Does selective logging affect the leaf structure of a late successional species?

Como o corte seletivo de madeira pode afetar a estrutura foliar de uma secundária tardia?

ORIGINAL PAPERS

Does selective logging affect the leaf structure of a late successional species?

Como o corte seletivo de madeira pode afetar a estrutura foliar de uma secundária tardia?

Guilherme Rodrigues Rabelo^I; Denise Espellet Klein^I,II; Maura Da Cunha^I,1

^IUniversidade Estadual do Norte Fluminense, Centro de Biociências e Biotecnologia, Lab. Biologia Celular e Tecidual, Av. Alberto Lamego 2000, 28013-602, Campos dos Goytacazes, RJ, Brazil. [e-mail]

^IIUniversidade Federal do Estado do Rio de Janeiro, Instituto de Biociências, Depto. Botânica, Av. Pasteur 458, 22290-240, Rio de Janeiro, RJ, Brazil. [e-mail]

ABSTRACT

The anatomical characteristics of both sun and shade leaves of Alseis pickelii were investigated in order to evaluate the consequences of selective logging (in seasonally dry Atlantic Forest) on the leaf structure of this species. Fully expanded sun and shade leaves were collected in two distinct stands of tabuleiro forest; a stand of recently logged forest and an unlogged stand. Only leaves from the unlogged stand revealed significantly different magnitudes of response to light regimes, producing leaves with structural characteristics associated with different levels of irradiance. The sun leaves from this stand had a thicker adaxial surface, mesophyll, palisade and spongy parenchyma, a secondary cell wall of fibers and a lower leaf area compared with the shade leaves. However, in the logged stand, the leaf cuticles of sun and shade leaves showed no significant differences, although the leaf area of the sun leaves was higher than the shade leaves. According to these data, we concluded that the unlogged stand produced typical "sun" and "shade" leaves. In contrast, leaves from the logged stand showed a lower variation of types, where neither typical "sun" nor typical "shade" leaves were produced, suggesting lower leaf plasticity of this late successional tree in this area.

Key-words: selective logging, leaf plasticity, sun and shade leaves, leaf structure, tabuleiro forest.

RESUMO

As características anatômicas de folhas de sol e sombra de Alseis pickelii foram investigadas a fim de se avaliar as consequências do corte seletivo de madeira sobre a estrutura foliar em uma floresta atlântica estacional semidecidual. Folhas expandidas de sol e de sombra foram coletadas em dois distintos setores da mata, setor explorado (área com recente atividade de corte seletivo), e setor preservado. Somente folhas do setor preservado revelaram significantes diferenças de resposta aos regimes de luz, produzindo folhas com características estruturais nitidamente associadas com diferentes níveis de irradiação. Folhas de sol deste setor apresentaram maiores espessuras da superfície adaxial, mesofilo, parênquima paliçádico e lacunoso, parede secundária das fibras e menor área foliar comparada às folhas de sombra. Entretanto, no setor explorado, as cutículas das folhas de sol e sombra não apresentaram diferenças significativas e as áreas foliares das folhas de sol foram maiores que a das folhas de sombra. De acordo com estes resultados, conclui-se que o setor preservado produziu árvores com típicas folhas de "sol" e "sombra". Em contraste, no setor explorado as árvores apresentaram menor variação nos tipos de folhas, onde nem típicas folhas de "sol" ou de "sombra" foram produzidas, sugerindo menor plasticidade desta espécie secundária tardia nesta área.

Palavras-chave: corte seletivo, plasticidade foliar, folhas de sol-sombra, estrutura foliar, floresta de tabuleiros.

Introduction

Selective logging is considered one of the main causes of treefall gaps in Brazilian forests (Rondon Neto et al. 2000). This type of disturbance causes widespread damage to surrounding trees, subcanopy vegetation, and soils; and also impacts the hydrological processes, erosion, fire, carbon storage, and animal species (Nepstad et al. 1995; Veríssimo et al. 1992; Curran et al. 2004). Unlike deforestation, which can be observed from satellites, selective logging causes a spatially diffuse thinning of large trees, which is hard to monitor using satellite images (Asner et al. 2005). The most obvious impact of selective logging is the increase in canopy openness, which exposes organisms to changes in light, humidity, and temperature (Almeida 1989).

This process requires acclimation of shade plants, from the understory, to sunlight, and demonstrates the close association between the anatomical adaptation of leaves and the efficiency of photosynthesis when plants grow under different levels of light (Carpenter & Smith 1981; Ashton & Berlyn 1992). Although leaf anatomy should not be used solely as a basis for the prediction of a species' ability to acclimate, the variation found in the anatomy of leaves provides an indication of the ecological plasticity of a species (Strauss-Debenedetti & Berlyn 1994).

The ecological effects of variations in light, humidity, and temperature on leaf anatomy have been studied; however, most of these studies were carried out in greenhouses (e.g., Chabot et al. 1979; Tognetti et al. 1998; Lee et al. 2000; Paiva et al. 2003) compared to native tropical populations (Chazdon & Kaufmann 1993; Rôças et al. 1997, 2001; Hlwatika & Bhat 2002). The effects of microclimatic alterations caused by selective logging on the plasticity of leaf anatomy have not been studied. The present study proposes an analysis that can be used to determine the acclimation capacity of Alseis pickelii Pilger et Shmale.

Alseis pickelii (Rubiaceae, Cinchonoideae) is a late successional tree, 10 to 13 meters tall, which occurs in the understory of tropical deciduous forests, such as xeric shrublands and deciduous seasonal forests (Pereira Moura 2001). This type of forest has diminished over time due to deforestation for charcoal production, farming (e.g., pasture, sugar cane, and pineapple), and logging (Villela et al. 2006). The profile diagrams of unlogged and logged stands have shown differences in canopy structure, mainly in height and in crown connectivity (Villela et al. 2006).

Most plant species have the ability to develop distinct leaves when growing at different light levels (Chazdon & Kaufmann 1993; Lee et al. 2000), and a wide amount of leaf variation has been described in several species from the Brazilian Atlantic Forest that were subjected to extreme conditions of sun and shade (Scarano et al. 1999, 2002; Rôças et al. 2001; Mantuano et al. 2006; Pereira et al. 2009). The present investigation was carried out in order to identify the effects of light on the leaf structure of A. pickelii, by comparing sun and shade leaves from two stands (unlogged and logged) where this species is exposed to different light, humidity and temperature regimes. The study areas are in the most important remnant of tabuleiro forest (a type of lowland Atlantic forest) in the state of Rio de Janeiro, Brazil. Our hypothesis is that selective logging affects the leaf structure and consequently the leaf acclimation capacity of this species.

Material and Methods

Study area

The study areas are located in the Guaxindiba Ecological Reserve in the São Francisco do Itabapoana district (21º24'S, 41º04'W) of northern Rio de Janeiro, Brazil. This is the largest fragment of a lowland forest on Tertiary formations (ca. 1200 ha according Villela et al. 2006), known as tabuleiro forest (RadamBrasil 1983). The elevation of this region ranges from 20 m to 200 m, which distinguishes this lowland forest from other regions within the Atlantic Forest along the Brazilian coast. Tabuleiro forest is classified as seasonal, semideciduous, lowland forest due to its phytogeographic features (Veloso et al. 1991). The climate can be classified as Aw, according to Köppen (1948), and is seasonal, with an intense dry season from May to August (RadamBrasil 1983). Mean annual rainfall is ca. 1000 mm; the wettest month is December and the driest is August (Villela et al. 2006). The mean annual temperature is 23ºC (RadamBrasil 1983). The soils are ultisols (USDA classification), with a low capacity of water retention and low levels of nutrients (Villela et al. 2006).

Leaf samples of Alseis pickelii were collected in two distinct stands at the Guaxindiba Ecological Station, during February to April of 2006". One stand, here referred to as the "logged stand" (LS), was part of an area of recently logged forest (less than five years ago). In the second stand, here referred to as the "unlogged stand" (US), selective logging has not occurred for the last 45 years and is, at this time, without traces of selective logging or forest fires (Souza 2005). The noticeable differences between the two stands are canopy structure and crown connectivity. Climatic observations and canopy cover (Tab. 1) measurements were made over the summer and winter at each site, at the four cardinal points for each of five chosen individuals at both US and LS. All climate observations were made at breast height and measurements were carried out between 11:30h and 13:30h; additionally, open fields were measured to provide a better comparison among the forest stands. Photosynthetic active radiation (PAR) was measured with a LI-190SA quantum sensor adapted to a LI-250A Light Meter (Li-Cor Inc.). Air temperature (ºC) and air humidity (%) were measured with HT-300 thermo-hygrometer (Instrutherm), and canopy cover (%) was measured using a 1 × 1 meter quadrat (Freitas et al. 2002).

Sampling, measurements and statistical analyses

For the anatomical analysis, seven fully expanded leaves growing in the sun and seven in the shade were collected from five adults randomly chosen in each of the two stands. The leaves were classified according to the amount of canopy light they were exposed to.

Fragments of the middle third of the leaf blade were fixed for two hours in solutions of 2.5% glutaraldehyde and 4.0% formaldehyde in a 0.05 M sodium cacodylate buffer, to pH 7.2, at room temperature. After being rinsed with the same buffer, the samples were post-fixed with 1.0% osmium tetroxide in a 0.05 M sodium cacodylate buffer (pH 7.2) for one hour. Subsequently, the samples were dehydrated in a graded series of acetone solutions. The material was infiltrated and embedded in epoxy resin. Transverse sections of approximately 0.70 µm were obtained and stained with toluidine blue (0.1% aqueous solution) (Johansen 1940). The slides were mounted in appropriate resin. Anatomical descriptions and measurements of the epidermis, mesophyll, and vascular bundles were made with image analysis software (analySIS^®) using an Axioplan Zeiss microscope. For scanning electron microscopy, the samples were fixed, post-fixed, dehydrated the same way as used for light microscopy, rinsed in the same buffer, and dehydrated in an ascendant acetone series. Afterwards, the samples were CO₂ critical-point-dried (CPD 030 – Baltec). Dried samples were adhered to stubs with carbon adhesive tape (3M) and sputter coated with 20 nm gold (SCD 050 – Baltec). The material was observed using a ZEISS DSM962 operating at 25 kV. Stomatal density was estimated from fragments of the leaf blades that were cleared by dipping the samples in 80% lactic acid and then autoclaved at 1 atm and 120 ºC, for 25 minutes, to separate the epidermis (O'Brien & McCully 1981). Counting and measurements were obtained using a sample size of 25 fields that were 0.24 mm². To test for phenolic compounds, a ferric chloride histochemical test was carried out for free-hand sections of newly collected material (Johansen 1940). Differences among leaf types and stands were tested by one-way analysis of variance (ANOVA), followed by Tukey's multiple comparison test (Zar 1996), and differences in microclimatic observations and canopy cover measurements were analyzed using the T-test (Zar 1996). The statistical analyses were performed using the statistical software package STATISTICA (StatSoft, USA).

Results

Despite phenotypic variations, Alseis pickelii shared some anatomical features irrespective of site and microhabitat (Fig 1). These features included: an adaxial and abaxial surface with a single cell layer, sinuous anticlinal cell walls only in the adaxial epidermis, paracytic stomata only on abaxial surfaces, dorsiventral mesophyll, a collateral arrangement in the vascular system, parenchymatic and fibrous bundle sheath cells, bundle sheath extension prolonged to the adaxial epidermis, and presence of phenols in the cells of spongy parenchyma.

Figure 1 and Table 2 compare the leaf anatomical structure of individuals from the logged and unlogged stands. When comparing sun and shade leaves from the unlogged stand, the adaxial surface was thicker in the former. No significant difference was found in the adaxial surface of sun and shade leaves from the logged stand (Fig. 1a–d). The abaxial surface showed no significant difference between sun and shade leaves from both stands (Tab. 2). The hypostomatic leaves of A. pickelii showed significantly different density of stomata in the sun and shade leaves of both stands, and higher occurrence in the sun leaves of both stands (Tab. 2). The thickness of the adaxial cuticle in sun and shade leaves of the logged stand was greater than the width in leaves of the unlogged stand; however, no significant difference was found in the sun and shade leaves from the logged stand (Tab. 2).

The dorsiventral mesophyll in the sun leaves of the unlogged stand had 2–4 cell layers of palisade parenchyma and 3–5 layers of spongy parenchyma. In contrast, shade leaves from the unlogged stand and both leaf types from the logged stand had significantly fewer cells and thinner tissues (Fig. 1 a-d; Tab. 2); 2–3 cell layers of palisade parenchyma and 3–4 layers of spongy parenchyma. Phenolic compounds were found in the spongy parenchyma mainly in the sun leaves from the unlogged stand and both leaves from the logged stand (Fig. 1 e–h).

The vascular system of A. pickelii presented a collateral arrangement, with parenchymatic and fibrous bundle sheath cells (Fig. 1 i) and a bundle sheath extension (Fig. 1 j). The secondary cell wall thickness of the perivascular fibers was wider in the sun leaves compared to the shade leaves from the unlogged stand, and no significant difference was found in the logged stand (Tab. 2). The leaf area was significantly different between sun and shade leaves from both stands. Sun leaves from the unlogged stand had lower area compared to shade leaves. However, this did not occur in leaves from the logged stand, where sun leaves had higher leaf area compared to shade leaves (Tab. 2).

Discussion

In spite of the microclimatic differences between the unlogged and logged stands, Alseis pickelii did not produce leaves with structural characteristics associated with different levels of irradiance in the same way in both stands. Only leaves from the unlogged stand revealed different magnitudes of response to light regimes, producing typical "sun" and "shade" leaves. In contrast, leaves from the logged stand showed lower phenotypic plasticity, which means that it was not possible to structurally distinguish sun leaves from shade leaves in this stand.

The occurrence of a thicker adaxial surface in the sun leaves of the unlogged stand appears to have had a greater role in protecting the leaves from excess irradiance (Strauss-Debenedetti & Berlyn 1994). Stomata density has already been cited for other species as being directly related to the amount of exposure to both light and water (Bastos et al. 1993; Rôças et al. 1997, 2001), and a greater number of stomata were found in the sun leaves of A. pickelii from both stands, allowing for efficient gas exchange (Lleras 1977), better control of transpiration, and possibly the avoidance of excessive water loss (Weyers & Meidner 1990). There was no significant difference in the width of the cuticles of the sun and shade leaves from the logged stand but the values were higher than for the leaves from the unlogged stand. This was probably a response to higher exposure to light (Cutler et al. 1982) and suggests a homogeneous environment in the logged stand.

The typical sun and shade leaves observed in the unlogged stand showed a classic pattern of response and adaptation to light exposure in the leaf tissues (Björkman 1981). The thicker palisade and spongy parenchyma from the sun leaves in this stand represents leaf tissue that maximizes light absorption and carbon fixation. Tubular palisade cells facilitate the penetration of direct sunlight, and thicker spongy parenchyma helps scatter the light, thus increasing the chance that light will be absorbed for photosynthesis (Vogelmann & Martin 1993; Vogelmann et al. 1996). The thicker mesophyll in sun leaves also facilitates CO₂ dissolution into the water within the cell wall, which decreases the resistance to CO₂ diffusion from the intercellular space to the chloroplast stroma (Evans 1999; Terashima et al. 2001). Furthermore, sun leaves from the unlogged stand also had a higher amount of lignified tissues, which possibly enhance durability and promote greater mechanical resistance, for example, against herbivory (Lee et al. 2000). An increase in defense mechanisms is supported by the phenolic compounds (Feeny 1976; Mantuano et al. 2006) that were frequently observed in the sun leaves from both stands, and the shade leaves from the logged stand.

The reduction of leaf area of the sun leaves from the unlogged stand is similar to that observed in many other species growing at different levels of light (Abrams & Kubiske 1990; Niinemets & Kull 1998; Klich 2000; Mendes et al. 2001). This adaptation could generate an increase in convective heat dissipation that could counteract the negative effects of overheating and high transpiration rates (Gates 1980).

The incapacity of A. pickelii to produce typical shade leaves in the logged stand is clearly related to high amounts of light caused by a greater amount of open space in the canopy. However, if sun leaves from both stands were collected at the same light exposure at the canopy level, why didn't the sun leaves from the logged stand produced typical sun leaves? It seems that this species needs stimulus from both low and high regimes of light to be able to develop different types of leaves. Although acclimation cannot be predicted from leaf anatomy alone (Strauss-Debenedetti & Berlyn 1994) the variation in the spectrum of leaf types found within the logged stand suggests lower leaf plasticity of this late successional tree and, consequently, that selective logging represents a clear threat to the conservation of this species. Further studies are necessary to better understand the acclimation and fitness mechanisms in this species.

Acknowledgements

The authors are indebted to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), the Fundação de Amparo a Pesquisa do Rio de Janeiro (FAPERJ), and Coordenação de Aperfeiçoando de Pessoal de Nível Superior (CAPES) for their financial support. We thank Dr. J.S. Souza for suggesting the study area, the technicians B.F. Ribeiro and G.A. de Moraes of LBCT/CBB/UENF for helping with laboratory tasks, and the biologists D.O. dos Santos and G.M. Gonçalves for their help with collecting plants. This study was part of the Master's thesis of the first author, presented to the Programa de Pós-Graduação em Biociências e Biotecnologia.

Artigo recebido em 24/08/2010

Aceito para publicação em 16/03/2011

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Publication Dates

• Publication in this collection
  31 Jan 2013
• Date of issue
  June 2012