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Does ecophysiological behaviour explain habitat occupation of sympatric Clusia species in a Brazilian Atlantic rainforest?

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Plasticity of ecophysiological acclimation determines habitat occupation of species of Clusia in an Atlantic rainforest of Brazil. Ecophysiological performance is not sufficient for explaining widespread versus locally restricted distribution of species among physiognomic sub-sites within the forest.

Abstract

Four species of Clusia were studied that have distinct habitat distribution patterns within an Atlantic rainforest research reserve, in Espírito Santo state, southeast Brazil, throughout five sites: a riverine forest, a hill forest, two rock outcrops and an ecotone hill forest/rock outcrop. Clusia aemygdioi Gomes da Silva & B. Weinberg and Clusia intermedia G. Mariz were locally widespread among the sites while Clusia marizii Gomes da Silva & B. Weinberg and Clusia spiritu-sanctensis G. Mariz & B.Weinberg were locally restricted. Clusia spiritu-sanctensis was the only obligate crassulacean acid metabolism (CAM) species, showing low 13C-discrimination (δ 13C −16.5 to −19.2  ‰) and nocturnal acid accumulation. Data of 13C discrimination and photosynthetic performance show that C. marizii, C. intermedia and C. aemygdioi performed C3 photosynthesis. The latter may have some intrinsic capacity for CAM, which needs to be further studied. Because of local abundance Tibouchina heteromalla (D. Don) Cogn. (Melastomaceae) and Kielmeyera occhioniana Saddi (Clusiaceae) were included for comparison with the Clusia species and for typical obligate C3-photosynthesis behaviour. We asked whether the habitat occupation patterns of the studied species could be explained by ecophysiological performance especially with respect to photosynthesis. The hill forest with a denser tree cover was the most shaded site, and the plants there had shade-plant characteristics, while at all the other sites the plants showed sun-plant features. Clusia intermedia consistently had an inferior performance. Nevertheless, it is equally abundant as C. aemygdioi in one of the sun-exposed, and probably most stressful rock outcrop sites. The obligate C3-species T. heteromalla performed remarkably well. The CAM in C. spiritu-sanctensis did not appear to be directly related to habitat occupation although it conferred plasticity by flexible expression of CAM phases. Flexibility of acclimation determined habitat occupation of the plants performing C3 photosynthesis. Ecophysiological performance of the four Clusia species was only slightly related to widespread versus restricted occurrence patterns. Thus, ecophysiological performance alone is not sufficient for explaining the local distribution and abundance of these species, and aspects related to reproductive output deserve future examination.

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References

  • Adams MA, Grierson PF (2001) Stable isotopes at natural abundance in terrestrial plant ecology and ecophysiology: an update. Plant Biol 3:299–310

    Article  CAS  Google Scholar 

  • Araujo DSD (2000) Análise florística e fitogeográfica das restingas do Estado do Rio de Janeiro. D.Sc. Thesis. Rio de Janeiro: Ecologia, Universidade Federal do Rio de Janeiro

  • Araujo DSD, Scarano FR (2007) Biogeographic features of Clusia, with emphasis on South American and especially Brazilian species. In: Lüttge U (ed) Clusia–a woody neotropical genus of remarkable plasticity and diversity. Springer, Heidelberg, pp 31–54

    Google Scholar 

  • Bawa KS (1990) Plant pollinator interactions in tropical rainforests. Ann Rev Ecol Syst 21:399–422

    Article  Google Scholar 

  • Bilger W, Schreiber U, Bock M (1995) Determination of quantum efficiency of photosystem II and of non-photochemical quenching of chlorophyll fluorescence in the field. Oecologia 102:425–432

    Article  Google Scholar 

  • Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:489–504

    Article  PubMed  Google Scholar 

  • Broadmeadow MSJ, Griffiths H, Maxwell C, Borland A (1992) The carbon isotope ratio of plant organic material reflects temporal and spatial variations in CO2 within tropical forest formation in Trinidad. Oecologia 89:435–441

    Article  Google Scholar 

  • Chambers JC, MacMahon JA (1994) A day in the life of a seed: movements and fates of seeds and their implications for natural and managed systems. Ann Rev Ecol Syst 25:263–292

    Article  Google Scholar 

  • Crawford RMM (1989) Studies in plant survival. Blackwell, Oxford

    Google Scholar 

  • de Mattos EA, Grams TEE, Ball E, Franco AC, Haag-Kerwer A, Herzog B, Scarano FR, Lüttge U (1997) Diurnal patterns of chlorophyll a fluorescence and stomatal conductance in species of two types of coastal tree vegetation in southeastern Brazil. Trees 11:363–369

    Google Scholar 

  • Ehleringer JR (1993) Variation in leaf carbon isotope discrimination in Encelia farinosa: implications for growth, competition, and drought survival. Oecologia 95:340–346

    Article  Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989a) Carbon isotope discrimination and photosynthesis. Ann Rev Plant Physiol 40:503–537

    Article  CAS  Google Scholar 

  • Farquhar GD, Hubick KT, Coudon AG, Richards RA (1989b) Carbon isotope fractionation and plant water-use efficiency. In: Rundel PW, Ehleringer JR, Nagy KA (eds) Stable isotopes in ecological research. Springer, Heidelberg, pp 21–40

    Chapter  Google Scholar 

  • Franco AC, Haag-Kerwer A, Herzog B, Grams TEE, Ball E, de Mattos EA, Scarano FR, Barreto SMB, Garcia MA, Mantovani A, Lüttge U (1996) The effect of light levels on daily patterns of chlorophyll fluorescence and organic acid accumulation in the tropical CAM tree Clusia hilariana. Trees 10:359–365

    Google Scholar 

  • Franco AC, Herzog B, Hübner C, Mattos EA, Scarano FR, Ball E, Lüttge U (1999) Diurnal changes in chlorophyll a fluorescence, CO2-exchange and organic acid decarboxylation in the tropical CAM tree Clusia hilariana. Tree Physiol 19:635–644

    Article  PubMed  Google Scholar 

  • Gomes da Silva A, Weinberg B (1984) Clusia marizii, uma nova espécie de Guttiferae do Espírito Santo, Brasil. Bradea 4(4):161–164

    Google Scholar 

  • Gomes da Silva A, Weinberg B (1985) Clusia aemygdioi, uma nova espécie de Guttiferae do Espírito Santo, Brasil. Bradea 4(24):161–164

    Google Scholar 

  • Guehl J-M, Bonal D, Ferhi A, Barigah TS, Farquhar G, Granier A (2004) Community-level diversity of carbon-water relations in rainforest trees. In: Gourlet-Fleury S, Guehl J-M, Laroussinie O (eds) Ecology and management of a neotropical rainforest. Elsevier, Amsterdam, pp 75–94

  • Herzog B, Hübner C, Ball E, Bastos RN, Franco AC, Scarano FR, Lüttge U (1999) Comparative study of the C3/CAM intermediate species Clusia parviflora Saldanha et Engl. and the obligate CAM species Clusia hilariana Schlecht. growing sympatrically exposed and shaded in the Atlantic restinga of Brazil. Plant Biol 1:453–459

    Article  Google Scholar 

  • Högberg P (1997) 15N natural abundance in soil-plant systems. New Phytol 137:179–203

    Article  Google Scholar 

  • Joly CA, Metzger JP, Tabarelli M (2014) Experiences from the Brazilian Atlantic forest: ecological findings and conservation initiatives. New Phytol 204:459–473

    Article  PubMed  Google Scholar 

  • Liebig M, Scarano FR, de Mattos EA, Zaluar HLT, Lüttge U (2001) Sex differentiation in the dioecious neotropical CAM tree Clusia hilariana Schltdl.: ecophysiological and floristic implications. Trees 15:278–288

    Article  Google Scholar 

  • Lüttge U (1986) Nocturnal water storage in plants having crassulacean acid metabolism. Planta 168:287–289

    PubMed  Google Scholar 

  • Lüttge U (2007a) Photosynthesis. In: Lüttge U (ed) Clusia–a woody neotropical genus of remarkable plasticity and diversity. Springer, Heidelberg, pp 135–186

  • Lüttge U (2007b) Physiological ecology. In: Lüttge U (ed) Clusia–a woody neotropical genus of remarkable plasticity and diversity. Springer, Heidelberg, pp 187–234

  • Lüttge U (2008) Physiological ecology of tropical plants, 2nd edn. Springer, Heidelberg

    Google Scholar 

  • Lüttge U, Duarte HM (2007) Morphology, anatomy, life forms and hydraulic architecture. In: Lüttge U (ed) Clusia–a woody neotropical genus of remarkable plasticity and diversity. Springer, Heidelberg, pp 17–30

  • Lüttge U, Scarano FR (2007) Synecological comparisons sustained by ecophysiological fingerprinting of intrinsic photosynthetic capacity of plants as assessed by measurements of light response curves. Bras J Bot 30:355–364

    Google Scholar 

  • Lüttge U, Duarte HM, Scarano FR, de Mattos EA, Cavalin PO, Franco AC, Fernandes GW (2007) Physiological ecology of photosynthesis of five sympatric species of Velloziaceae in the rupestrian fields of Serra do Cipó, Minas Gerais, Brazil. Flora 202:637–646

    Article  Google Scholar 

  • Mantovani A (1999) A method to improve leaf succulence quantification. Braz Arch Biol Technol 42:9–14

    Google Scholar 

  • Mariz G (1974) Clusiaceae Clusia intermedia G. Mariz. In: Guttiferae of pernambuco (Brazil). Candollea 29:9

  • Mariz G, Weinberg B (1982) Clusia spiritu-sanctensis, uma espécie nova de Guttiferae. Bradea 3(29):233–238

    Google Scholar 

  • Martinelli LK, Piccolo MC, Townsend AR, Vitousek PM, Cuevas E, McDowell W, Robertson GP, Santos OC, Treseder K (1999) Nitrogen stable isotope composition of leaves and soil: tropical versus temperate forests. Biogeochemistry 46:45–65

    CAS  Google Scholar 

  • Martins RL, Wendt T, Margis R, Scarano FR (2007) Reproductive biology. In: Lüttge U (ed) Clusia–a woody neotropical genus of remarkable plasticity and diversity. Springer, Heidelberg, pp 73–94

    Google Scholar 

  • Mendes SL, Padovan MP (2000) A Estação Biológica de Santa Lúcia, Santa Teresa, Espírito Santo. Boletim do Museu de Biologia Mello Leitão (Nova Série) 11(12):7–34

    Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  PubMed  Google Scholar 

  • Osmond CB (1978) Crassulacean acid metabolism: a curiosity in context. Ann Rev Plant Phys 29:379–414

    Article  CAS  Google Scholar 

  • Pereira OJ, Araujo DSD (2000) Análise florística das restingas dos estados do Espírito Santo e Rio de Janeiro. In: Esteves FA, Lacerda LD (eds) Ecologia de Restingas e Lagoas Costeiras. NUPEM/UFRJ, Macaé, pp 25–63

    Google Scholar 

  • Rascher U, Liebig M, Lüttge U (2000) Evaluation of instant light-response curves of chlorophyll fluorescence parameters obtained with a portable chlorophyll fluorometer on site in the field. Plant Cell Environ 23:1397–1405

    Article  CAS  Google Scholar 

  • Reinert F, Roberts A, Wilson MJ, de Ribas L, Cardinot G, Griffiths H (1997) Gradation in nutrient composition and photosynthetic pathways across the restinga vegetation of Brazil. Bot Acta 110:135–142

    Article  CAS  Google Scholar 

  • Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153

    Article  Google Scholar 

  • Ribeiro MC, Martensen AC, Metzger JP, Tabarelli M, Scarano FR, Fortin MJ (2011) The Brazilian Atlantic forest: a shrinking biodiversity hotspot. In: Zachos FE, Habel JC (eds) Biodiversity hotspots. Springer, Heidelberg

    Google Scholar 

  • Rizzini CT (1979) Tratado de Fitogeografia do Brasil, vol 2. Edusp, São Paulo

    Google Scholar 

  • Roberts A, Griffiths H, Borland A, Reinert F (1996) Is crassulacean acid metabolism activity in sympatric species of hemiepiphytic stranglers such as Clusia related to carbon cycling as a photoprotective process? Oecologia 106:28–38

    Article  CAS  Google Scholar 

  • Saddi N (1984) Novas espécies de Kielmeyera Martius (Guttiferae) do sudeste brasileiro. Rodriguésia 36:59–64

    Google Scholar 

  • Saiter FZ, Guilherme FAG, Thomaz LD, Wendt T (2011) Tree changes in a mature rainforest with high diversity and endemism on the Brazilian coast. Biodivers Conserv 20:1921–1949

    Article  Google Scholar 

  • Scarano FR (2002) Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic rainforest. Ann Bot 90:517–524

    Article  PubMed Central  PubMed  Google Scholar 

  • Scarano FR (2009) Plant communities at the periphery of the Atlantic rainforest: rare-species bias and its risks for conservation. Biol Conserv 142:1201–1208

    Article  Google Scholar 

  • Scarano FR, Duarte HM, Ribeiro KT, Rodrigues PJFP, Barcellos EMB, Franco AC, Brulfert J, Deléens E, Lüttge U (2001) Four sites with contrasting environmental stress in southeastern Brazil: relations of species, life form diversity, and geographical distribution to ecophysiological parameters. Bot J Linn Soc 136:345–364

    Article  Google Scholar 

  • Scarano FR, Duarte HM, Franco AC, Geßler A, de Mattos EA, Nahm M, Rennenberg H, Zaluar HLT, Lüttge U (2005a) Ecophysiology of selected tree species in different plant communities at the periphery of the Atlantic Forest of SE–Brazil. I. Behaviour of three different species of Clusia in an array of plant communities. Trees 19:497–509

    Article  CAS  Google Scholar 

  • Scarano FR, Duarte HM, Franco AC, Geßler A, de Mattos EA, Rennenberg H, Lüttge U (2005b) Physiological synecology of tree species in relation to geographic distribution and ecophysiological parameters at the Atlantic forest periphery in Brazil: an overview. Trees 19:493–496

    Article  Google Scholar 

  • Schreiber U, Bilger W (1993) Progress in chlorophyll fluorescence research: major developments during the last years in retrospect. Progr Botany 54:151–173

    CAS  Google Scholar 

  • Thiele A, Krause GH, Winter K (1998) In situ study of photoinhibition of photosynthesis and xanthophyll cycle activity in plants growing in natural gaps of the tropical forest. Aust J Plant Physiol 25:189–195

    Article  Google Scholar 

  • Thomaz LD, Monteiro R (1997) Composição florística da mata atlântica de encosta da Estação Biológica de Santa Lúcia, município de Santa Teresa-ES. Boletim do Museu de Biologia Mello Leitão (Nova Série) 7:3–86

    Google Scholar 

  • Vaasen A, Scarano FR, Hampp R (2007) Population biology of different Clusia species in the state of Rio de Janeiro. In: Lüttge U (ed) Clusia–a woody neotropical genus of remarkable plasticity and diversity. Springer, Heidelberg, pp 117–127

    Google Scholar 

  • Valladares F, Sanchez-Gomez D, Zavala MA (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J Ecol 94:1103–1116

    Article  Google Scholar 

  • Winter K, Holtum JAM (2002) How closely do the δ 13C values of crassulacean acid metabolism plants reflect the proportion of CO2 fixed during day and night? Plant Physiol 129:1843–1851

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Winter K, Wallace BJ, Stocker GC, Roksandic Z (1983) Crassulacean acid metabolism in Australian vascular epiphytes and some related species. Oecologia 57:129–141

    Article  Google Scholar 

  • Winter K, Holtum JAM, Smith JA (2015) Crassulacean acid metabolism: a continuous or discrete trait? New Phytol. doi:10.1111/nph.13446

    Google Scholar 

  • Witkowski ETF, Lamont BB (1991) Leaf specific mass confounds leaf density and thickness. Oecologia 88:486–493

    Article  Google Scholar 

  • Zaluar HLT, Scarano FR (2000) Facilitação em restingas de moitas: um século de buscas por espécies focais. In: Esteves FA, Lacerda LD (eds) Ecologia de Restingas e Lagoas Costeiras. NUPEM-UFRJ, Rio de Janeiro, pp 3–23

    Google Scholar 

  • Zar JH (2010) Biostatistical analysis, 5th edn. Prentice Hall, Upper Saddle River

    Google Scholar 

  • Ziegler H (1994) Stable isotopes in plant physiology and ecology. Progress Botany 56:1–24

    Google Scholar 

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Acknowledgments

We thank the editor and three reviewers for helpful suggestions. We are grateful to V. G. Demuner (Museu Mello Leitão, Santa Teresa), C. Ducatti (Instituto de Biociências, Universidade do Estado de São Paulo) and J.A. Marchese (Laboratório de Bioquímica e Fisiologia Vegetal, Faculdade de Agronomia, Pato Branco) for various highly appreciated contributions to this study and J. F. Baumgratz and F. Z. Saiter for additional taxonomic support. We also thank Zilma Lóss and staff at Pousada Paradiso for hospitality and friendship; Prof. Hélio Q. B. Fernandes and staff at Museu de Biologia Mello Leitão, and Mr. and Mrs. Molino at Reserva Biológica Santa Lúcia for logistic support; Escola Superior São Francisco de Assis (ESFA) and Prof. Selma A. Hebling for laboratory facilities; Thiago Senna for laboratory assistance at ESFA; CNPq (Brazilian Research Council) for productivity grants to FRS, EAM, TW and ACF, and for research funds to TW through the Programa Mata Atlântica no.690149/01-8; CAPES (Brazilian Education Council) for research grants to ATCD (Bolista CAPES/BRASIL); and Volkswagen Stiftung, Germany, for funding.

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Communicated by R. Guy.

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Lüttge, U., Scarano, F.R., de Mattos, E.A. et al. Does ecophysiological behaviour explain habitat occupation of sympatric Clusia species in a Brazilian Atlantic rainforest?. Trees 29, 1973–1988 (2015). https://doi.org/10.1007/s00468-015-1277-1

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