Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Distribution of crassulacean acid metabolism in orchids of Panama: evidence of selection for weak and strong modes

Katia Silvera A C , Louis S. Santiago B and Klaus Winter A
+ Author Affiliations
- Author Affiliations

A Smithsonian Tropical Research Institute, P.O. Box 2072, Balboa, Ancón, Republic of Panama.

B Department of Integrative Biology and Center for Stable Isotope Biogeochemistry, 3060 Valley Life Science Building, University of California, Berkeley, CA 94720, USA.

C Corresponding author. Email: katiasilvera@yahoo.com

D This paper originates from a presentation at the IVth International Congress on Crassulacean Acid Metabolism, Tahoe City, California, USA, July–August 2004

Functional Plant Biology 32(5) 397-407 https://doi.org/10.1071/FP04179
Submitted: 3 October 2004  Accepted: 6 January 2005   Published: 27 May 2005

Abstract

Crassulacean acid metabolism (CAM) is one of three metabolic pathways found in vascular plants for the assimilation of carbon dioxide. In this study, we investigate the occurrence of CAM photosynthesis in 200 native orchid species from Panama and 14 non-native species by carbon isotopic composition (δ13C) and compare these values with nocturnal acid accumulation measured by titration in 173 species. Foliar δ13C showed a bimodal distribution with the majority of species exhibiting values of approximately –28‰ (typically associated with the C3 pathway), or –15‰ (strong CAM). Although thick leaves were related to δ13C values in the CAM range, some thin-leaved orchids were capable of CAM photosynthesis, as demonstrated by acid titration. We also found species with C3 isotopic values and significant acid accumulation at night. Of 128 species with δ13C more negative than –22‰, 42 species showed nocturnal acid accumulation per unit fresh mass characteristic of weakly expressed CAM. These data suggest that among CAM orchids, there may be preferential selection for species to exhibit strong CAM or weak CAM, rather than intermediate metabolism.

Keywords: carbon stable isotope, crassulacean acid metabolism, evolution, Orchidaceae, photosynthesis.


Acknowledgments

We thank Orquideas Tropicales, Inc. and Dr Gaspar Silvera for permitting the use and abuse of the orchids in the greenhouse. We are grateful to Dr Aurelio Virgo for competent assistance in the laboratory. K.S. acknowledges Dr Robert L. Dressler and Dr Germán Carnevali for discussions and comments on species nomenclature. This work was supported by the Smithsonian Tropical Research Institute, the Andrew W. Mellon Foundation, a Smithsonian Tropical Research Institute Internship to K.S. and a National Science Foundation Fellowship to L.S.S.


References


Atwood JT (1986) The size of the Orchidaceae and the systematic distribution of epiphytic orchids. Selbyana 9, 171–186. open url image1

Bender MM, Rouhani I, Vines HM, Black CC (1973) 13C / 12C ratio changes in crassulacean acid metabolism plants. Plant Physiology 52, 427–430. open url image1

Borland AM, Griffiths H, Broadmeadow MSJ, Fordham MC, Maxwell C (1993) Short-term changes in carbon-isotope discrimination in the C3–CAM intermediate Clusia minor L. growing in Trinidad. Oecologia 95, 444–453.
Crossref | GoogleScholarGoogle Scholar | open url image1

Crayn DM, Smith JAC, Winter K (2001) Carbon-isotope ratios and photosynthetic pathways in the Rapateaceae. Plant Biology 3, 569–576.
Crossref | GoogleScholarGoogle Scholar | open url image1

Crayn DM, Winter K, Smith JAC (2004) Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae. Proceedings of the National Academy of Sciences USA 101, 3703–3708.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dressler, RL (1993a). ‘Field guide to the orchids of Costa Rica and Panama.’ a. (Cornell University Press: Ithaca, NY)

Dressler, RL (1993b). ‘Phylogeny and classification of the orchid family.’ b. (Cambridge University Press: Cambridge)

Dressler RL (2002) New species and combinations in Costa Rican orchids. II. Lankesteriana 3, 28. open url image1

Dressler RL, Higgins WE (2003) Guarianthe, a generic name for the Cattleya skinneri complex. Lankesteriana 7, 37–38. open url image1

Dressler RL, Williams NH (2003) New combinations in mesoamerican Oncidiinae (Orchidaceae). Selbyana 24, 44–45. open url image1

Ehleringer, JR ,  and  Osmond, CB (1989). Stable isotopes. In ‘Plant physiological ecology’. pp. 255–280. (Chapman and Hall: London)

Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40, 503–537.
Crossref | GoogleScholarGoogle Scholar | open url image1

Franco AC, Ball E, Lüttge U (1992) Differential effects of drought and light levels on accumulation of citric and malic acids during CAM in Clusia.  Plant, Cell and Environment 15, 821–829. open url image1

Griffiths H (1992) Carbon isotope discrimination and the integration of carbon assimilation pathways in terrestrial CAM plants. Plant, Cell and Environment 15, 1051–1062. open url image1

Higgins WE (1997) A reconsideration of the genus Prosthechea (Orchidaceae). Phytologia 82, 370–383. open url image1

Holtum JAM, Winter K (1999) Degrees of crassulacean acid metabolism in tropical epiphytic and lithophytic ferns. Australian Journal of Plant Physiology 26, 749–757. open url image1

Holtum JAM, Aranda J, Virgo A, Gehrig HH, Winter K (2004) δ13C values and crassulacean acid metabolism in Clusia species from Panama. Trees — Structure and Function 18, 658–668. open url image1

Kluge M, Brulfert J, Ravelomanana D, Lipp J, Ziegler H (1991) Crassulacean acid metabolism in Kalanchoë species collected in various climatic zones of Madagascar: a survey by δ13C analysis. Oecologia 88, 407–414.
Crossref | GoogleScholarGoogle Scholar | open url image1

Luer C (2004) Pleurothallis subgenus Acianthera and three allied subgenera. A second century of new species of Stelis of Ecuador. Epibator, Ophidion, Zootrophion. Addenda to Brachionidium, Dracula, Lepanthes, Platystele, Pleurothallis, Porroglossum and Masdevallia. New genera and combinations. Monographs in Systematic Botany from Missouri Botanical Garden 95, 1–265. open url image1

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 Phytologist 106, 593–629. open url image1

Ojeda I, Carnevali G, Romero-González GA (2005) New species and combinations in Heterotaxis Lindley (Orchidaceae: Maxillariinae) with a nomenclatural synopsis of the genus. Novon In press , open url image1

O’Leary MH (1981) Carbon isotope fractionation in plants. Phytochemistry 20, 553–567.
Crossref | GoogleScholarGoogle Scholar | open url image1

O’Leary MH (1988) Carbon isotopes in photosynthesis. Bioscience 38, 328–336. open url image1

Osmond CB, Allaway WG, Sutton BG, Troughton JH, Queiroz O, Lüttge U, Winter K (1973) Carbon isotope discrimination in photosynthesis of CAM plants. Nature 246, 41–42. open url image1

Pierce S, Winter K, Griffiths H (2002) Carbon isotope ratio and the extent of daily CAM use by Bromeliaceae. New Phytologist 156, 75–83.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pridgeon AM, Chase MW (2001) A phylogenetic reclassification of Pleurothallidinae (Orchidaceae). Lindleyana 16, 235–271. open url image1

Pridgeon AM, Solano R, Chase MW (2001) Phylogenetic relationships in Pleurothallidinae (Orchidaceae): combined evidence from nuclear and plastid DNA sequences. American Journal of Botany 88, 2286–2308. open url image1

Rundel PW, Rundel JA, Ziegler H, Stichler W (1979) Carbon isotope ratios of central Mexican Crassulaceae in natural and glasshouse environments. Oecologia 38, 45–50.
Crossref | GoogleScholarGoogle Scholar | open url image1

Smith, JAC ,  and  Winter, K (1996). Taxonomic distribution of crassulacean acid metabolism. In ‘Crassulacean acid metabolism’. pp. 427–436. (Springer-Verlag: Berlin)

Ting IP (1985) Crassulacean acid metabolism. Annual Review of Plant Physiology 36, 595–622.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wanek W, Huber W, Arndt SK, Popp M (2002) Mode of photosynthesis during different life stages of hemiepiphytic Clusia species. Functional Plant Biology 29, 725–732.
Crossref | GoogleScholarGoogle Scholar | open url image1

Williams NH, Chase MW, Fulcher T, Whitten WM (2001a) Molecular systematics of the Oncidiinae based on evidence from four DNA sequence regions: expanded circumscriptions of Cyrtochilum, Erycina, Otoglossum and Trichocentrum and a new genus (Orchidaceae). Lindleyana 162, 113–139. open url image1

Williams NH, Chase MW, Whitten WM (2001b) Phylogenetic position of Miltoniopsis, Caucaea, a new genus, Cyrtochiloides and relationship of Oncidium phymatochilum based on nuclear and chloroplast DNA sequence data (Orchidaceae: Oncidiinae). Lindleyana 16, 272–285. open url image1

Winter K (1979) δ13C values of some succulent plants from Madagascar. Oecologia 40, 103–112.
Crossref | GoogleScholarGoogle Scholar | open url image1

Winter, K ,  and  Smith, JAC (1996). An introduction to crassulacean acid metabolism: biochemical principles and ecological diversity. In ‘Crassulacean acid metabolism’. pp. 1–13. (Springer-Verlag: Berlin)

Winter K, Holtum JAM (2002) How closely do the δ13C values of crassulacean acid metabolism plants reflect the proportion of CO2 fixed during day and night? Plant Physiology 129, 1843–1851.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Winter K, Wallace BJ, Stocker GC, Roksandic Z (1983) Crassulacean acid metabolism in Australian vascular epiphytes and some related species. Oecologia 57, 129–141.
Crossref | GoogleScholarGoogle Scholar | open url image1

Winter K, Aranda J, Holtum JAM (2005) Carbon isotope composition and water-use efficiency in plants with crassulacean acid metabolism. Functional Plant Biology 32, 381–388.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zotz G (2004) How prevalent is crassulacean acid metabolism among vascular epiphytes? Oecologia 138, 184–192.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zotz G, Ziegler H (1997) The occurrence of crassulacean acid metabolism among vascular epiphytes from Central Panama. New Phytologist 137, 223–229.
Crossref | GoogleScholarGoogle Scholar | open url image1