Photosynthetic pathways in Bromeliaceae: phylogenetic and ecological significance of CAM and C3 based on carbon isotope ratios for 1893 species

• Published in: Botanical journal of the Linnean Society Vol. 178; no. 2; pp. 169 - 221
• Main Authors: Crayn, Darren M, Winter, Klaus, Schulte, Katharina, Smith, J. Andrew C
• Format: Journal Article
• Language: English
• Published: Oxford Academic Press 01.06.2015; Blackwell Publishing Ltd; Oxford University Press
• Subjects: adaptive radiation; carbon; Crassulacean acid metabolism; Dyckia; ecophysiology; epiphytes; epiphytism; isotopes; Neotropics; photosynthesis; phylogeny; surveys; temperature; Tillandsia; tropics
• ISSN: 0024-4074; 1095-8339
• DOI: 10.1111/boj.12275

A comprehensive analysis of photosynthetic pathways in relation to phylogeny and elevational distribution was conducted in Bromeliaceae, an ecologically diverse Neotropical family containing large numbers of both terrestrial and epiphytic species. Tissue carbon isotope ratio (δ¹³C) was used to determine the occurrence of crassulacean acid metabolism (CAM) and C₃photosynthesis in 1893 species, representing 57% of species and all 56 genera in the family. The frequency of δ¹³C values showed a strongly bimodal distribution: 1074 species (57%) had values more negative than −20‰ (mode = −26.7‰), typical of predominantly daytime carbon fixation via the C₃pathway, whereas 819 species (43%) possessed values less negative than −20‰ (mode = −13.3‰), indicative of predominantly nocturnal fixation of carbon via the CAM pathway. Amongst the six almost exclusively terrestrial subfamilies in Bromeliaceae, Brocchinioideae, Lindmanioideae and Navioideae consisted entirely of C₃species, with CAM species being restricted to Hechtioideae (all species of Hechtia tested), Pitcairnioideae (all species belonging to a xeric clade comprising Deuterocohnia, Dyckia and Encholirium) and Puyoideae (21% of Puya spp.). Of the other two subfamilies, in the overwhelmingly epiphytic (plus lithophytic) Tillandsioideae, 28% of species possessed CAM photosynthesis, all restricted to the derived genus Tillandsia and tending towards the more extreme epiphytic ‘atmospheric’ life‐form. In Bromelioideae, with comparable numbers of terrestrial and epiphytic species, 90% of taxa showed CAM; included in these are the first records of CAM photosynthesis in Androlepis, Canistropsis, Deinacanthon, Disteganthus, Edmundoa, Eduandrea, Hohenbergiopsis, Lymania, Pseudananas, Ronnbergia and Ursulaea. With respect to elevational gradients, the greatest number of C₃bromeliad species were found at mid‐elevations between 500 and 1500 m, whereas the frequency of CAM species declined monotonically with increasing elevation. However, in Puya, at least ten CAM species have been recorded at elevations > 3000 m, showing that CAM photosynthesis is not necessarily incompatible with low temperatures. This survey identifies five major origins of CAM photosynthesis at a higher taxonomic level in Bromeliaceae, but future phylogenetic work is likely to reveal a more fine‐scale pattern of gains and losses of this trait, especially in ecologically diverse and widely distributed genera such as Tillandsia and Puya. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 178, 169–221.