, Volume 18, Issue 6, pp 658–668

δ13C values and crassulacean acid metabolism in Clusia species from Panama

  • Joseph A. M. Holtum
  • Jorge Aranda
  • Aurelio Virgo
  • Hans H. Gehrig
  • Klaus Winter
Original Article


The genus Clusia is notable in that it contains arborescent crassulacean acid metabolism (CAM) plants. As part of a study of CAM in Clusia, titratable acidities were measured in 25 species and δ13C values were measured for 38 species from Panamá, including seven undescribed species, and 11 species from Colombia, Costa Rica and Honduras. CAM was detected in 12 species. Clusia flava, C. rosea and C. uvitana exhibited δ13C values or diurnal fluctuations in acidity indicative of strong CAM. In C. croatii, C. cylindrica, C. fructiangusta, C. lineata, C. odorata, C. pratensis, C. quadrangula, C. valerioi and C. sp. D diurnal fluctuations in acidity were consistent with weak CAM but the δ13C values were C3-like. All of the species that exhibited strong or weak CAM were in the C. flava or C. minor species groups. CAM was not detected in any member of the C. multiflora species group. Strong CAM species were not collected at altitudes above 680 m a.s.l. On the basis of δ13C values, the expression of CAM was similar in terrestrial, hemi-epiphytic and epiphytic species and did not differ between individuals of the same species that exhibited different life-forms. This study indicates that phylogenetic affiliation may be a predictor of an ability to exhibit CAM in Clusia species from the Panamanian region, and that weak CAM is probably a common photosynthetic option in many Clusia species. δ13C value is not a particularly good indicator of a potential of Clusia species growing in the field to exhibit CAM because it appears that the contribution in most species of CAM to carbon gain is generally rather small when integrated over the life-time of leaves.


Clusia Crassulacean acid metabolism (CAM) Photosynthetic pathway Stable carbon isotopes 


  1. Arroyo MK, Medina E, Ziegler H (1990) Distribution and δ 13C values of Portulacaceae species of the high Andes in northern Chile. Bot Acta 103:291–295Google Scholar
  2. Borland AM, Griffiths H, Maxwell K, Broadmeadow MSJ, Griffiths N, Barnes JD (1992) On the ecophysiology of Clusiaceae in Trinidad; expression of CAM in Clusia minor L. during the transition from wet to dry season and characterization of three endemic species. New Phytol 122:349–357Google Scholar
  3. Borland AM, Griffiths H, Broadmeadow MSJ, Fordham H, Maxwell K (1993) Short-term changes in carbon isotope discrimination in the C3-CAM intermediate Clusia minor L. growing in Trinidad. Oecologia 95:444–453Google Scholar
  4. Borland AM, Técsi LI, Leegood RC, Walker RP (1998) Inducibility of crassulacean acid metabolism (CAM) in Clusia species; physiological/biochemical characterisation and intercellular localization of carboxylation and decarboxylation processes in three species which exhibit different degrees of CAM. Planta 205:342–351CrossRefGoogle Scholar
  5. Crayn DM, Smith JAC, Winter K (2001) Carbon-isotope ratios and photosynthetic pathways in the Neotropical family Rapateaceae. Plant Biol 3:569–576CrossRefGoogle Scholar
  6. Crayn DM, Winter K, Smith JAC (2004) Multiple origins of CAM photosynthesis and the epiphytic habit in the Neotropical family Bromeliaceae. Proc Natl Acad Sci USA 101:3703–3708CrossRefPubMedGoogle Scholar
  7. Davidse G, Herrera Ch, Warner RH (1984) Collection index key: DAVIDSE 26075, specimen ID: 00202147, w3TROPICOS Exsiccatae Data Base. Missouri Botanical Garden, MissouriGoogle Scholar
  8. Diaz M, Haag-Kerwer A, Wingfield R, Ball E, Olivares E, Grams TEE, Ziegler H, Lüttge U (1996) Relationships between carbon and hydrogen isotope ratios and nitrogen levels in leaves of Clusia species and two other Clusiaceae genera at various sites and different altitudes in Venezuela. Trees 10:351–358CrossRefGoogle Scholar
  9. Earnshaw MJ, Winter K, Ziegler H, Stichler W, Crutwell NEG, Kerenga K, Cribb PJ, Wood J, Croft JR, Carver KA, Gunn TC (1987) Altitudinal changes in the incidence of crassulacean acid metabolism in vascular epiphytes and related life forms in Papua New Guinea. Oecologia 73:566–572Google Scholar
  10. Franco AC, Ball E, Lüttge U (1990) Patterns of gas exchange and organic acid oscillations in tropical trees of the genus Clusia. Oecologia 85:108–114Google Scholar
  11. Franco AC, Ball E, Lüttge U (1991) The influence of nitrogen, light and water stress on CO2 exchange and organic acid accumulation in the C3-CAM tree, Clusia minor. J Exp Bot 42:597–603Google Scholar
  12. Gehrig HH, Aranda J, Cushman MA, Virgo A, Cushman JC, Hammel BE, Winter K (2003) Cladogram of Panamanian Clusia based on nuclear DNA: implications for the origins of crassulacean acid metabolism. Plant Biol 5:59–70CrossRefGoogle Scholar
  13. Gibson AC, Nobel PS (1990) The cactus primer. Harvard University Press, CambridgeGoogle Scholar
  14. Grams TEE, Herzog B, Lüttge U (1998) Are there species in the genus Clusia with obligate C-3-photosynthesis? J Plant Physiol 152:1–9Google Scholar
  15. Gustafsson MHG, Bittrich V (2002) Evolution and morphological diversity and resin secretion in flowers of Clusia (Clusiaceae): insights from ITS sequence variation. Nord J Bot 22:183–203Google Scholar
  16. Gustafsson MHG, Bittrich V, Stevens PF (2002) Phylogeny of Clusiaceae based on RBCL sequences. Int J Plant Sci 163:1045–1054CrossRefGoogle Scholar
  17. Haag-Kerwer A, Franco AC, Lüttge U (1992) The effect of temperature and light on gas exchange and acid accumulation in the C3-CAM plant Clusia minor. J Exp Bot 43:345–352Google Scholar
  18. Hammel BE (1986) New species of Clusiaceae from Central America with notes on Clusia and synonymy in the tribe Clusieae. Selbyana 9:112–120Google Scholar
  19. Harling G, Andersson L (1985) Collection index key: HARLING 23754, specimen ID: 00208420, w3TROPICOS Exsiccatae Data Base. Missouri Botanical Garden, St. LouisGoogle Scholar
  20. Holmgren PK, Holmgren NH, Barnett LC (1990) Index herbarium. I. The herbaria of the world. New York Botanical Garden, New YorkGoogle Scholar
  21. Holtum JAM, Winter K (1999) Degrees of crassulacean acid metabolism in tropical epiphytic and lithophytic ferns. Aust J Plant Physiol 26:749–757Google Scholar
  22. Keeley JE, Keeley SC (1989) Crassulacean acid metabolism (CAM) in a high elevation tropical cactus. Plant Cell Environ 12:331–336Google Scholar
  23. Keeley JE, Osmond CB, Raven JA (1984) Stylites, a vascular land plant without stomata absorbs CO2 via its roots. Nature 310:694–695Google Scholar
  24. Lüttge U (1996) Clusia: plasticity and diversity in a genus of C3/CAM intermediate tropical trees. In: Winter K, Smith JAC (eds) Crassulacean acid metabolism. Springer, Berlin Heidelberg New York, pp 296–311Google Scholar
  25. 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
  26. Lüttge U, Pfeiffer T, Fischer-Schliebs E, Ratajczak R (2000) The role of vacuolar malate-transport capacity in crassulacean acid metabolism and nitrate nutrition. Higher malate-transport capacity in ice plant after crassulacean acid metabolism-induction and in tobacco under nitrate nutrition. Plant Physiol 124:1335–1347CrossRefPubMedGoogle Scholar
  27. de Mattos EA, Lüttge U (2001) Chlorophyll fluorescence and organic acid oscillations during transition from CAM to C3-photosynthesis in Clusia minor L. (Clusiaceae). Ann Bot 88:457–463CrossRefGoogle Scholar
  28. Maguire B (1976) Apomixis in the genus Clusia (Clusiaceae)—a preliminary report. Taxon 25:241–244Google Scholar
  29. Medina E, Delgado M (1976) Photosynthesis and night CO2-fixation in Echeveria columbiana Poellnitz. Photosynthetica 10:155–163Google Scholar
  30. Pierce S, Winter K, Griffiths H (2002a) The role of CAM in high rainfall cloudforests: an in situ comparison of photosynthetic pathways in Bromeliaceae. Plant Cell Environ 25:1183–1192CrossRefGoogle Scholar
  31. Pierce S, Winter K, Griffiths H (2002b) Carbon isotope ratio and the extent of daily CAM use by Bromeliaceae. New Phytol 156:75–84CrossRefGoogle Scholar
  32. Pipoly JJ, Kearns DM, Berry PE (1998) Clusia In: Berry PE, Holst BK, Yatskievych K (eds) Flora of the Venezuelan Guayana, vol 4, Caesalpiniaceae-Ericaceae. Missouri Botanical Garden, St. Louis, pp 260–294Google Scholar
  33. Schmitt AK, Lee HSJ, Lüttge U (1988) The response of the C3-CAM tree, Clusia rosea, to light and water stress. J Exp Bot 39:1581–1590Google Scholar
  34. Smith JAC, Ingram J, Tsiantis MS, Barkla BJ, Bartholomew DM, Bettey M, Pantoja O, Pennington AJ (1996) Transport across the vacuolar membrane in CAM plants. In: Winter K, Smith JAC (eds) Crassulacean acid metabolism. Springer, Berlin Heidelberg New York, pp 53–71Google Scholar
  35. Sternberg LSL, Ting IP, Price D, Hann J (1987) Photosynthesis in epiphytic and rooted Clusia rosea Jacq. Oecologia 72:457–460Google Scholar
  36. Ting IP, Lord EM, Sternberg da SL, DeNiro MJ (1985) Crassulacean acid metabolism in the strangler Clusia rosea Jacq. Science 229:969–971Google Scholar
  37. Tinoco Ojanguren C, Vásquez-Yanez V (1983) Especies CAM en la selva húmeda tropical de los Tuxtlas Veracruz. Bol Soc Bot Méx 45:150–153Google Scholar
  38. Vaasen A, Begerow D, Lüttge U, Hampp R (2002) The genus Clusia L.: molecular evidence for independent evolution of photosynthetic flexibility. Plant Biol 4:86–93Google Scholar
  39. Wanek W, Huber H, Arndt SK, Popp M (2002) Mode of photosynthesis during different life stages of hemiepiphytic Clusia species. Funct Plant Biol 29:725–732CrossRefGoogle Scholar
  40. 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 129:1843–1851CrossRefPubMedGoogle Scholar
  41. Winter K, Smith JAC (eds) (1996) Crassulacean acid metabolism. Springer, Berlin Heidelberg New YorkGoogle Scholar
  42. Winter K, Wallace BJ, Stocker GC, Roksandic Z (1983) Crassulacean acid metabolism in Australian vascular epiphytes and some related species. Oecologia 57:129–141Google Scholar
  43. Winter K, Zotz G, Baur B, Dietz KJ (1992) Light and dark CO2 fixation in Clusia uvitana as affected by plant water status and CO2 availability. Oecologia 91:47–51Google Scholar
  44. Zotz G, Winter K (1993) Short-term regulation of crassulacean acid metabolism activity in a tropical hemiepiphyte, Clusia uvitana. Plant Physiol 102:835–841PubMedGoogle Scholar
  45. Zotz G, Winter K (1994) A one-year study of carbon, water and nutrient relationships in a tropical C3-CAM hemi-epiphyte, Clusia uvitana. New Phytol 127:45–60Google Scholar
  46. Zotz G, Winter K (1996) Seasonal changes in daytime versus nighttime CO2 fixation of Clusia uvitana in situ. In: Winter K, Smith JAC (eds) Crassulacean acid metabolism. Springer, Berlin Heidelberg New York, pp 312–323Google Scholar
  47. Zotz G, Reichling P, Krack S (1999) Another woody hemiepiphyte with CAM: Havetiopsis flexilis SPRUCE ex PLANCH. Et TR. (Clusiaceae). Flora 194:215–220Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Joseph A. M. Holtum
    • 1
    • 2
  • Jorge Aranda
    • 1
  • Aurelio Virgo
    • 1
  • Hans H. Gehrig
    • 1
  • Klaus Winter
    • 1
  1. 1.Smithsonian Tropical Research InstituteBalboaRepublic of Panama
  2. 2.Tropical Plant Sciences, School of Tropical BiologyJames Cook UniversityTownsvilleAustralia

Personalised recommendations