In the epiphytic tillandsioids, Guzmania monostachia, Werauhia sanguinolenta, and Guzmania lingulata (Bromeliaceae), juvenile plants exhibit an atmospheric habit, whereas in adult plants the leaf bases overlap and form water-holding tanks. CO2 gas-exchange measurements of the whole, intact plants and δ13C values of mature leaves demonstrated that C3 photosynthesis was the principal pathway of CO2 assimilation in juveniles and adults of all three species. Nonetheless, irrespective of plant size, all three species were able to display features of facultative CAM when exposed to drought stress. The capacity for CAM was the greatest in G. monostachia, allowing drought-stressed juvenile and adult plants to exhibit net CO2 uptake at night. CAM expression was markedly lower in W. sanguinolenta, and minimal in G. lingulata. In both species, low-level CAM merely sufficed to reduce nocturnal respiratory net loss of CO2. δ13C values were generally less negative in juveniles than in adult plants, probably indicating increased diffusional limitation of CO2 uptake in juveniles.
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crassulacean acid metabolism
photon flux density (400–700 nm)
Smithsonian Tropical Research Institute
leaf-air water vapour pressure difference
Abràmoff, M.D., Magelhães, P.J., Ram, S.J.: Image processing with ImageJ. — Biophot. Int. 11: 36–42, 2004.
Adams, W.W.III, Martin, C.E.: Physiological consequences of changes in life form of the Mexican epiphyte Tillandsia deppeana (Bromeliaceae). — Oecologia 70: 298–304, 1986a.
Adams, W.W.III, Martin, C.E.: Morphological changes accompanying the transition from juvenile (atmospheric) to adult (tank) forms in the Mexican epiphyte Tillandsia deppeana (Bromeliaceae). — Amer. J. Bot. 73: 1207–1214, 1986b.
Benzing, D.H.: Bromeliaceae — Profile of an Adaptive Radiation. — Cambridge Univ. Press, Cambridge 2000.
Cernusak, L.A., Winter, K., Aranda, J. et al.: Transpiration efficiency of a tropical pioneer tree (Ficus insipida) in relation to soil fertility. — J. Exp. Bot. 58: 3549–3566, 2007.
Cernusak, L.A., Winter, K., Aranda, J., Turner, B.L.: Conifers, angiosperm trees, and lianas: growth, whole-plant water and nitrogen use efficiency, and stable isotope composition (δ13C and δ18O) of seedlings grown in a tropical environment. — Plant Physiol. 148: 642–659, 2008.
Crayn, D.M., Winter, K., Smith, J.A.C.: Multiple origins of crassulacean acid metabolism and the epiphytic habit in the neotropical family Bromeliaceae. — Proc. Nat. Acad. Sci. USA 101: 3703–3708, 2004.
Farquhar, G.D., Ehleringer, J.R., Hubick, K.T.: Carbon isotope discrimination and photosynthesis. — Annu. Rev. Plant Physiol. Plant Mol. Biol. 40: 503–537, 1989.
Givnish, T.J., Barfuss, M.H.J., Van Ee, B. et al.: Phylogeny, adaptive radiation, and historical biogeography in Bromeliaceae: insights from an eight-locus plastid phylogeny. — Amer. J. Bot. 98: 872–895, 2011.
Goldstein, G., Andrade, J.L., Nobel, P.S.: Differences in water relations parameters for the chlorenchyma and the parenchyma of Opuntia ficus-indica under wet versus dry conditions. — Aust. J. Plant Physiol. 18: 95–107, 1991.
Griffiths, H., Lüttge, U., Stimmel, K.H. et al.: Comparative ecophysiology of CAM and C3 bromeliads. III. Environmental influences on CO2 assimilation and transpiration. — Plant Cell Environ. 9: 385–393, 1986.
Griffiths, H., Maxwell, K.: In memory of C.S. Pittendrigh: does exposure in forest canopies relate to photoprotective strategies in epiphytic bromeliads. — Functional Ecology 13: 15–23, 1999.
Griffiths, H., Smith, J.A.C.: Photosynthetic pathways in the Bromeliaceae of Trinidad: relation between life forms, habitat preference and occurrence of CAM. — Oecologia 60: 176–184, 1983.
Holtum, J.A.M., Smith, J.A.C., Neuhaus, H.E.: Intracellular transport and pathways of carbon flow in plants with crassulacean acid metabolism. — Funct. Plant Biol. 32: 429–449, 2005.
Holtum, J.A.M., Winter, K.: Degrees of crassulacean acid metabolism in tropical epiphytic and lithophytic ferns. — Aust. J. Plant Physiol. 26: 749–757, 1999.
Holtum, J.A.M., Winter, K.: Carbon isotope composition of canopy leaves in a tropical forest in Panama throughout a seasonal cycle. — Trees 19: 545–561, 2005.
Holtum, J.A.M., Winter, K.: Photosynthetic CO2 uptake in seedlings of two tropical tree species exposed to oscillating elevated concentrations of CO2. — Planta 218: 152–158, 2003.
Lüttge, U., Klauke, B., Griffiths, H. et al.: Comparative ecophysiology of CAM and C3 bromeliads. V. Gas exchange and leaf structure of the C3 bromeliad Pitcairnia integrifolia. — Plant Cell Environ. 9: 411–419, 1986b.
Lüttge, U., Stimmel, K.-H., Smith, J.A.C., Griffiths, H.: Comparative ecophysiology of CAM and C3 bromeliads. II. Field measurements of gas exchange of CAM bromeliads in the humid tropics. — Plant Cell Environ. 9: 377–383, 1986a.
Maxwell, K.: Resistance is useful: diurnal patterns of photosynthesis in C3 and crassulacean acid metabolism epiphytic bromeliads. — Funct. Plant Biol. 29: 679–687, 2002.
Maxwell, C., Griffiths, H., Borland, A.M. et al.: Photoinhibitory responses of the epiphytic bromelioid Guzmania monostachia during the dry season in Trinidad maintain photochemical integrity under adverse conditions. — Plant Cell Environ. 15: 37–47, 1992.
Maxwell, C., Griffiths, H., Young, A.J.: Photosynthetic acclimation to light regime and water stress by the C3-CAM epiphyte Guzmania monostachia: gas-exchange characteristics, photochemical efficiency and the xanthophyll cycle. — Funct. Ecol. 8: 745–754, 1994.
Medina, E., Delgado, M., Troughton, J.H., Medina, J.D.: Physiological ecology of CO2 fixation in Bromeliaceae. — Flora 166: 137–152, 1977.
Medina, E., Minchin, P.: Stratification of δ13C values in Amazonian rain forests. — Oecologia 45: 377–378, 1980.
Mez, C.: [Physiological studies on Bromeliaceae. I. The water economy of extremely atmospheric tillandsias.] — Jahr. Wiss. Bot. 40: 157–229, 1904. [In German]
Osmond, C.B.: Crassulacean acid metabolism: a curiosity in context. — Annu. Rev. Plant Physiol. 29: 379–414, 1978.
Pierce, S., Maxwell, K., Griffiths, H., Winter, K.: Hydrophobic trichome layers and epicuticular wax powders in Bromeliaceae. — Amer. J. Bot. 88: 1371–1389, 2001.
Pierce, S., Winter, K., Griffiths, H.: Carbon isotope ratio and the extent of daily CAM use by Bromeliaceae. — New Phytol. 156: 75–83, 2002.
R Development Core Team: A language and environment for statistical computing. — R Foundation for Statistical Computing, Vienna 2011.
Schmidt, G., Zotz, G.: Ecophysiological consequences of differences in plant size: in situ carbon gain and water relations of the epiphytic bromeliad, Vriesea sanguinolenta. — Plant Cell Environ. 24: 101–111, 2001.
Schmidt, J.E., Kaiser, W.M.: Response of the succulent leaves of Peperomia magnoliaefolia to dehydration: water relations and solute movement in chlorenchyma and hydrenchyma. — Plant Physiol. 83: 190–194, 1987.
Smith, J.A.C., Griffiths, H., Bassett, M., Griffiths, N.M.: Daynight changes in the leaf water relations of epiphytic bromeliads in the rain forests of Trinidad. — Oecologia 67: 475–485, 1985.
Smith, J.A.C., Griffiths, H., Lüttge, U.: Comparative ecophysiology of CAM and C3 bromeliads. I. The ecology of the Bromeliaceae in Trinidad. — Plant Cell Environ. 9: 359–376, 1986.
Silvera, K., Santiago, L.S., Winter, K.: Distribution of crassulacean acid metabolism in orchids of Panama: evidence of selection for weak and strong modes. — Funct. Plant Biol. 32: 397–407, 2005.
Tomlinson, P.B.: Monocotyledons — towards an understanding of their morphology and anatomy. — Adv. Bot. Res. 3: 207–292, 1970.
West-Eberhard, M.J., Smith, J.A.C., Winter, K.: Photosynthesis, reorganized. — Science 332: 311–312, 2011.
Winter, K., Aranda, J.E., Holtum, J.A.M.: Carbon isotope composition and water-use efficiency in plants with crassulacean acid metabolism. — Funct. Plant Biol. 32: 381–388, 2005.
Winter, K., Garcia, M., Holtum, J.A.M.: On the nature of facultative and constitutive CAM: environmental and developmental control of CAM expression during early growth of Clusia, Kalanchoë, and Opuntia. — J. Exp. Bot. 59: 1829–1840, 2008.
Winter, K., Garcia, M., Holtum, J.A.M.: Drought-stress-induced up-regulation of CAM in seedlings of a tropical cactus, Opuntia elatior, operating predominantly in the C3 mode. — J. Exp. Bot. 62: 4037–4042, 2011.
Winter, K., Holtum, J.A.M.: How closely do the ·13C values of crassulacean acid metabolism plants reflect the proportion of CO2 fixed during day and night? — Plant Physiol. 129: 1843–1851, 2002.
Winter, K., Holtum, J.A.M.: Environment or development? Lifetime net CO2 exchange and control of the expression of crassulacean acid metabolism in Mesembryanthemum crystallinum. — Plant Physiol. 143: 98–107, 2007.
Winter, K., Holtum, J.A.M.: Induction and reversal of crassulacean acid metabolism in Calandrinia polyandra: effects of soil moisture and nutrients. — Funct. Plant Biol. 38: 576–582, 2011.
Winter, K., Smith, J.A.C. (ed.): Crassulacean Acid Metabolism. — Ecological Studies, Vol. 114. Springer, Berlin — Heidelberg — New York 1996.
Zotz, G., Enslin, A., Hartung, W., Ziegler, H.: Physiological and anatomical changes during the early ontogeny of the heteroblastic bromeliad, Vriesea sanguinolenta, do not concur with the morphological change from atmospheric to tank form. — Plant Cell Environ. 27: 1341–1350, 2004.
Zotz, G., Harris, G.K., Königer, M., Winter K.: High rates of photosynthesis in the tropical pioneer tree, Ficus insipida Willd. — Flora 190: 265–272, 1995.
Zotz, G., Wilhelm, K., Becker, A.: Heteroblasty—A review. — Bot. Rev. 77: 109–151, 2011.
Acknowledgements: J.D.B. was recipient of a short-term fellowship from the Smithsonian Tropical Research Institute and received travel support from the Facultad de Ciencias, Universidad de los Andes. Dayana Agudo performed the δ13C analyses, Jorge Ceballos helped with microscopy, and Oris Acevedo provided logistical support on Barro Colorado Nature Monument.
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Beltrán, J.D., Lasso, E., Madriñán, S. et al. Juvenile tank-bromeliads lacking tanks: do they engage in CAM photosynthesis?. Photosynthetica 51, 55–62 (2013). https://doi.org/10.1007/s11099-012-0077-8