões celulares de Croton floribundus. Floresta 40:663-671. [ Links ]
Longui, E.L., Bufolo, A., Aguiar, O.T., Lima, I.L. & Florsheim, S.M.B. 2009a. Anatomia comparada do lenho de Piptadenia gonoacantha (Mart.) J.F.Macbr. em dois tipos de vegetação. Hoehnea 36:715-724. [ Links ]
Longui, E.L., Lima, I.L., Florsheim, S.M.B. & Bufolo, A. 2009b. Variação anatômica radial do lenho de açoita-cavalo (Luehea divaricata) e sua influência na densidade aparente. Revista do Instituto Florestal 21:181-190. [ Links ]
Lorenzi, H. 2002. Árvores Brasileiras: manual de identificação e cultivo de plantas arbóreas do Brasil. 2 ed. Plantarum, Nova Odessa. [ Links ]
Luchi, A.E. 2004. Anatomia do lenho de Croton urucurana Baill. (Euphorbiaceae) de solos com diferentes níveis de umidade. Revista Brasileira de Botânica 27:271-280. [ Links ]
Marcati, C.R., Angyalossy-Alfonso, V. & Benetati, L. 2001. Anatomia comparada do lenho de Copaifera langsdorffii Desf. (Leguminosae-Caesalpinoideae) de floresta e cerradão. Revista Brasileira de Botânica 24:311-320. [ Links ]
Martínez-Vilalta, J. & Pockman, W.T. 2002. The vulnerability to freezing-induced xylem cavitation of Larrea tridentata (Zygophyllaceae) in the Chihuahuan desert. American Journal of Botany. 89:1916-1924. [ Links ]
Noshiro, S. & Baas, P. 2000. Latitudinal trends in wood anatomy within species and genera: case study in Cornus S.L. (Cornaceae). American Journal of Botany 87:1495-1506. [ Links ]
Oliveira, L.P. & Peichl, B. 1986. Solos e conservação. In: J.L. Nagy (org). Manual do Técnico Florestal: apostilas do Colégio Florestal de Irati, v. 1. Ingra S.A., Campo Largo. [ Links ]
Pittermann, J., Sperry, J.S., Hacke, U.G., Wheeler, J.K. & Sikkema, E.H. 2005. Torus-Margo Pits Help Conifers Compete with Angiosperms. Science 310:1924. [ Links ]
Pollito, P.A.Z. 2004. Dendrologia, anatomia do lenho e "status" de conservação das espécies lenhosas dos gêneros Cinchona, Croton e Uncari no estado do Acre, Brasil. Tese de doutorado, Universidade de São Paulo, Piracicaba. [ Links ]
Rossi, M., Faria, A.J., Wenzel, R., Câmara, C.D., Arcova, F.C.S., Cicco, V., Ranzini, M., Luiz, R.A.F., Santos, J.B.A., Souza, L.F.S. & Veneziani, Y. 2009. Avaliação do meio físico. In: C. Leonel (coord.) Plano de Manejo do Parque Estadual Alberto Löfgren. Instituto Florestal, São Paulo, pp. 69-107. [ Links ]
Sperry, J.S. & Hacke, U.G. 2004. Analysis of circular bordered pit function I. Angiosperm vessels with homogenous pit membranes. American Journal of Botany 91:369-385. [ Links ]
Tsoumis, G. 1968. Wood as raw material. Pergamon Press, Oxford. [ Links ]
Tyree, M.T., Davis, S.D. & Gochard, H. 1994. Biophysical perspectives of xylem evolution: is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction? IAWA Journal 15:335-360. [ Links ]
Received: 21.02.2011; accepted: 8.03.2012