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Isotopic Composition of Leaf Carbon (Δ13c) and Nitrogen (Δ15n) of Deciduous and Evergreen Understorey Trees in Two Tropical Brazilian Atlantic Forests

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Isotopic Composition of Leaf Carbon (Δ13c) and Nitrogen (Δ15n) of Deciduous and Evergreen Understorey Trees in Two Tropical Brazilian Atlantic Forests Journal of Tropical Ecology (2018) 34:145–156. © Cambridge University Press 2018 doi:10.1017/S0266467418000093 Isotopic composition of leaf carbon (δ13C) and nitrogen (δ15N) of deciduous and evergreen understorey trees in two tropical Brazilian Atlantic forests 1, 2 1 Angela Pierre Vitória ∗, Eleinis Ávila-Lovera ,TatianedeOliveiraVieira , Ana Paula Lima do Couto-Santos3,TiagoJoséPereira4,LigiaSilveiraFunch5,LeandroFreitas6, Lia d’Afonseca Pedreira de Miranda5,PabloJ.F.PenaRodrigues6,CarlosEduardoRezende1 and Louis S. Santiago2,7 1 Universidade Estadual do Norte Fluminense Darcy Ribeiro, Laboratório de Ciências Ambientais, Av. Alberto Lamego, 2000, UENF, CBB, Parque Califórnia, 28013–602, Campos dos Goytacazes, Rio de Janeiro, Brazil 2 Department of Botany and Plant Sciences, University of California, Riverside, CA 92521, USA 3 Departamento de Ciências Exatas e Naturais, Universidade Estadual do Sudoeste da Bahia, BR 415, Km 3, 45700-000, Itapetinga, Bahia, Brazil 4 Department of Nematology, University of California, Riverside, CA 92521, USA 5 Departamento de Ciências Biológicas, Universidade Estadual de Feira de Santana, BR 116, Km 3, 44031–460, Feira de Santana, Bahia, Brazil 6 Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rua Pacheco Leão, 915, 22460-030, Rio de Janeiro, Brazil 7 Smithsonian Tropical Research Institute, Apartado 0843–03092, Balboa, Republic of Panamá (Received 14 February 2017; revised 1 March 2018; accepted 2 March 2018) Abstract: Isotopic composition of leaf carbon (δ13C) and nitrogen (δ15N) is determined by biotic and abiotic factors. In order to determine the infuence of leaf habit and site on leaf δ13Candδ15N in the understorey of two Atlantic forests in Brazil that differ in annual precipitation (1200 and 1900 mm), we measured these isotopes in the shaded understorey of 38 tropical tree species (20 in the 1200-mm site and 18 in the 1900-mm site). Mean site values for δ15N were signifcantly lower at the 1200-mm site ( 1.4‰)comparedwiththe1900-mmsite( 3.0‰), and δ13Cwas − + signifcantly greater in the 1200-mm site ( 30.4‰) than in the 1900-mm site ( 31.6‰). Leaf C concentration was − − greater and leaf N concentration was lower at 1200-mm than at 1900-mm. Leaf δ15Nwasnegativelycorrelatedwith δ13Cacrossthetwosites.Leaf δ13Candδ15N of evergreen and deciduous species were not signifcantly different within a site. No signifcant phylogenetic signal for any traits among the study species was found. Overall, site differences were the main factor distinguishing traits among species, suggesting strong functional convergence to local climate and soils within each site for individuals in the shaded understorey. Key Words: leaf habit, leaf traits, N and C concentration, tropical rain forest, water use effciency INTRODUCTION Leaf δ13Ccanalsovarywithleafhabit,morphology, genetics and irradiance (Dawson et al. 2002,Francoet al. Tropical forests are extremely diverse environments (Mo- 2005,Rossattoet al. 2013,Sobrado&Ehleringer1997, rellato & Haddad 2000,Putzet al. 2001,terSteegeet al. Vitoria et al. 2016), which may refect differences in 2013)andtheidentifcationoffunctionalgroupsfacilit- photosynthetic water use effciency (WUE). ates understanding of more complex ecological processes In sites with high mean annual precipitation (MAP), (Powers & Tiffn 2010). Leaf δ13Ccanbeusedtoorganize lower δ13Cvaluesareobserved(Cornwellet al. 2018, plant functional groups because it refects conditions Leffer & Enquist 2002,Maet al. 2012). Cornwell et al. during photosynthesis, with increasing discrimination (2018) showed that woody evergreen species have lower 13 13 against CasintercellularCO2 availability increases leaf δ CthanwoodydeciduousspecieswhenMAPis (Farquhar et al. 1982), leading to lower values of δ13C. higher than 1000 mm, and an inverse pattern when MAP is lower than 1000 mm. In temperate zones, deciduous species and species with short leaf lifespans generally 13 ∗ Corresponding author. Email: [email protected] exhibit lower δ C and presumably lower WUE than /36768:DDAC, 534697 957 013667CC, A3D,,C475DDD:7.34697.7D7C8C7333473D :DDAC, 534697 957D7C :DDAC,6 9 2 146 ANGELA PIERRE VITÓRIA ET AL. evergreen species and species with long leaf lifespans 2008). The vegetation of the 1200-mm site is classifed (Ehleringer & Cooper 1988,Marshall&Zhang1994). as evergreen seasonal forest (Richards 1998)andthe However, the relationship between leaf δ13C and decidu- soil is yellowish-red latosol with sandy clay loam texture ousness has been somewhat controversial in the tropics, (Funch et al., 2008). The topography is undulating and with reports of lower discrimination against 13Cin the altitude ranges between 400 and 600 m asl, which deciduous compared with evergreen species in Venezuela confers a mesothermal climate to this site (Cwb)(Kottek (Sobrado & Ehleringer 1997), greater discrimination et al. 2006). Mean temperature oscillates around 18°Cin against 13Cindeciduouscomparedwithevergreenspe- April–September and exceeds 22°Cinthehottermonths cies in Brazil, and no difference in other studies (Franco of October–February (Funch et al. 2002). The 1200-mm et al. 2005,Leffer&Enquist2002,Powers&Tiffn2010). site has clouds for much of the year, and the rainy season Variation of δ15Ninplantsandsoilcanrefecttemporal occurs between December–April, with a peak between and spatial variation in N sources, soil N availability and March–April, whereas the dry season varies between 5– Nacquisitionfromalternativesourcessuchasbiological 6mooccurringbetweenMay–October. N2-fxation, mycorrhizal associations and atmospheric The 1900-mm site is located in south-eastern Brazil, in deposition (Bai et al. 2009,Bustamanteet al. 2004, the União Biological Reserve (22°27′S, 42°02′W). This Dawson et al. 2002,Omettoet al. 2006,Powers&Tiffn site has a gently undulating topography ranging from 2010). Values of δ15Ninsoilandplantssystematically sea level to 370 m asl. The vegetation of the 1900- decrease with the increasing of MAP due to variation mm site is classifed as lowland wet forest (Braga et al. in the openness of the N cycle until the point of soil 2016). The soil is dystrophic red-yellow podzolic with waterlogging (Amundson et al. 2003,Austin&Vitousek sandy clay texture (Lima et al. 2011). Climate is tropical 1998,Handleyet al. 1999,Nardotoet al. 2008,Santiago humid (Aw)(Kotteket al. 2006), with an average annual et al. 2004,Schuur&Matson2001). Differences in the temperature of 25°C, and about 85% of precipitation oc- frequency of leaf N re-translocation with leaf lifespan curring between October–April. Although precipitation have been suggested to also infuence δ15Nvaluesof does occur throughout the year, there are 3–4 mo of dry tropical trees, where shorter leaf lifespans re-translocate season. leaf N more frequently than evergreen species (Santiago Thirty-eight species of 18 families were sampled: 20 at et al. 2004)andδ15N becomes enriched during re- the 1200-mm site and 18 at the 1900-mm site. Species assimilation of nitrate and leaf N re-metabolism (Evans were chosen according to previous information about 2001). leaf habit. The classifcation scheme for leaf habit of We determined leaf δ13Candδ15N in evergreen and the 38 species is based on Frankie et al. (1974)and deciduous species in the understorey from two tropical included evergreen, evergreen with discontinuous pro- Atlantic forests in Brazil that differ in MAP: 1200 mm duction, deciduous and semi-deciduous species. For data and 1900 mm in order to determine the infuence of leaf presentation and analyses, evergreen species and species habit and site on leaf δ13Candδ15N. We hypothesized that evergreen with discontinuous production were grouped in understorey leaves: (1) deciduous species have traits under the category evergreen, whereas deciduous and associated with maximizing C gain with higher leaf N and semi-deciduous species were considered deciduous. For lower δ13C than evergreen species; (2) evergreen species each species, fve adult individuals 10–15 m tall with show lower δ15Nthandeciduousspecies;and(3)values diameter at breast height of 10–30 cm had leaves at for δ13Candδ15Naregreateratthedriersite. heights of 2.5–5.0 m sampled, except for the following species at the 1900-mm site: Ficus gomelleira (n 4), Cupania racemosa (n 4), Brosimum glazioui (n = 4), METHODS Virola gardneri (n 2),= Micropholis guianensis (n = 2), Ocotea diospyrifolia=(n 2). Photosynthetically active= Study sites and species leaves of the second or third= pair, under shade conditions 2 1 (< 40 µmol m− s− in both sites) were collected. We This study was carried out in two evergreen tropical opted to collect samples in the shade conditions due to Atlantic forests in Brazil (IBGE 2012): one in Bahia the differences in the cloud cover between forests, and state that receives 1200 mm of annual precipitation and consequently irradiance differences in the canopy leaves, 1 13 one in Rio de Janeiro state that receives 1900 mm y− since irradiance has an infuence on the δ C(Vitoriaet al. (Figure 1). The 1200-mm site is located within a semi- 2016). Our leaf isotopic composition data can therefore arid region of Brazil in Chapada Diamantina National be considered as conservative in terms of emphasizing Park (CDNP), north-eastern Brazil (12°28′S, 41°23′W). differences in climate between the two sites. Leaves were However, due to moist air masses, altitude, orography collected between 2011–2013 at the 1200-mm site and and climatic conditions, it shows foristic similarities to in 2015 at the 1900-mm site.
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