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Australia Lacks Stem Succulents but Is It Depauperate in Plants With Available online at www.sciencedirect.com ScienceDirect Australia lacks stem succulents but is it depauperate in plants with crassulacean acid metabolism (CAM)? 1,2 3 3 Joseph AM Holtum , Lillian P Hancock , Erika J Edwards , 4 5 6 Michael D Crisp , Darren M Crayn , Rowan Sage and 2 Klaus Winter In the flora of Australia, the driest vegetated continent, [1,2,3]. Crassulacean acid metabolism (CAM), a water- crassulacean acid metabolism (CAM), the most water-use use efficient form of photosynthesis typically associated efficient form of photosynthesis, is documented in only 0.6% of with leaf and stem succulence, also appears poorly repre- native species. Most are epiphytes and only seven terrestrial. sented in Australia. If 6% of vascular plants worldwide However, much of Australia is unsurveyed, and carbon isotope exhibit CAM [4], Australia should host 1300 CAM signature, commonly used to assess photosynthetic pathway species [5]. At present CAM has been documented in diversity, does not distinguish between plants with low-levels of only 120 named species (Table 1). Most are epiphytes, a CAM and C3 plants. We provide the first census of CAM for the mere seven are terrestrial. Australian flora and suggest that the real frequency of CAM in the flora is double that currently known, with the number of Ellenberg [2] suggested that rainfall in arid Australia is too terrestrial CAM species probably 10-fold greater. Still unpredictable to support the massive water-storing suc- unresolved is the question why the large stem-succulent life — culent life-form found amongst cacti, agaves and form is absent from the native Australian flora even though euphorbs. He identified a rainfall predictability envelope exotic large cacti have successfully invaded and established in within which the majority of large succulents in the Australia. Americas and Africa are found and argued that the lack of such environments in Australia explained the lack of Addresses 1 large succulents in Australia (Figure 1a). Nonetheless, Terrestrial Ecosystems and Climate Change, College of Marine and Environmental Sciences, James Cook University, Townsville 4811, exotic large succulents have successfully invaded native Queensland, Australia vegetation in Australia, occupying areas of rainfall 2 Smithsonian Tropical Research Institute, PO Box 0843-03092, Balboa, predictability outside Ellenberg’s envelope (Figure 1b– Anco´ n, Panama 3 d). For example, in the 1920s, 1.5 billion tons of the Department of Ecology and Evolutionary Biology, Brown University, Box G-W, Providence, RI 02912, USA obligate CAM stem-succulent Opuntia stricta infested 4 Research School of Biology, Australian National University, Canberra 25 million ha of eastern Australia [6,7]. The Opuntia 2601, ACT, Australia 5 incursion has been explained as an anomaly enabled by Australian Tropical Herbarium, James Cook University, PO Box 6811, the destruction of native woody vegetation [2,8,9]. How- Cairns 4870, Queensland, Australia 6 ever, 90 years after the virtual eradication of Opuntia by Department of Ecology and Evolutionary Biology, University of Toronto, Canada the introduced moth, Cactoblastus cactorum, around 27 spe- cies of opuntioid cacti have naturalized across a range of Corresponding author: Holtum, Joseph AM ([email protected]) soil types and climatic zones in south eastern Australia [10] infesting 1 million ha in South Australia alone [11], Current Opinion in Plant Biology 2016, 31:109–117 again outside the Ellenberg envelope (Figure 1d). Fur- thermore, we now know that Agave tequilana, a large This review comes from a themed issue on Physiology and metabolism obligate CAM leaf-succulent native to Central America, can achieve high rates of biomass accumulation under Edited by Robert T Furbank and Rowan F Sage Australian rainfall conditions [12,13]. For a complete overview see the Issue and the Editorial Available online 15th April 2016 The apparent underrepresentation of CAM and succu- http://dx.doi.org/10.1016/j.pbi.2016.03.018 lence in the Australian terrestrial flora is somewhat of an enigma. Worldwide, CAM has evolved over 60 times in 1369-5266/Published by Elsevier Ltd. 35 families of vascular plants and succulence has appeared in many major plant lineages [14,15], although the appearance of large stem-succulents is less common. Increasing aridity and falling CO2 concentration during the Miocene are thought to have provided the ecological Introduction opportunity for a global surge in the diversification of Australia is the driest vegetated continent and is the only succulent and CAM lineages [3,14]. But apparently in warm continent with no native large stem-succulents Australia, the Miocene and Pliocene expansion of arid www.sciencedirect.com Current Opinion in Plant Biology 2016, 31:109–117 110 Physiology and metabolism Table 1 The evidence for CAM in the 107 endemic Australian vascular plants for which CAM is currently documented. Unless specified otherwise, the evidence is for leaf tissue. Species are listed if they are Australian natives and they exhibit at least one of the following three characteristics: an organ has a d13C value less negative than S20%, a tissue exhibits nocturnal acidification, or an organ exhibits a gas- exchange pattern characteristic of CAM. 13 + Family, genus and species Habit d C DH CAM gas-exchange À1 % mmol g fwt Aizoaceae Carpobrotus rossii (Haw) Schwantes T À21.8 [17] 6 [17] Disphyma crassifolium subsp. clavellatum (Haw) Chinnock T À20.7 [17] 96 [17], 10 [17] Anacampserotaceae A Anacampseros australiana J.M. Black T À23.8 [44] 58 [44] Yes Apocynaceae Dischidia major (Vahl) Merr. E À16.0 [45], À17.8 [27] Dischidia nummularia R.Br. E À15.7 to À17.6 [27] Dischidia ovata Benth. E À14.8 [27] A Hoya anulata Schltr. E À13.3 Hoya australis R.Br. ex J.Traill E À15.8 to À19.2 [27] Hoya australis R.Br. ex J.Traill subsp. australis E À15.9 to À18.6 [27] A Hoya macgillivrayi F.M.Bailey E À18.2 A Hoya pottsii J.Traill E À13.2 , À18.3 [27] Hoya revoluta Wight ex. Hook.f. E À11.8 [27] A Cynanchum viminale subsp. australe (R.Br.) Meve & Liede T À12.3 [17] 155 [17] Yes Crassulaceae Crassula helmsii (Kirk) Cockayne A 70 [46] Yes [46] Crassula sieberiana (Schult. & Schulte.f.) Druce T 5 [24] Yes [24] Lycopodiaceae Isoetes australis S.Williams A 56 [28] Isoetes drummondii A.Braun A 78 [28] Montiaceae A Calandrinia polyandra Benth T À22.2 [25], À26.1 60 [25] Yes [25] Orchidaceae Bulbophyllum aurantiacum F.Muell. E À12.4 [27] Bulbophyllum baileyi F.Muell. L À16.8 [27] A Bulbophyllum bowkettiae F.M. Bailey E À17.0 A Bulbophyllum gadgarrense Rupp E À15.7 A Bulbophyllum globuliforme Nicholls E À11.1 A Bulbophyllum gracillimum (Rolfe) Rolfe E À12.6 A Bulbophyllum longiflorum Thouars E À12.7 A Bulbophyllum macphersonii Rupp E À12.2 [27], À15.2 A Bulbophyllum minutissimum F.Muell. E À12.3 , À17.0 [27] Bulbophyllum shepherdii (F.Muell.) Rchb.f. E À12.1 [27], À13.9 [27] 13 [27] A Bulbophyllum sladeanum A.D.Hawkes E À13.2 A Bulbophyllum wadsworthii Dockrill E À18.6 A Bulbophyllum windsorense B.Gray & D.L. Jones E À18.2 A Cadetia maideniana (Schltr.) Schltr. E À13.1 [27], À14.3 A Cadetia wariana Schltr. E À14.9 , À16.1 [27] A Chiloschista phyllorhiza (F.Muell.) Schltr. (root) E À16.0 , À17.5 [27] 12–40 [27] A Cymbidium canaliculatum R.Br. E À17.4 , À18.7 [27] A Dendrobium aemulum R.Br. E À13.4 A Dendrobium antennatum Lindl. E À13.5 , À14.1 [27] A Dendrobium aphyllum (Roxb.) C.E.C. Fisch. E À13.9 Dendrobium beckleri F. Muell. E À14.7 [27] 25 [27], 35 [27] Dendrobium bifalce Lindl. E À18.1 [27] A Dendrobium bigibbum Lindl. E À11.9 [27], À14.3 A Dendrobium cacatua M.A.Clem. & D.L.Jones E À16.6 A Dendrobium callitrophilum B.Gray & D.L. Jones E À11.5 A Dendrobium canaliculatum R.Br. E À12.0 , À13.1 [26] A Dendrobium comptonii Rendle E À19.5 A Dendrobium x delicatum (F.M.Bailey) F.M. Bailey E À16.7 Dendrobium dicuphum F.Muell. E À14.1 [27] A Dendrobium discolor Lindl. E À13.8 [27], À15.4 Dendrobium gracilicaule F.Muell. E À18.3 to À25.2 [27] A Dendrobium x gracillimum (Rupp) Leaney E À17.8 A Dendrobium johannis Rchb.f. E À13.8 , À13.9 [26] A Dendrobium lichenastrum (F.Muell.) Kraenzl. E À12.6 to À17.3 [27] A Dendrobium litorale Schltr. E À12.5 Current Opinion in Plant Biology 2016, 31:109–117 www.sciencedirect.com CAM in Australia Holtum et al. 111 Table 1 (Continued ) 13 + Family, genus and species Habit d C DH CAM gas-exchange À1 % mmol g fwt Dendrobium nindii W.Hill E À13.5 [27] A Dendrobium prenticei (F.Muell.) Nicholls E À15.6 Dendrobium speciosum Sm. E À14.5 to À15.9 [4] 3 [26] A Dendrobium x superbiens Rchb.f. E À13.8 A Dendrobium tetragonum A.Cunn. E À15.8 , À18.2 [27] A Dendrobium toressae (F.M. Bailey) Dockrill E À16.6 , À17.6 [27] A Didymoplexis pallens Griff. E À17.2 A Dockrillia bowmanii (Benth.) M.A.Clem. & D.L.Jones E À13.5 A Dockrillia brevicauda (D.L.Jones & M.A.Clem.) E À10.9 M.A.Clem. & D.L.Jones A Dockrillia calamiformis (Lodd.) M.A.Clem. & D.L. Jones E À15.5 A Dockrillia cucumerina (MacLeay ex Lindl.) Brieger E À12.9 , À13.5 [27] A Dockrillia dolichophylla (D.L. Jones & M.A. Clem.) M.A. E À13.5 Clem. & D.L. Jones A Dockrillia linguiformis (Sw.) Brieger E À11.9 [27], À15.5 4 [27] A Dockrillia mortii (F.Muell.) Rauschert E À16.6 A Dockrillia nugentii (F.M.
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