High Anatomical and Physiological Leaf Plasticity of Ocotea Odorifera (Lauraceae) in Response to Different Levels of Radiation Availability
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Botany High anatomical and physiological leaf plasticity of Ocotea odorifera (Lauraceae) in response to different levels of radiation availability Journal: Botany Manuscript ID cjb-2019-0128.R1 Manuscript Type: Article Date Submitted by the 14-Jul-2020 Author: Complete List of Authors: Leme, Gabriele; Universidade Federal de Alfenas, ICN Ramos, Flavio; Universidade Federal de Alfenas, ICN Pereira, Fabricio; Universidade Federal de Alfenas, Instituto de Ciências da NaturezaDraft Polo, Marcelo; Universidade Federal de Alfenas, ICN Sun leaves, Shade leaves, Shade-tolerant species, Light environments, Keyword: Photosynthetic efficiency Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : © The Author(s) or their Institution(s) Page 1 of 34 Botany 1 High anatomical and physiological leaf plasticity of Ocotea odorifera (Lauraceae) 2 in response to different levels of radiation availability 3 4 Gabriele Marques Leme1, Flavio Nunes Ramos1, Fabricio José Pereira1, Marcelo Polo1* 5 6 1Laboratório de Ecologia de Fragmentos Florestais (ECOFRAG), Instituto de Ciências 7 da Natureza, Universidade Federal de Alfenas (UNIFAL-MG), Rua Gabriel Monteiro 8 da Silva, n. 700, Alfenas, MG. CEP 37130-001, Brazil. email list: 9 [email protected], [email protected], fabricio.pereira@unifal- 10 mg.edu.br, [email protected] 11 *Author for correspondence: [email protected],Draft phone: +55 35 3701-9681. © The Author(s) or their Institution(s) Botany Page 2 of 34 12 Abstract 13 Our goal was to investigate leaf morpho-physiological plasticity of Ocotea 14 odorifera trees growing under different environmental conditions in a fragmented 15 forest. Microclimatic data were collected in a pasture matrix, forest edge, and forest 16 interior in three Atlantic Forest fragments. Leaf gas exchange, as well as leaf anatomy 17 in paradermal and transversal sections, were evaluated in individuals in these 18 environments. Radiation intensity and temperature had higher means in the pasture 19 matrix compared to that in both the forest interior and edge. However, internal portions 20 of the canopy did not exhibit significant variation in radiation or temperature. External 21 canopy leaves exhibited higher net photosynthesis in plants from the pasture matrix, but 22 the shaded forest interior favoredDraft this parameter for internal leaves. Variation in net 23 photosynthesis and other gas exchange parameters were related to thinner shade leaves 24 in forest interior individuals and internal leaves with lower stomatal density. Although 25 the pasture matrix, forest edge, and forest interior experienced differences in light and 26 temperature, leaf position in the canopy produced microclimatic variations, which 27 modified gas exchange and anatomy. Thus, O. odorifera shows the potential for 28 reforestation programs because of its high leaf plasticity, which will enable it to 29 overcome light and temperature variation. 30 31 Keywords: Light environments · Pasture matrix · Photosynthesis · Shade leaves · 32 Shade-tolerant species · Sun leaves © The Author(s) or their Institution(s) Page 3 of 34 Botany 33 Introduction 34 Tree communities in pastures in tropical habitats are formed by regeneration or 35 the remaining tree species retained by landowners during forest clearing and subsequent 36 management (Manning et al. 2006; Siqueira et al. 2017). Landowners maintain tree 37 species in pastures for two reasons: (i) shading efficiency (Titto et al. 2011), and (ii) 38 timber quality (Siqueira et al. 2017). However, these trees may die because of 39 environmental changes caused by high irradiation and temperature in pastures as 40 compared to that in forests. 41 The intensity and quality of light, as well as other microclimatic parameters, 42 vary within environments (Wagner et al. 2008, Barros et al. 2012, Reyer et al. 2013) 43 and consequently, may modify theDraft physiology, anatomy, and morphology of leaves 44 (Hogewoning et al. 2010, Macedo et al. 2011). Likewise, plants growing under different 45 light conditions may adjust their photosynthetic apparatus through phenotypic plasticity 46 (Valladares and Niinemets 2008, Wagner et al. 2008), which enables photosynthetic 47 acclimation and higher growth rates (Athanasiou et al. 2010). Moreover, leaves may 48 also exhibit anatomical (Weston et al. 2000) and physiological differences (Murchie and 49 Horton 1997) in response to changes in light intensity. Well-understood differences in 50 anatomy and physiology of sun and shade leaves prevent or mitigate damage (Fan et al. 51 2013). 52 The ability to acclimate to different radiation intensities varies among species 53 (Gratani 2014). Early successional and light-demanding species likely have higher 54 photosynthetic plasticity and acclimation capacity than late-successional and shade- 55 tolerant species (Portes et al. 2010, Longuetaud et al. 2013). However, there is 56 increasing evidence that acclimation potential is not always related to the successional © The Author(s) or their Institution(s) Botany Page 4 of 34 57 status of the plant species (Wyka et al. 2007, Souza et al. 2008, Kuptz et al. 2010). 58 Krause et al. (2012), for example, found that a late-successional tree species could grow 59 under full exposure to sunlight. Thus, the ability to tolerate high-light environments, 60 such as that in pastures, is species-specific and may represent a selective advantage. 61 Most studies on acclimation processes of plants have been conducted using 62 species exposed to a series of radiation intensity levels (Athanasiou et al. 2010). Few 63 studies have focused on photosynthetic responses of forest species to light conditions in 64 the field (Ramos and Grace 1990, Abrams and Mostoller 1995, Carswell et al. 2000, 65 Domingues et al. 2007), although some studies have investigated the photosynthetic 66 responses of seedlings planted in open pastures and under remnant shrubs and trees 67 (Loik and Holl 1999, 2001). In thisDraft study, we investigated the relationships between leaf 68 anatomy and photosynthetic traits under different light conditions. More precisely, we 69 investigated the plasticity of Ocotea odorifera trees along a radiation gradient. 70 Ocotea odorifera is a vulnerable tree species from the Brazilian Atlantic 71 Forest, which is commonly recommended for shading cattle in pastures. This species 72 develops a canopy that can reach 46 m in diameter and provides substantial shade 73 (Lopes et al. 1996). However, Carvalho (2005) has indicated that O. odorifera requires 74 low to medium shading intensity as a sapling and is classified as a late secondary or 75 shade-tolerant climax species. Additionally, this species does not survive when planted 76 in full exposure to sunlight and there is no report regarding its regeneration in secondary 77 vegetation (Carvalho 2005). However, we determined that adult O. odorifera could 78 survive in pastures and exhibited substantial anatomical and physiological plasticity in 79 its leaves. Our results are important to management and conservation programs where 80 this species is relevant for restoration projects. © The Author(s) or their Institution(s) Page 5 of 34 Botany 81 We hypothesized that photosynthetic responses of O. odorifera were mediated 82 by its leaf anatomy and the microclimate. The results from this study indicated plant 83 tolerance to different radiation conditions and additionally provided insights regarding 84 the suitability of this species for use in restoration programs. 85 86 Materials and Methods 87 88 Tree species and study sites 89 Ocotea odorifera (Vell.) Rohwer (Lauraceae), commonly known as sassafras, is 90 a Brazilian native tree species of the Atlantic Rainforest that occurs in the southern and 91 southeastern regions of Brazil andDraft some parts of Bahia State (Carvalho 2005). The 92 species is prized for the quality of its wood but particularly for the essential oil 93 components that contain safrole (Mossi et al. 2013), which is exported to Japan, the 94 United States, and some European countries (Oltramari 2001). Owing to its 95 indiscriminate exploitation, O. odorifera was included in the Brazilian checklist of 96 vulnerable plant species (IBAMA 2008) and was designated as vulnerable according to 97 The World Conservation Union Red List of Threatened Species (Varty 1998). The 98 natural reproduction of O. odorifera presents difficulties because of the time it takes to 99 reach physiological maturity, which is approximately 25 to 40 years, with an average 100 production of 2,000 diaspores/year/plant (Duarte da Silva et al. 2001). Furthermore, 101 fruits are difficult to obtain because of their irregular and biannual development (Inoue 102 et al. 1984). We chose this species because of its ecological importance, its endangered 103 status, and primarily because it appears in three distinct habitats: along forest edges, in 104 forest interiors, and as isolated trees in the pasture matrix near forest fragments. © The Author(s) or their Institution(s) Botany Page 6 of 34 105 The individuals chosen in our study were no taller than 6.0 m. Data sampling 106 occurred at an average canopy height of 2.0 m from nine individuals, which exhibited 107 good phytosanitary condition. Ocotea odorifera individuals in pastures were remnants 108 from the deforestation process and were left to provide shade for cattle. We considered 109 external leaves as those at the third internode or outer ones, and internal leaves as those 110 at the fourth internode or inner ones. Only fully expanded leaves were collected. 111 The study took place in three forest fragments near Alfenas City (21°25•45S, 112 45°56 •50W, and an altitude of 880 m asl) in southern Minas Gerais, Brazil. This is an 113 Atlantic Forest area with semi-deciduous vegetation and a Cwb type climate, with warm 114 and rainy summers and cold and dry winters. 115 The forest fragments studied wereDraft surrounded by pasture. We investigated three 116 environments with naturally occurring individuals of O. odorifera: (1) the pasture 117 matrix, (2) the forest edge, and (3) the forest interior (at least 200 m from any edge;Fig.