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Functional Diversity of Photosynthesis, Plant-Species Diversity, and Habitat Diversity

  • Ulrich LüttgeEmail author
Chapter
Part of the Progress in Botany book series

Abstract

Photosynthesis is the basis of productivity. With that it is prerequisite of growth, which is the driver of competition between plants and therefore of fitness for occupying space. Modes of photosynthesis are C3 , C4, and C2 photosynthesis and crassulacean acid metabolism (CAM), each with plasticity of modifications conveying flexibility and considerable functional diversity. At the level of macrohabitats, i.e., ecosystems and biomes, vegetation with dominant C3 and C4 photosynthesis, respectively, or prominent contribution of CAM, can be distinguished. At finer scaling levels, this becomes more difficult. At the community level, C4 and CAM vegetation as well as C3 vegetation, where CAM and C4 species are conspicuously immersed, can be observed. At the microhabitat level species with different modes of photosynthesis often are found to occur sympatrically side by side even with very similar life-forms and appear to be equally successful in adapting or acclimatizing to environmental conditions. They get involved in interactions of competition and facilitation. Diversity of modes of photosynthesis and their plasticity create various options, but at the level of microhabitats, ecophysiological performance with respect to photosynthesis often does not explain distinct distributions of plant species. Plasticity and diversity imply complexity. “Diversity creates diversity.” Understanding biodiversity means understanding complexity. The diversity of arrivals of plants carrying a diversity of functional traits of photosynthesis at sites governed by chance and their establishment at dynamically variable conditions appears best leading us to an understanding of why so often we find that ecophysiological performance per se is insufficient for explaining local distribution of plants and habitat occupation.

Notes

Acknowledgments

My warmest thanks I express to Erwin Beck, Manfred Kluge, Hans Pretzsch, and Fabio Rubio Scarano for critically reading the manuscript and valuable suggestions.

References

  1. Acevedo E, Badilla I, Nobel PS (1983) Water relations, diurnal acidity changes, and productivity of a cultivated cactus, Opuntia ficus-indica. Plant Physiol 72:775–780Google Scholar
  2. Ackerly DD, Dudley SA, Sultan SE, Schmitt J, Coleman JS, Linder CR, Sandquist DR, Geber MA, Evans AS, Dawson TE, Lechowicz MJ (2000) The evolution of plant ecophysiological traits: recent advances and future directions. BioSience 50:979–995Google Scholar
  3. Araujo DSD (2000) Análise florística e fitogeográfica das restingas do Estado do Rio de Janeiro. D.Sc. Thesis. Ecologia, Universidade Federal do Rio de Janeiro, Rio de JaneiroGoogle Scholar
  4. Balvanera P, Pfisterer AB, Buchmann N, He J-S, Nakashizuka T, Raffaelli D, Schmid B (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156Google Scholar
  5. Beck E (2008) Investing gradients. In: Beck E, Bendix J, Kottke I, Makeschin F, Mosandl R (eds) Gradients in a tropical mountain ecosystem of Ecuador, Ecological studies, vol 198. Springer, Berlin, pp 55–61Google Scholar
  6. Beck E (2019) Ecology: ecosystems and biodiversity. In: Wegner LH, Lüttge U (eds) Emergence and modularity in life science. Springer, Heidelberg, pp 195–213Google Scholar
  7. Beck E, Bendix J, Silva B, Rollenbeck R, Lehnert L, Hamer U, Potthast K, Tischer A, Roos K (2013) Future provisioning services: repasturation of abandoned pastures, problems, and pasture management. In: Bendix J, Beck E, Bräuning A, Makeschin F, Mosandl R, Scheu S, Wilcke W (eds) Ecosystem services, biodiversity and environmental change in a tropical mountain ecosystem of south Ecuador. Ecol Stud, vol 221, Springer, Berlin, pp 355–370Google Scholar
  8. Bellasio C (2017) A generalized stoichiometric model of C3, C2, C2+C4, and C4 photosynthetic metabolism. J Exp Bot 68:269–282Google Scholar
  9. Berner RA (1994) Geocarb II: a revised model of atmospheric CO2 over phanerozoic time. Am J Sci 294:56–91Google Scholar
  10. Bertness MD, Callaway RM (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193Google Scholar
  11. Brandão Correia CM, Dias ATC, Scarano FR (2010) Plant-plant associations and population structure of four woody plant species in a patchy coastal vegetation of Southeastern Brazil. Rev Bras Bot 33:607–613Google Scholar
  12. Brulheide H, Manegold M, Jandt U (2004) The genetical structure of Populus euphratica and Alhagi sparsifolia stands in the Taklimakan desert. In: Runge M, Zhang X (eds) Ecophysiology and habitat requirement of perennial plant species in the Taklimakan desert. Shaker, Aachen, pp 153–160Google Scholar
  13. Cahill JF (2013) Plant competition: can understanding trait-behavior linkages offer a new perspective on very old questions? Nova Acta Leopoldina 114(391):115–125Google Scholar
  14. Callaway RM (2013) Facilitation, competition and the organization of plant communities. Nova Acta Leopoldina 114(391):147–157Google Scholar
  15. Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–1965Google Scholar
  16. Cardoso D, Särkinen T, Alexander S, Amorim AM, Bittrich V et al (2017) Amazon plant diversity revealed by a taxonomical verified species list. Proc Nat Acad Sci U S A 114:10695–10700Google Scholar
  17. Dangles O, Herrera M, Anthelme F (2013) Experimental support of the stress-gradient hypothesis in herbivore-herbivore interactions. New Phytol 197:405–408Google Scholar
  18. de Freitas CA, Scarano FR, Biesboer DD (2003) Morphological variation in two facultative epiphytic bromeliads growing on the floor of a swamp forest. Biotropica 35:546–550Google Scholar
  19. 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 11:363–369Google Scholar
  20. de Mattos EA, Scarano FS, Cavalin PO, Fernandes WG, Rennenberg H, Lüttge U (2019) Ecophysiological performance of four species of Clusiaceae with different modes of photosynthesis in a mosaic of riverine, rupestrian grasslands and cerrado vegetation in SE-Brazil. Trees 33.  https://doi.org/10.1007/s00468-018-1805-x
  21. Dias ATC, Scarano FR (2007) Clusia as nurse plant. In: Lüttge U (ed) Clusia – a woody neotropical genus with remarkable plasticity and diversity. Springer, Heidelberg, pp 55–72Google Scholar
  22. Duarte HM, Gessler A, Scarano FR, Franco AC, de Mattos EA, Nahm M, Rennenberg H, Rodrigues PJFP, Zaluar HLT, Lüttge U (2005) Ecophysiology of six selected shrub species in different plant communities at the periphery of the Atlantic Forest of SE-Brazil. Flora 200:456–476Google Scholar
  23. Ebeling A, Klein AM, Tscharntke T (2011) Plant-flower visitor interaction webs: temporal stability and pollinator specialization increases along an experimental diversity gradient. Basic Appl Ecol 12:300–309Google Scholar
  24. Ellenberg H (1981) Ursachen des Vorkommens und Fehlens von Sukkulenten in den Trockengebieten der Erde. Flora 171:114–169Google Scholar
  25. Fiedler K, Beck E (2008) Investing gradients in ecosystem analysis. In: Beck E, Bendix J, Kottke I, Makeschin F, Mosandl R (eds) Gradients in a tropical mountain ecosystem of Ecuador, Ecological studies, vol 198. Springer, Berlin, pp 49–54Google Scholar
  26. Franco AC, Lüttge U (2002) Midday depression in savanna trees: coordinated adjustments in photochemical efficiency, photorespiration, CO2 assimilation and water use efficiency. Oecologia 131:356–365Google Scholar
  27. Franco AC, Olivares E, Ball E, Lüttge U, Haag-Kerwer A (1994) In situ studies of crassulacean acid metabolism in several sympatric species of tropical tress of the genus Clusia. New Phytol 126:203–211Google Scholar
  28. Franco AC, Haag-Kerwer A, Herzog B, Grams TEE, Ball E, de Mattos EA, Scarano FR, Barreto S, 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 10:359–365Google Scholar
  29. Functional Plant Biology (2002) CO2 concentrating mechanisms in aquatic photosynthetic organisms. Funct Plant Biol 29(2 and 3)Google Scholar
  30. Gessler A, Duarte HM, Franco AC, Lüttge U, de Mattos EA, Nahm M, Rodrigues PJFP, Scarano FR, Rennenberg H (2005a) Ecophysiology of selected tree species in different plant communities at the periphery of the Atlantic Forest of SE Brazil. III. Three legume trees in a semideciduous dry forest. Trees 19:523–530Google Scholar
  31. Gessler A, Duarte HM, Franco AC, Lüttge U, de Mattos EA, Nahm M, Scarano FR, Zaluar HLT, Rennenberg H (2005b) Ecophysiology of selected tree species in different plant communities at the periphery of the Atlantic Forest of SE Brazil. II. Spatial and ontogenetic dynamics in Andira legalis, a deciduous tree. Trees 19:510–522Google Scholar
  32. Gessler A, Nitschke R, de Mattos EA, Zaluar HLT, Scarano FR, Rennenberg H, Lüttge U (2008) Comparison of the performance of three different ecophysiological life forms in a sandy coastal restinga ecosystem of SE-Brazil: a nodulated N2-fixing C3-shrub (Andira legalis (Vell.) Toledo), a CAM-shrup (Clusia hilariana Schltdl.) and a tap root C3-hemicryptophye (Allagoptera arenaria (Gomes) O. Ktze.). Trees 22:105–119Google Scholar
  33. Grams TEE, Lüttge U (2011) Space as a resource. Progr Bot 72:349–370Google Scholar
  34. Grams TEE, Haag-Kerwer A, Olivares E, Ball E, Arndt S, Popp M, Medina E, Lüttge U (1997) Comparative measurements of chlorophyll a fluorescence, acid accumulation and gas exchange in exposed and shaded plants of Clusia minor L. and Clusia multiflora H.B.K. in the field. Trees 11:240–247Google Scholar
  35. Grant MC (1993) The trembling plant. Discover (Los Angeles) 84:82–89Google Scholar
  36. Green JM, Williams GJ (1982) The subdominant status of Echinocereus viridiflorus and Mammillaria vivipara in shortgrass prairie: the role of temperature and water effects on gas exchange. Oecologia 52:43–48Google Scholar
  37. Griffin JN, O’Gorman EJ, Emmerson MC, Jenkins SR, Klein A-M, Loreau M, Symstad A (2009) Biodiversity and the stability of ecosystem functioning. In: Naeem S, Bunker DE, Hector A, Loreau M, Perrings C (eds) Biodiversity, ecosystem functioning, and human well beeing. Oxford University Press, Oxford, pp 78–93Google Scholar
  38. Griffiths H, Smith JAC (1983) Photosynthetic pathways in the Bromeliaceae of Trinidad: relations between life-forms, habitat preference and occurrence of CAM. Oecologia 60:176–184Google Scholar
  39. Griffiths H, Smith JAC, Lüttge U, Popp M, Cram WJ, Diaz M, Lee HSJ, Medina E, Schäfer C, Stimmel K-H (1989) Ecophysiology of xerophytic and halophytic vegetation of a coastal alluvial plain in northern Venezuela. IV. Tillandsia flexuosa Sw. and Schomburgkia humboldtiana Reichb., epiphytic CAM plants. New Phytol 111:273–282Google Scholar
  40. Grime JP, Mackey JML, Hillier SH, Read DJ (1987) Floristic diversity in a model system using experimental microcosms. Nature 328:420–422Google Scholar
  41. Gustafsson MHG, Winter K, Bittrich V (2007) Diversity, phylogeny and classification of Clusia. In: Lüttge U (ed) Clusia. A woody neotropical genus of remarkable plasticity and diversity. Ecol Stud, vol 94, Springer, Berlin, pp 95–116Google Scholar
  42. Haag-Kerwer A, Grams TEE, Olivares E, Ball E, Arndt S, Popp M, Medina E, Lüttge U (1996) Comparative measurements of gas exchange, acid accumulation and chlorophyll a fluorescence of different species of Clusia showing C3 photosynthesis, or crassulacean acid metabolism, at the same field site in Venezuela. New Phytol 134:215–226Google Scholar
  43. Hector A, Schmid B, Beierkuhnlein C, Caldeira MC, Diemer M, Dimitrakopoulos PG, Finn JA, Freitas H, Giller PS, Good J, Harris R, Högberg P, Huss-Danell K, Joshi J, Jumpponen A, Körner C, Leadley PW, Loreau M, Minns A, Mulder CPH, O’Donovan G, Otway SJ, Pereira JS, Prinz A, Read DJ, Scherer-Lorenzen M, Schulze E-D, Siamantziouras A-SD, Spehn EM, Terry AC, Troumbis AY, Woodward FI, Yachi S, Lawton JH (1999) Plant diversity and productivity experiments in European grasslands. Science 286:1123–1127Google Scholar
  44. Heldt HW, Piechulla B (2008) Pflanzenbiochmie, 4th edn. Spektrum Akademischer Verlag, HeidelbergGoogle Scholar
  45. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335Google Scholar
  46. Herzog B, Hübner C, Ball E, Bastos RN, Franco AC, Scarano FR, Lüttge U (1999a) 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 coastal restinga of Brazil. Plant Biol 1:453–459Google Scholar
  47. Herzog B, Hoffmann S, Hartung W, Lüttge U (1999b) Comparison of photosynthetic responses of the sympatric tropical C3 species Clusia multiflora H.B.K. and the C3-CAM intermediate species Clusia minor L. to irradiance and drought stress in a phytotron. Plant Biol 1:460–470Google Scholar
  48. Hibberd JM, Sheehy JE, Langdale JA (2008) Using C4 photosynthesis to increase the yield of rice – rationale and feasibility. Curr Opin Plant Biol 11:228–231Google Scholar
  49. Huang JK, Ray CP, Rozelle S (2002) Enhancing the crops to feed the poor. Nature 418:678–684Google Scholar
  50. Journal of Experimental Botany (2017) C4 photosynthesis: 50 years of discovery and innovation. J Exp Bot 68(2), special issueGoogle Scholar
  51. Jurić I, González-Pérez V, Hibberd JM, Edwards G, Burroughs NJ (2017) Size matters for single-cell C4 photosynthesis in Bienertia. J Exp Bot 68:255–267Google Scholar
  52. Kemperman JA, Barnes BV (1976) Clone size in American aspens. Can J Bot 54:2603–2607Google Scholar
  53. Kluge M, Brulfert J, Rauh W, Ravelomanana D, Ziegler H (1995) Ecophysiological studies on the vegetation of Madagascar: a δ13C and δD survey for incidence of Crassulacean acid metabolism (CAM) among orchids from montane forests and succulents from the xerophytic thorn-bush. Isotopes Environ Health Stud 31:191–210Google Scholar
  54. Körner C (2012) Biological diversity – the essence of life and ecosystem functioning. Nova Acta Leopoldina 116(394):147–159Google Scholar
  55. Lange OL, Schulze E-D, Kappen L, Evenari M, Buschbom U (1975) CO2 exchange pattern under natural conditions of Caralluma negevenis, a CAM plant of the Negev desert. Photosynthetica 9:318–326Google Scholar
  56. Lauterbach M, Billakurthi K, Kadereit G, Ludwig M, Westhoff P, Gowik U (2017) C3 cotyledons are followed by C4 leaves: intra-individual transcriptome analysis of Salsola soda (Chenopodiaceae). J Exp Bot 68:161–176Google Scholar
  57. Lee HSJ, Lüttge U, Medina E, Smith JAC, Cram WJ, Diaz M, Griffitsh H, Popp M, Schäfer C, Stimmel K-H, Thonke B (1989) Ecophysiology of xerophytic and halophytic vegetation of a coastal alluvial plain in northern Venezuela. III. Bromelia humilis Jacq., a terrestrial CAM bromeliad. New Phytol 111:253–271Google Scholar
  58. Li Y, Heckmann D, Lercher MJ, Maurino VG (2017) Combining genetic and evolutionary engineering to establish C4 metabolism in C3 plants. J Exp Bot 68:117–125Google Scholar
  59. Lin Y, Berger U, Grimm V, Ji Q-R (2012) Differences between symmetric and asymmetric facilitation matter: exploring the interplay between modes of positive and negative plant interactions. J Ecol 100:1482–1491Google Scholar
  60. Loomis WE (1953) Growth and differentiation – an introduction and summary. In: Loomis WE (ed) Growth and differentiation in plants. Iowa State College Press, Ames, pp 1–17Google Scholar
  61. Loreau M, Mazancourt CD (2013) Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecol Lett 16:106–115Google Scholar
  62. Lovelock J (1979) Gaia. A new look at life on Earth. Oxford University Press, OxfordGoogle Scholar
  63. Lovelock J (2009) The vanishing face of Gaia – a final warning. Basic Books, New YorkGoogle Scholar
  64. Lovelock J (2010) Our sustainable retreat. In: Crist E, Rinker HB (eds) Gaia in turmoil: climate change, biodepletion, and Earth ethics in an age of crisis. MIT Press, Cambridge, pp 21–24Google Scholar
  65. Luo Y, Nobel PS (1993) Growth characteristics of newly initiated cladodes of Opuntia ficus-indica as affected by shading, drought and elevated CO2. Physiol Plant 87:467–474Google Scholar
  66. Lüttge U (1986) Nocturnal water storage in plants having crassulacean acid metabolism. Planta 168:287–289Google Scholar
  67. Lüttge U (1987) Carbon dioxide and water demand: crassulacean acid metabolism (CAM), a versatile ecological adaptation exemplifying the need for integration in ecophysiological work. New Phytol 106:593–629Google Scholar
  68. Lüttge U (ed) (1989) Vascular plants as epiphytes. Evolution and ecophysiology. Ecol Stud, vol 76, Springer, BerlinGoogle Scholar
  69. Lüttge U (1999) One morphotype, three physiotypes: sympatric species of Clusia with obligate C3 photosynthesis, obligate CAM and C3-CAM intermediate behaviour. Plant Biol 1:138–148Google Scholar
  70. Lüttge U (2002) CO2 concentrating: consequences in crassulacean acid metabolism. J Exp Bot 53:2131–2142Google Scholar
  71. Lüttge U (2004) Ecophysiology of crassulacean acid metabolism (CAM). Ann Bot 93:629–652Google Scholar
  72. Lüttge U (2005) Physiologische Ökologie der Photosynthese – autökologische und synökologische Aspekte anhand von δ13C- und δ18O-Daten. In: Rundgespräche der Kommission für Ökologie, Bay Akad Wiss: Auf Spurensuche in der Natur, vol 30. Dr. Friedrich Pfeil, München, pp 69–82Google Scholar
  73. Lüttge U (2006) Photosynthetic flexibility and ecophysiological plasticity: questions and lessons from Clusia, the only CAM tree, in the tropics. New Phytol 171:7–25Google Scholar
  74. Lüttge U (ed) (2007a) Clusia. A woody neotropical genus of remarkable plasticity and diversity, Ecological studies, vol 194. Springer, BerlinGoogle Scholar
  75. Lüttge U (2007b) Photosynthesis. In: Lüttge U (ed) Clusia. A woody neotropical genus of remarkable plasticity and diversity, Ecological studies, vol 194. Springer, Berlin, pp 135–186Google Scholar
  76. Lüttge U (2007c) Physiological ecology. In: Lüttge U (ed) Clusia. A woody neotropical genus of remarkable plasticity and diversity, Ecological studies, vol 194. Springer, Berlin, pp 187–234Google Scholar
  77. Lüttge U (2008a) Physiological ecology of tropical plants, 2nd edn. Springer, BerlinGoogle Scholar
  78. Lüttge U (2008b) Clusia: holy grail and enigma. J Exp Bot 59:1503–1514Google Scholar
  79. Lüttge U (2010) Ability of crassulacean acid metabolism plants to overcome interacting stresses in tropical environments. AoB Plants 2010:plq005.  https://doi.org/10.1093/aobpla/plq005CrossRefGoogle Scholar
  80. Lüttge U (2011) Photorespiration in phase III of crassulacean acid metabolism: evolutionary and ecophysiological implications. Progr Bot 72:371–384Google Scholar
  81. Lüttge U (2012) Modularity and emergence: biology’s challenge in understanding life. Plant Biology 14:865–871Google Scholar
  82. Lüttge U (2013) Evo-Devo-Eco and ecological stem species: potential repair systems in the planetary biosphere crisis. Progr Bot 74:191–212Google Scholar
  83. Lüttge U (2016) Plants shape the terrestrial environment on Earth: challenges of management for sustainability. Progr Bot 77:187–217Google Scholar
  84. Lüttge U, Scarano FR (2004) Ecophysiology. Rev Bras Bot 27:1–10Google Scholar
  85. 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. Rev Bras Bot 30(3):355–364Google Scholar
  86. Lüttge U, Medina E, Cram WJ, Lee HSJ, Popp M, Smith JAC (1989a) Ecophysiology of xerophytic and halophytic vegetation of a coastal alluvial plain in northern Venezuela. II. Cactaceae. New Phytol 111:245–251Google Scholar
  87. Lüttge U, Popp M, Medina E, Cram WJ, Diaz M, Griffiths H, Lee HSJ, Schäfer C, Smith JAC, Stimmel K-H (1989b) Ecophysiology of xerophytic and halophytic vegetation of a coastal alluvial plain in northern Venezuela. V. The Batis maritimaSesuvium portulacastrum vegetation unit. New Phytol 111:283–291Google Scholar
  88. Lüttge U, Fetene M, Liebig M, Rascher U, Beck E (2001) Ecophysiology of niche occupation by two giant rosette plants, Lobelia gibberoa Hemsl and Solanecio gigas (Vatke) C. Jeffrey, in an afromontane forest valley. Ann Bot 88:267–278Google Scholar
  89. Lüttge U, Scarano FR, de Mattos EA, Franco AC, Broetto F, Dias ATC, Duarte HM, Uehlein N, Wendt T (2015) Does ecophysiological behaviour explain habitat occupation of sympatric Clusia species in a Brazilian Atlantic rainforest? Trees 29:1973–1988Google Scholar
  90. Martins RL, Wendt T, Margis R, Scarano FR (2007) Reproductive biology. In: Lüttge U (ed) Clusia – a woody neotropical genus with remarkable plasticity and diversity. Springer, Heidelberg, pp 73–94Google Scholar
  91. Matyssek R, Lüttge U (2013) Gaia: the planet holobiont. In: Matyssek R, Lüttge U, Rennenberg H (eds) The alternatives growth and defense: resource allocation at multiple scales in plants. Nova Acta Leopoldina NF114/391, pp 325–344Google Scholar
  92. Matyssek R, Schnyder H, Elstner E-F, Munch J-C, Pretzsch H, Sandermann H (2002) Growth and parasite defence in plants: the balance between resource sequestration and retention. Plant Biol 4:133–136Google Scholar
  93. Matyssek R, Agerer R, Ernst D, Munch J-C, Oßwald W, Pretzsch H, Priesack E, Schnyder H, Treutter D (2005) The plant’s capacity in regulating resource demand. Plant Biol 7:560–580Google Scholar
  94. Matyssek R, Koricheva J, Schnyder H, Ernst D, Munch JC, Oßwald W, Pretzsch H (2012) The balance between resource sequestration and retention: a challenge in plant science. In: Matyssek R, Schnyder H, Oßwald W, Ernst D, Munch JC, Pretzsch H (eds) Growth and defence in plants. Resource allocation at multiple scales, Ecological studies, vol 220. Springer, Heidelberg, pp 3–24Google Scholar
  95. Medina E, Cram WJ, Lee HSJ, Lüttge U, Popp M, Smith JAC, Diaz M (1989) Ecophysiology of xerophytic and halophytic vegetation of a coastal alluvial plain in northern Venezuela. I. Site description and plant communities. New Phytol 111:233–243Google Scholar
  96. Mitchell PL, Sheehy JE (2006) Superarching rice photosynthesis to increase yield. New Phytol 171:688–693Google Scholar
  97. Nobel PS (1996) High productivity of certain agronomic CAM species. In: Winter K, Smith JAC (eds) Crassulacean acid metabolism. Biochemistry, ecophysiology and evolution, Ecological stuies, vol 114. Springer, New York, pp 255–265Google Scholar
  98. Oliver TH, Heard MS, Isaac NJB, Roy DB, Procter D, Eigenbrod F, Freckleton R, Hector A, Orme CDL, Petchey OL, Proença V, Raffaelli D, Suttle KB, Mace GM, Martín-López B, Woodcock BA, Bullock JM (2015) Biodiversity and resilience of ecosystem functions. Trends Ecol Evol 30:673–684Google Scholar
  99. Osmond CB (1978) Crassulacean acid metabolism: a curiosity in context. Annu Rev Plant Physiol 29:379–414Google Scholar
  100. Osmond CB, Grace SC (1995) Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? J Exp Bot 46:1351–1362Google Scholar
  101. Pathre U, Sinha AK, Shirke PA, Sane PV (1998) Factors determining the midday depression of photosynthesis in trees under monsoon climate. Trees 12:472–481Google Scholar
  102. Pierce S, Winter K, Griffiths H (2002) The role of CAM in high rainfall cloud forests: an in situ comparison of photosynthetic pathways in Bromeliaceae. Plant Cell Environ 25:1181–1189Google Scholar
  103. Pimentel MCP, Barros MJ, Cirne P, de Mattos EA, Oliveira RC, Pereira MCA, Scarano FR, Zaluar HLT, Araujo DSD (2007) Spatial variation in the structural and floristic composition of “restinga” vegetation in southeastern Brazil. Rev Bras Bot 30:543–551Google Scholar
  104. Pittendrigh C (1948) The bromeliad-Anopheles-malaria complex in Trinidad. I. The bromeliad flora. Evolution 2:58–89Google Scholar
  105. Plant, Cell and Environment (1986) Bromeliad ecophysiology. Plant Cell Environ 9(5)Google Scholar
  106. Popp M, Kramer D, Lee H, Diaz M, Ziegler H, Lüttge U (1987) Crassulacean acid metabolism in tropical dicotyledonous trees of the genus Clusia. Trees 1:238–247Google Scholar
  107. Proulx R, Wirth C, Voigt W, Weigelt A, Roscher C, Attinger S, Baade J, Barnard RL, Buchmann N, Buscot F, Eisenhauer N, Fischer M, Gleixner G, Halle S, Hildebrandt A, Kowalski E, Kuu A, Lange M, Milcu A, Niklaus PA, Oelmann Y, Rosenkranz S, Sabais A, Scherber C, Scherer-Lorenzen M, Scheu S, Schulze E-D, Schumacher J, Schwichtenberg G, Soussana J-F, Temperton VM, Weisser WW, Wilcke W, Schmid B (2010) Diversity promotes temporal stability across levels of ecosystem organization in experimental grassland. Plos One 5:e13382Google Scholar
  108. Pyankov VI, Ziegler H, Akhani H, Deigele C, Lüttge U (2010) European plants with C4 photosynthesis: geographical and taxonomic distribution and relations to climate parameters. Bot J Linn Soc 163:283–304Google Scholar
  109. Ratajczak R, Richter J, Lüttge U (1994) Adaptation of the tonoplast V-type H+-ATPase of Mesembryanthemum crystallinum to salt stress, C3-CAM transition and plant age. Plant Cell Environ 17:1101–1112Google Scholar
  110. 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 110:135–142Google Scholar
  111. Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota NM (2009) The Brazilian Atlantic forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153Google Scholar
  112. 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, pp 405–434Google Scholar
  113. Rizzini CT (1979) Tratado de Fitogeografia do Brasil, vol 2. Edusp, São PauloGoogle Scholar
  114. 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 106:28–38Google Scholar
  115. Roscher C, Temperton VM, Scherer-Lorenzen M, Schmitz M, Schumacher J, Schmid B, Buchmann N, Weisser WW, Schulze E-D (2005) Overyielding in experimental grassland communities – irrespective of species pool or spatial scale. Ecol Lett 8:419–429Google Scholar
  116. Sage RF (2016) A portrait of the C4 photosynthetic family on the 50th anniversary of its discovery: species number, evolutionary lineages, and Hall of Fame. J Exp Bot 67:4039–4056Google Scholar
  117. Sage RF, Pearcy RW (2000) The physiological ecology of C4 photosynthesis. In: Leegood RC, Sharkey TD, von Caemmerer S (eds) Photosynthesis: physiology and metabolism. Kluwer Academic Publisher, Dordrecht, pp 497–532Google Scholar
  118. Sage RF, Stata M (2015) Photosynthetic diversity meets biodiversity: the C4 plant example. J Plant Physiol 172:104–119Google Scholar
  119. Sage RF, Li M, Monson RK (1999) The taxonomic distribution of C4 photosynthesis. In: Sage RF, Monson RK (eds) C4 plant biology. Academic Press, New York, pp 551–584Google Scholar
  120. Scarano FR (2002) Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic rainforest. Ann Bot 90:517–524Google Scholar
  121. Scarano FR (2009) Plant communities at the periphery of the Atlantic rain forest: rare-species bias and its risks for conservation. Biol Conserv 142:1201–1208Google Scholar
  122. Scarano FR, Ribeiro KT, Moraes LFD, Lima HC (1997) Plant establishment on flooded and non-flooded patches of a swamp forest in southeastern Brazil. Brazil J Trop Ecol 14:793–803Google Scholar
  123. Scarano FR, de Mattos EA, Franco AC, Herzog B, Ball E, Grams TEE, Mantovani A, Barreto S, Haag-Kerwer A, Lüttge U (1999) Habitat segregation of C3 and CAM Nidularium (Bromeliaceae) in response to different light regimes in the understory of a swamp forest in southeastern Brazil. Flora 194:281–288Google Scholar
  124. 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 geographic distribution to ecophysiological parameters. Bot J Linn Soc 136:345–364Google Scholar
  125. Scarano FR, Duarte HM, Franco AC, Gessler A, de Mattos EA, Rennenberg H, Lüttge U (2005a) Physiological synecology of tree species in relation to geographic distribution and ecophysiological parameters at the Atlantic forest periphery in Brazil: an overview. Trees 19:493–496Google Scholar
  126. Scarano FR, Duarte HM, Franco AC, Gessler A, de Mattos EA, Nahm M, Rennenberg H, Zaluar HLT, Lüttge U (2005b) Ecophysiology of selected tree species in different plant communities at the periphery of the Atlantic Forest of SE Brazil. I. Performance of three different species of Clusia in an array of plant communities. Trees 19:497–509Google Scholar
  127. Scherber C, Eisenhauer N, Weisser WW, Schmid B, Voigt W, Fischer M, Schulze E-D, Roscher C, Weigelt A, Allan E, Beßler H, Bonkowski M, Buchmann N, Buscot F, Clement LW, Ebeling A, Engels C, Halle S, Kertscher I, Klein AM, Koller R, König S, Kowalski E, Kummer V, Kuu A, Lange M, Lauterbach D, Middelhoff C, Migunova VD, Milcu A, Müller R, Partsch S, Petermann JS, Renker C, Rottstock T, Sabais A, Scheu S, Schumacher J, Temperton VM, Tscharntke T (2010) Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment. Nature 468:553–556Google Scholar
  128. Schläpfer F, Schmid B (1999) Ecosystem effects of biodiversity: a classification of hypotheses and exploration of empirical results. Ecol Appl 9:893–912Google Scholar
  129. Schulze E-D, Lange OL, Evenari M, Kappen L, Buschbom U (1974) The role of air humidity and leaf temperature in controlling stomatal resistance of Prunus armeniaca L. under desert conditions. I. A simulation of the daily course of stomatal resistance. Oecologia 17:159–170Google Scholar
  130. Schulze E-D, Lange OL, Kappen L, Evenari M, Buschbom U (1975a) The role of air humidity and leaf temperature in controlling stomatal resistance of Prunus armeniaca L. under desert conditions. II. The significance of leaf water status and internal carbon dioxide concentration. Oecologia 18:219–233Google Scholar
  131. Schulze E-D, Lange OL, Evenari M, Kappen L, Buschbom U (1975b) The role of air humidity and leaf temperature in controlling stomatal resistance of Prunus armeniaca L. under desert conditions. III. The effect on water use efficiency. Oecologia 19:303–314Google Scholar
  132. Schüssler C, Freitag H, Koteyeva N, Schmidt D, Edwards G, Voznesenskaya E, Kadereit G (2017) Molecular phylogeny and forms of photosynthesis in tribe Salsoleae (Chenopodiaceae). J Exp Bot 68:207–223Google Scholar
  133. Silva B, Roos K, Voss I, König N, Rollenbeck R, Scheibe R, Beck E, Bendix J (2012) Simulating canopy photosynthesis for two competing species of an anthropogenic grassland community in the Andes of southern Ecuador. Ecol Model 239:14–26Google Scholar
  134. Smith JAC (1989) Epiphytic bromeliads. In: Lüttge U (ed) Vascular plants as epiphytes. Evolution and ecophysiology. Ecol Stud, vol 76, pp 109–138, Springer, BerlinGoogle Scholar
  135. Smith JAC, Griffiths H, Bassett M, Griffiths NM (1985) Day-night changes in the leaf water relations of epiphytic bromeliads in the rain forests of Trinidad. Oecologia 67:475–485Google Scholar
  136. Smith JAC, Griffiths H, Lüttge U (1986) Comparative ecophysiology of CAM and C3 bromeliads. I. The ecology of the Bromeliaceae in Trinidad. Plant Cell Environ 9:359–376Google Scholar
  137. Souza GM, Lüttge U (2015) Stability as a phenomenon emergent from plasticity – complexity – diversity in eco-physiology. Progr Bot 76:211–239Google Scholar
  138. Souza GM, Bertolli SC, Lüttge U (2016) Hierarchy and information in a system approach to plant biology: explaining the irreducibility in plant ecophysiology. Progr Bot 77:167–186Google Scholar
  139. Spreitzer RJ, Salvucci ME (2002) RUBISCO: structure, regulatory interactions, and possibilities for a better enzyme. Annu Rev Plant Biol 53:449–457Google Scholar
  140. Surridge C (2002) Agricultural biotech: the rice squad. Nature 416:576–578Google Scholar
  141. Tenhunen JD, Lange OL, Gebel J, Beyschlag W, Weber JA (1984) Changes in photosynthetic capacity, carboxylation efficiency, and CO2-compensation point associated with midday stomatal closure and midday depression of net CO2 exchange of leaves of Quercus suber. Planta 162:193–203Google Scholar
  142. 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 Museo de Biologia Mello Leitão (Nova Série) 7:3–86Google Scholar
  143. Tilman D, Wedin D, Knops J (1996) Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379:718–720Google Scholar
  144. Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C (2001) Diversity and productivity in a long-term grassland experiment. Science 294:843–845Google Scholar
  145. Tilman D, Reich PB, Knops JMH (2006) Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441:629–632Google Scholar
  146. Vareschi V (1980) Vegetationsökologie der Tropen. Eugen Ulmer, StuttgartGoogle Scholar
  147. Walter H, Breckle SW (1984) Ökologie der Erde. 2. Spezielle Ökologie der tropischen und subtropischen Zonen. Gustav Fischer, StuttgartGoogle Scholar
  148. Weigelt A, Weisser WW, Buchmann N, Scherer-Lorenzen M (2009) Biodiversity for multifunctional grasslands: equal productivity in high-diversity low-input and low-diversity high-input systems. Biogeosciences 6:1695–1706Google Scholar
  149. Winter K, von Willert DJ (1972) NaCl-induzierter Crassulaceensäurestoffwechsel bei Mesembryanthemum crystallinum. Z Pflanzenphysiol 67:166–170Google Scholar
  150. 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 3–23Google Scholar
  151. Zotz G, Hietz P (2001) The physiological ecology of vascular epiphytes: current knowledge, open questions. J Exp Bot 52:2067–2078Google Scholar

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Authors and Affiliations

  1. 1.Department of BiologyTechnical University of DarmstadtDarmstadtGermany

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