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CAM Evolution in Bromeliads: Resolving Patterns of Ecological Opportunity, Speciation and Niche Conservatism

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CAM Evolution in Bromeliads: Resolving Patterns of Ecological Opportunity, Speciation and Niche Conservatism C4–CAM–2013: August 6–10, 2013 Champaign–Urbana, Illinois, U.S.A. CAM evolution in bromeliads: resolving patterns of ecological opportunity, speciation and niche conservatism J. Andrew C. Smith Department of Plant Sciences, University of Oxford, U.K. in collaboration with: Klaus Winter (STRI, Panama) Darren Crayn, Katharina Schulte (Cairns, Australia) Daniele Silvestro, Georg Zizka (Frankfurt, Germany) Steven Heathcote, Nick Brown and Yadvinder Malhi (Oxford) with financial support from the Smithsonian Institution and NERC (postgraduate studentship to S.H.) Families containing species capable of CAM Major families Minor families Rubiaceae Talinaceae Polypodiaceae Aizoaceae Vitaceae Vittariaceae Apocynaceae Zamiaceae Asparagaceae Welwitschiaceae Bromeliaceae Anacampserotaceae Aquatic plants Cactaceae Araceae Isoetaceae Crassulaceae Asteraceae Alismataceae Didiereaceae Clusiaceae Apiaceae Commelinaceae Euphorbiaceae Crassulaceae Cucurbitaceae Orchidaceae Hydrocharitaceae Geraniaceae Xanthorrhoeaceae Plantaginaceae Gesneriaceae Lamiaceae Montiaceae Oxalidaceae Total = 36 families Passifloraceae Terminology after Piperaceae APG III (2009) Portulacaceae ≈ 17 000 species CAM photosynthesis and succulence in the semi-desert biome Cactaceae and Ferocactus acanthodes Agavoideae (Asparagaceae) Agave deserti Sonoran Desert, California Mammillaria sp. Opuntia bigelovii The forest canopy: a highly stratified and heterogeneous ecological niche for epiphytes CAM in the forest canopy: tropical epiphytes – Bromeliaceae and Orchidaceae CAM in the forest canopy: tropical epiphytes – Bromeliaceae and Orchidaceae Coutinho, L.M. (1963) Boletim no. 288, Faculdade de Filosofia, Ciências e Letra de Universidade de São Paulo, Botânica, 20, 81–98. Coutinho, L.M. (1969) Boletim no. 331, Faculdade de Filosofia, Ciências e Letra de Universidade de São Paulo, Botânica, 24, 77–102. Distribution of carbon-isotope ratios in Bromeliaceae with Klaus Winter and Darren Crayn 45 40 Bromeliaceae A (1873 spp.) 35 30 25 20 15 10 C3 CAM Number Number of species 5 0 4540 35 30 25 20 15 10 5 40 Bromelioideae13C (‰) B (498 spp.) 35 30 25 20 15 10 5 0 45 40 Pitcairnioideae C (586 spp.) 35 Number of species of Number 30 25 20 15 10 5 0 45 40 Tillandsioideae D 35 (789 spp.) 30 25 20 15 10 5 0 Š 40 Š3535 Š3030 Š2525 Š2020 Š1515 Š1010 Š 5 13C13 C(‰ (ä)) Main topics ● Bromeliaceae as a study-group: biogeography and ecophysiology ● Phylogenetic approaches to understanding the origins of CAM ● Niche partitioning and the adaptive significance of CAM in bromeliads ● Photosynthetic plasticity and the significance of C3 – CAM intermediates ● Future prospects for understanding the evolution of CAM Neotropical family Bromeliaceae (~ 3200 spp.) P Tillandsia Hechtia Life-forms in Bromeliaceae After: Schimper (1888); Mez (1904); Tietze (1906); Pittendrigh (1948); Benzing (1990) Type I Type II Type III Type IV Ananas comosus Bromelia serra Aechmea fasciata Tillandsia recurvata 1. Roots: Soil Soil + tank Mechanical Mechanical 2. Tank: Lacking Rudimentary Prominent Lacking 3. Trichomes: Simple Rel. simple Absorbent, Absorbent, leaf bases covering shoot Life-forms in Bromeliaceae After: Schimper (1888); Mez (1904); Tietze (1906); Pittendrigh (1948); Benzing (1990) TypeTERRESTRIAL I Type II Type III EPIPHYTIC Type IV Ananas comosus Bromelia serra Aechmea fasciata Tillandsia recurvata 1. Roots: Soil Soil + tank Mechanical Mechanical 2. Tank: Lacking Rudimentary Prominent Lacking 3. Trichomes: Simple Rel. simple Absorbent, Absorbent, leaf bases covering shoot Biogeographic regions of bromeliads deduced from species presence–absence data (S. Heathcote) . Based on 31 239 georeferenced herbarium specimens to give presence–absence data for 2° grid cells . Distance matrix constructed using β-similarity index (Kreft & Jetz, 2010) . Regions delimited using non- hierarchical k-means clustering (Hammer et al., 2001) Biogeographic regions of bromeliads deduced from species presence–absence data (S. Heathcote) . Based on 31 239 georeferenced herbarium specimens to give presence–absence data for 2° grid cells . Distance matrix constructed using β-similarity index (Kreft & Jetz, 2010) . Regions delimited using non- hierarchical k-means clustering (Hammer et al., 2001) Biogeographic realms of bromeliads deduced from species presence–absence data Guiana Shield many early-diverging lineages and endemics e.g. Brocchinia Lindmania Connellia Cottendorfia Navia Brewcaria Biogeographic realms of bromeliads deduced from species presence–absence data Northern South America Pitcairnia (C3) Many epiphytic Tillandsioideae (both C3 and CAM), including early-diverging lineages (Glomeropitcairnia and Catopsis) Terrestrial and epiphytic Bromelioideae (CAM) Biogeographic realms of bromeliads deduced from species presence–absence data Central America Hechtia Large number of Tillandsioideae and Bromelioideae (both C3 and CAM) incl. endemic Bromelioideae Androlepis Hohenbergiopsis Ursulaea Biogeographic realms of bromeliads deduced from species presence–absence data Caribbean many epiphytic Tillandsioideae, especially ‘atmospherics’ (CAM) Terrestrial and epiphytic Bromelioideae (CAM) Biogeographic realms of bromeliads deduced from species presence–absence data North America relatively few species, epiphytic Tillandsioideae (CAM) Biogeographic realms of bromeliads deduced from species presence–absence data Andes and Amazon basin many representatives of: Pitcairnioideae (C3) Puyoideae (C3 and CAM) Tillandsioideae (C3 and CAM) Biogeographic realms of bromeliads deduced from species presence–absence data Chile North: drought-tolerant Puya and Tillandsia South: notable for early- diverging lineages of: Puyoideae (Puya spp.) Bromelioideae Greigia Fascicularia Ochagavia Biogeographic realms of bromeliads deduced from species presence–absence data CAM Pitcairnioideae the ‘Dyckia’ clade: Deuterocohnia Dyckia Encholirium ‘Pleistocenic Dry Arc’ many Bromelioideae (CAM), esp. terrestrial Biogeographic realms of bromeliads deduced from species presence–absence data Atlantic Forest many terrestrial and epiphytic Bromelioideae (CAM) CAM to C3 transition along a climatic gradient in the bromeliad flora of Trinidad 100 % CAM 8 % CAM After Griffiths & Smith (1983) Distribution of carbon-isotope ratios in Bromeliaceae with Klaus Winter and Darren Crayn 45 40 Bromeliaceae A (1873 spp.) 35 30 25 20 15 10 C3 CAM Number Number of species 5 0 4540 35 30 25 20 15 10 5 40 Bromelioideae13C (‰) B (498 spp.) 35 30 25 20 15 10 5 0 45 40 Pitcairnioideae C (586 spp.) 35 Number of species of Number 30 25 20 15 10 5 0 45 40 Tillandsioideae D 35 (789 spp.) 30 25 20 15 10 5 0 Š 40 Š3535 Š3030 Š2525 Š2020 Š1515 Š1010 Š 5 13C13 C(‰ (ä)) 18 16 Epiphytes A (667 spp.) 14 12 10 8 6 4 C3 CAM 2 0 18 16 Lithophytes B (202 spp.) 14 12 10 8 6 4 Relative2 abundance of CAM in terrestrial 0 and epiphytic bromeliads 18 16 Terrestrials C (466 spp.) 14 Number of species C CAM 12 3 10 8 6 4 52 % 48 % 2 0 30 Epiphytes + D 25 lithophytes (869 spp.) 20 Number of species Number 15 Number ofNumberspecies 10 5 57 % 43 % 0 –40 –35 –30 –25 –20 –15 –10 –5 1313 CC (‰)(‰) C3 – CAM distribution by genus Phylogenetic niche conservatism (PNC) Majority of genera are either entirely C3 or entirely CAM … … with the exception of Puya and Tillandsia Environmental influences on carbon-isotope ratios . Light intensity . Aridity . Elevation Decreasing Increasing 4545 4040 BromeliaceaeBromeliaceae AA (1873 spp.) (1873(1873 spp.spp.)) 3535 3030 2525 2020 1515 Higher Lower pi /pa pi /pa 1010 C3 CAM C3 55 Number of species 00 454540 35 30 25 20 15 10 5 13 4040 BromelioideaeBromelioideaeδ C (‰)13 C (‰) BB (498(498 spp.spp.)) 3535 3030 2525 2020 1515 1010 55 00 4545 4040 PitcairnioideaePitcairnioideae CC (586(586 spp.spp.)) 3535 Number of species Number of species 3030 Number of species of Number 30 2525 2020 1515 1010 55 00 4545 4040 TillandsioideaeTillandsioideae DD (789(789 spp.spp.)) 3535 (789 spp.) 3030 2525 2020 1515 1010 55 00 ĞĞ 4040 Ğ35Ğ35 Ğ30Ğ30 Ğ25Ğ25 Ğ20Ğ20 Ğ15Ğ15 Ğ10Ğ10 ĞĞ 55 Š 40 Š3535 Š3030 Š2525 Š2020 Š1515 Š1010 Š 5 1313 13C13 CC(‰ (ä)(ä)) Environmental influences on carbon-isotope ratios . Light intensity Kohn (2010) Aridity: . Aridity . Elevation Decreasing Increasing 4545 4040 BromeliaceaeBromeliaceae AA (1873 spp.) (1873(1873 spp.spp.)) 3535 3030 2525 2020 Puya chilensis complex 1515 1010 C3 CAM C3 55 Number of species 00 454540 35 30 25 20 15 with D.10 Silvestro, 5 13 K. Schulte & G. Zizka 4040 BromelioideaeBromelioideaeδ C (‰)13 C (‰) BB MAP (mm) (498(498 spp.spp.)) 3535 3030 2525 2020 1515 1010 55 00 4545 4040 PitcairnioideaePitcairnioideae CC (586(586 spp.spp.)) 3535 Number of species Number of species 3030 Number of species of Number 30 2525 2020 1515 1010 55 00 4545 4040 TillandsioideaeTillandsioideae DD (789(789 spp.spp.)) 3535 (789 spp.) 3030 2525 2020 1515 1010 55 00 ĞĞ 4040 Ğ35Ğ35 Ğ30Ğ30 Ğ25Ğ25 Ğ20Ğ20 Ğ15Ğ15 Ğ10Ğ10 ĞĞ 55 Š 40 Š3535 Š3030 Š2525 Š2020 Š1515 Š1010 Š 5 1313 13C13 CC(‰ (ä)(ä)) Environmental influences on carbon-isotope ratios . Light intensity . Aridity . Elevation Elevation: Decreasing Increasing 4545 −8 −10 4040 BromeliaceaeBromeliaceae AA (1873 spp.) −12 (1873(1873 spp.spp.)) 35 −14 3535 −16 N.S. 3030 −18 (n = 390) −20 2525 −20 −22 2020 −24 ) −26 1515 ‰ −28 C ( −30 1010 C 13 CAM 3 C −32 3 p < 0.001 55 Number of species −34 y = 0.00147x − 28.8 0 −36 (n = 824) 0 −38 0 1000 2000 3000 4000 5000 454540 35 30 25 20 15 10 5 Altitude (m) 13 4040 BromelioideaeBromelioideaeδ C (‰)13 C (‰) BB (498(498 spp.spp.)) 3535 3030 2525 2020 1515 1010 55 00 4545 4040 PitcairnioideaePitcairnioideae
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