Dynamic Carboniferous tropical forests: new views of plant function and potential for physiological forcing of climate

New Phytologist

Volumn 215, Issue 4, 2017, Pages 1333-1353

  Wilson, Jonathan P ^a   Montañez, Isabel P ^b   White, Joseph D ^c   DiMichele, William A ^d   McElwain, Jennifer C ^e   Poulsen, Christopher J ^f   Hren, Michael T ^g  

^a HAVERFORD COLLEGE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BAYLOR UNIVERSITY   (United States)

^d DEPARTMENT OF PALEOBIOLOGY   (United States)

^e UNIVERSITY COLLEGE DUBLIN   (Ireland)

^f UNIVERSITY OF MICHIGAN   (United States)

^g UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Carboniferous; medullosans; paleoclimate; paleophysiology; vegetation climate feedbacks

Indexed keywords

ANGIOSPERM; BIOPHYSICS; CARBONIFEROUS; CLIMATE FEEDBACK; CLIMATE FORCING; ECOSYSTEM MODELING; FOSSIL; GROWTH FORM; INTEGRATED APPROACH; PALEOCLIMATE; PHYSIOLOGY; TRANSPIRATION; TROPICAL FOREST; VEGETATION;

MAGNOLIOPHYTA; TRACHEOPHYTA;

CARBON;

FOREST; METABOLISM; PHYLOGENY; PHYSIOLOGY; PLANT LEAF; PLANT PHYSIOLOGY; PLANT STEM; TROPIC CLIMATE;

CARBON; FORESTS; PHYLOGENY; PLANT LEAVES; PLANT PHYSIOLOGICAL PHENOMENA; PLANT STEMS; TROPICAL CLIMATE;

EID: 85026325411     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.14700     Document Type: Review

References (233)

1. Andrews HN. 1945. Contributions to our knowledge of American Carboniferous Floras. VII. Some pteridosperm stems from Iowa. Annals of the Missouri Botanical Garden 32: 323–360.
2. Auge RM, Green CD, Stodola AJ, Saxton AM, Olinick JB, Evans RM. 2000. Correlations of stomatal conductance with hydraulic and chemical factors in several deciduous tree species in a natural habitat. New Phytologist 145: 483–500.
3. 2 barometer: implications for the early Cenozoic atmosphere. Earth and Planetary Science Letters 439: 158–171.
4. Bashforth AR, Cleal CJ, Gibling MR, Falcon-Lang HJ, Miller RF. 2014. Paleoecology of early Pennsylvanian vegetation on a seasonally dry tropical landscape (Tynemouth Creek Formation, New Brunswick, Canada). Review of Palaeobotany and Palynology 200: 229–263.
5. Bashforth AR, DiMichele WA, Eble CF, Nelson WJ. 2016a. A Middle Pennsylvanian macrofloral assemblage from wetland deposits in Indiana (Illinois Basin): a taxonomic contribution with biostratigraphic, paleobiogeographic, and paleoecologic implications. Journal of Paleontology 90: 589–631.
6. Bashforth AR, DiMichele WA, Eble CF, Nelson WJ. 2016b. Dryland vegetation from the Middle Pennsylvanian of Indiana (Illinois Basin): the dryland biome in glacioeustatic, paleobiogeographic, and paleoecologic context. Journal of Paleontology 90: 785–814.
7. Bashforth AR, Zodrow EL. 2007. Partial reconstruction and palaeoecology of Sphenophyllum costae (Middle Pennsylvanian, Nova Scotia, Canada). Bulletin of Geosciences 82: 365–382.
8. Bateman RM, Hilton J. 2009. Palaeobotanical systematics for the phylogenetic age: applying organspecies, form-species and phylogenetic species concepts in a framework of reconstructed fossil and extant whole-plants. Taxon 58: 1254–1280.
9. Batenburg LH. 1981. Vegetative anatomy and ecology of Sphenophyllum zwickaviense, S. emarginatum, and other “compression species” of Sphenophyllum. Review of Palaeobotany and Palynology 32: 275–313.
10. 2 levels during the Permo-Carboniferous glaciation inferred from fossil lycopsids. Proceedings of the National Academy of Sciences, USA 99: 12567–12571.
11. 2 event on the terrestrial carbon cycle. Proceedings of the National Academy of Sciences, USA 97: 12428–12432.
12. 2 ratios in the Permo-Carboniferous atmosphere. Geochimica Cosmochimica Acta 66: 3757–3769.
13. 2 signal from fossil stomata. New Phytologist 153: 387–397.
14. Bergman NM, Lenton TM, Watson AJ. 2004. COPSE: a new model of biogeochemical cycling over Phanerozoic time. American Journal of Science 304: 397–437.
15. Berner RA. 2009. Phanerozoic atmospheric oxygen: new results using the GEOCARBSULF model. American Journal of Science 309: 603–606.
16. Betts RA, Boucher O, Collins M, Cox PM, Falloon PD, Gedney N, Hemming DL, Huntingford C, Jones CD, Sexton DMH et al. 2007. Projected increase in continental runoff due to plan responses to increasing carbon dioxide. Nature 448: 1037–1041.
17. 2. Proceedings of the National Academy of Sciences, USA 108: 4041–4046.
18. Bota J, Medrano H, Flexas J. 2004. Is photosynthesis limited by decreased Rubisco activity and RuBP content under progressive water stress? New Phytologist 162: 671–681.
19. Boyce CK, Brodribb TJ, Feild TS, Zwieniecki MA. 2009. Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proceedings of the Royal Society B: Biological Sciences 276: 1771–1776.
20. Boyce CK, DiMichele WA. 2016. Arborescent lycophyte productivity and lifespan: constraining the possibilities. Review of Palaeobotany and Palynology 227: 97–110.
21. Boyce CK, Fan Y, Zwieniecki MA. 2017. Did trees grow up to the light, up to the wind, or down to the water? How modern high productivity colors perception of early plant evolution New Phytologist. 215: 552–557.
22. Boyce CK, Knoll AH. 2002. Evolution of developmental potential and the multiple independent origins of leaves in Paleozoic vascular plants. Paleobiology 28: 70–100.
23. Boyce CK, Lee JE. 2010. An exceptional role for flowering plant physiology in the expansion of tropical rainforests and biodiversity. Proceedings of the Royal Society B 277: 3437–3443.
24. Boyce CK, Lee JE, Feild TS, Brodribb TJ, Zwieniecki MA. 2010. Angiosperms helped put the rain in the rainforests: the impact of plant physiological evolution on tropical biodiversity. Annals of the Missouri Botanical Garden 97: 527–540.
25. 2 on terrestrial productivity prior to angiosperm evolution. Proceedings of the National Academy of Sciences, USA 109: 10403–10408.
26. Brodersen C, Jansen S, Choat B, Rico C, Pittermann J. 2014. Cavitation resistance in seedless vascular plants: the structure and function of interconduit pit membranes. Plant Physiology 165: 895–904.
27. Brodribb TJ, Feild TS. 2010. Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecology Letters 13: 175–183.
28. Brodribb TJ, Feild TS, Jordan GJ. 2007. Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 144: 1890–1898.
29. Brodribb TJ, Feild TS, Sack L. 2010. Viewing leaf structure and evolution from a hydraulic perspective. Functional Plant Biology 37: 488–498.
30. Brodribb TJ, McAdam SAM. 2011. Passive origins of stomatal control in vascular plants. Science 331: 582–585.
31. Broutin J, Doubinger J, Farjanel G, Freytet F, Kerp H, Langiaux J, Lebreton ML, Sebban S, Satta S. 1990. Le renouvellement des flores au passage Carbonifére Permien: approches stratigraphique, biologique, sédimentologique. Comptes Rendues 311: 1563–1569.
32. Burleigh JG, Mathews S. 2004. Phylogenetic signal in nucleotide data from seed plants: implications for resolving the seed plant tree of life. American Journal of Botany 91: 1599–1613.
33. Cadotte MW, Cavender-Bares J, Tilman D, Oakley TH. 2009. Using phylogenetic, functional and trait diversity to understand patterns of plant community productivity. PLoS ONE 4: e5695.
34. Campbell GS. 1991. Simulation of water uptake by plant roots. In: Hanks J, Ritchie JT, eds. Modeling plant and soil systems. Madison, WI, USA: American Society of Agronomy, 273–285.
35. Carvalho A, Nabais C, Vieira J, Rossi S, Campelo F. 2015. Plastic response of tracheids in Pinus pinaster in a water-limited environment: adjusting lumen size instead of wall thickness. PLoS ONE 10: e0136305.
36. Cato S, McMillan L, Donaldson L, Richardson T, Echt C, Gardner R. 2006. Wood formation from the base to the crown in Pinus radiata: gradients of tracheid wall thickness, wood density, radial growth rate and gene expression. Plant Molecular Biology 60: 565–581.
37. Cecil CB, DiMichele WA, Elrick SD. 2014. Middle and Late Pennsylvanian cyclothems, American Midcontinent: ice-age environmental changes and terrestrial biotic dynamics. Comptes Rendus Geoscience 346: 159–168.
38. Chaloner WG, Meyen SV. 1973. Carboniferous and Permian floras of the northern continents. In: Hallam A, ed. Atlas of palaeobiogeography. Amsterdam, the Netherlands: Elsevier, 169–186.
39. Chater C, Kamisugi Y, Movahedi M, Fleming A, Cuming AC, Gray JE, Beerling DJ. 2011. Regulatory mechanism controlling stomatal behavior conserved across 400 million years of land plant evolution. Current Biology 21: 1025–1029.
40. Choat B, Brodie TW, Cobb AR, Zwieniecki MA, Holbrook NM. 2006. Direct measurements of intervessel pit membrane hydraulic resistance in two angiosperm tree species. American Journal of Botany 93: 993–1000.
41. Choat B, Cobb AR, Jansen S. 2008. Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function. New Phytologist 177: 608–626.
42. Choat B, Jansen S, Zwieniecki MA, Smets E, Holbrook NM. 2004. Changes in pit membrane porosity due to deflection and stretching: the role of vestured pits. Journal of Experimental Botany 55: 1569–1575.
43. Choat B, Medek DE, Stuart SA, Pasquet-Kok J, Egerton JJG, Salari H, Sack L, Ball MC. 2011. Xylem traits mediate a trade-off between resistance to freeze–thaw-induced embolism and photosynthetic capacity in overwintering evergreens. New Phytologist 191: 996–1005.
44. Choat B, Pittermann J. 2009. New insights into bordered pit structure and cavitation resistance in angiosperms and conifers. New Phytologist 182: 557–560.
45. Cichan MA. 1985. Vascular cambium and wood development in Carboniferous plants. II. Sphenophyllum plurifoliatum Williamson and Scott (Sphenophyllales). Botanical Gazette 146: 395–403.
46. Cichan MA. 1986. Conductance in the wood of selected Carboniferous plants. Paleobiology 12: 302–310.
47. Cleal CJ. 2007. The Westphalian Stephanian macrofloral record from the South Wales Coalfield, UK. Geological Magazine 144: 465–486.
48. Cleal CJ. 2008a. Palaeofloristics of Middle Pennsylvanian lyginopteridaleans in variscan Euramerica. Palaeogeography, Palaeoclimatology, Palaeoecology 261: 1–14.
49. Cleal CJ. 2008b. Palaeofloristics of Middle Pennsylvanian medullosaleans in variscan Euramerica. Palaeogeography, Palaeoclimatology, Palaeoecology 268: 164–180.
50. Cleal CJ, Thomas BA. 2005. Palaeozoic tropical rainforests and their effect on global climates: is the past the key to the present? Geobiology 3: 13–31.
51. Cleal CJ, Uhl D, Cascales-Miñana B, Thomas BA, Bashforth AR, King SC, Zodrow EL. 2012. Plant biodiversity changes in Carboniferous tropical wetlands. Earth-Science Reviews 114: 124–155.
52. Comstock JP, Sperry JS. 2000. Theoretical considerations of optimal conduit length for water transport in vascular plants. New Phytologist 148: 195–218.
53. Dang QL, Cheng S. 2004. Effects of soil temperature on ecophysiological traits in seedlings of four boreal tree species. Forest Ecology and Management 194: 379–387.
54. Danielson JÅ, Johanson U. 2008. Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biology 8: 45.
55. Davies NS, Gibling MR. 2011. Evolution of fixed-channel alluvial plains in response to Carboniferous vegetation. Nature Geoscience 4: 629–633.
56. Day ME. 2000. Influence of temperature and leaf-to-air vapor pressure deficit on net photosynthesis and stomatal conductance in red spruce (Picea rubens). Tree Physiology 20: 57–64.
57. Day TA, Heckathorn SA, DeLucia EH. 1991. Limitations of photosynthesis in Pinus taeda L. (loblolly pine) at low soil temperatures. Plant Physiology 96: 1246–1254.
58. De Micco V, Aronne G, Baas P. 2008. Wood anatomy and hydraulic architecture of stems and twigs of some Mediterranean trees and shrubs along a mesic-xeric gradient. Trees 22: 643–655.
59. De Micco V, Battipaglia G, Balzano A, Cherubini P, Aronne G. 2016. Are wood fibres as sensitive to environmental conditions as vessels in tree rings with intra-annual density fluctuations (IADFs) in Mediterranean species? Trees 30: 971–983.
60. Delevoryas T. 1955. The Medulloasae: structure and relationships. Palaeontographica B 97: 114–167.
61. DeLucia EH, Whitehead D, Clearwater MJ. 2003. The relative limitation of photosynthesis by mesophyll conductance in co-occurring species in a temperate rainforest dominated by the conifer Dacrydium cupressinum. Functional Plant Biology 30: 1197–1204.
62. 13C discrimination and implications for studies of past and future climate. Proceedings of the National Academy of Sciences, USA 107: 5738–5743.
63. DiMichele WA. 2014. Wetland-dryland vegetational dynamics in the Pennsylvanian ice age tropics. Internationakl Journal of Plant Sciences 175: 123–164.
64. DiMichele WA, Cecil CB, Chaney DS, Elrick SD, Lucas SG, Lupia R, Nelson WJ, Tabor NJ. 2011. Pennsylvanian-Permian vegetational changes in tropical Euramerica. In: Harper JW, ed. Geology of the Pennsylvanian–Permian in the Dunkard Basin. Harrisburg, PA, USA: Field Conference of Pennsylvania Geologists, 60–102.
65. DiMichele WA, Cecil CB, Montañez IP, Falcon-Lang HJ. 2010. Cyclic changes in Pennsylvanian paleoclimate and effects on floristic dynamics in tropical Pangaea. International Journal of Coal Geology 83: 329–344.
66. DiMichele WA, Kerp H, Tabor NJ, Looy CV. 2008. The so-called “Paleophytic-Mesophytic” transition in equatorial Pangea: multiple biomes and vegetational tracking of climate change through geological time. Palaeogeography, Palaeoclimatology, Palaeoecology 268: 152–163.
67. DiMichele WA, Montañez IP, Poulsen CJ, Tabor NJ. 2009. Climate and vegetational regime shifts in the late Paleozoic ice age earth. Geobiology 7: 200–226.
68. DiMichele WA, Phillips TL. 1996. Clades, ecological amplitudes, and ecomorphs: phylogenetic effects and persistence of primitive plant communities in the Pennsylvanian-age tropical wetlands. Palaeogeography, Palaeoclimatology, Palaeoecology 127: 83–105.
69. DiMichele WA, Phillips TL, Nelson WJ. 2002. Place vs. time and vegetational persistence: a comparison of four tropical mires from the Illinois Basin during the height of the Pennsylvanian ice age. International Journal of Coal Geology 50: 43–72.
70. DiMichele WA, Phillips TL, Pfefferkorn HW. 2006. Paleoecology of Late Paleozoic pteridosperms from tropical Euramerica. Journal of the Torrey Botanical Society 133: 83–118.
71. Doi M, Kitagawa Y, Shimazaki KI. 2015. Stomatal blue light response is present in early vascular plants. Plant Physiology 169: 1205–1213.
72. 2 concentration. Tree Physiology 30: 1001–1015.
73. Donaldson LA. 1983. Anatomy of root wood in Araucariaceae and some Podocarpaceae indigenous to New Zealand. New Zealand Journal of Botany 21: 221–227.
74. Doyle JA. 2006. Seed ferns and the origin of angiosperms. Journal of the Torrey Botanical Society 133: 169–209.
75. Doyle JA. 2008. Integrating molecular phylogenetic and paleobotanical evidence on origin of the flower. International Journal of Plant Sciences 169: 816–843.
76. Doyle JA. 2012. Molecular and fossil evidence on the origin of the angiosperms. Annual Review of Earth and Planetary Sciences 40: 301–326.
77. D'Rozario A, Labandeira C, Guo WY, Yao YF, Li CS. 2011. Spatiotemporal extension of the Euramerican Psaronius component community to the Late Permian of Cathaysia: in situ coprolites in a P. housuoensis stem from Yunnan Province, southwest China. Palaeogeography, Palaeoclimatology, Palaeoecology 306: 127–133.
78. Edwards D, Kerp H, Hass H. 1998. Stomata in early land plants: an anatomical and ecophysiological approach. Journal of Experimental Botany 49: 255–278.
79. 2. Frontiers in Plant Science 7: 1253.
80. 2 versus Rubisco deactivation as determinants of the photosynthetic decline of ageing evergreen leaves. Plant, Cell & Environment 29: 2168–2184.
81. Falcon-Lang HJ. 2004. Pennsylvanian tropical rain forests responded to glacial-interglacial rhythms. Geology 32: 689–692.
82. Falcon-Lang HJ. 2005. Small cordaitalean trees in a marine-influenced coastal habitat in the Pennsylvanian Joggins Formation, Nova Scotia. Journal of the Geological Society 162: 485–500.
83. Falcon-Lang HJ. 2015. A calamitalean forest preserved in growth position in the Pennsylvanian coal measures of South Wales: implications for palaeoecology, ontogeny and taphonomy. Review of Palaeobotany and Palynology 214: 51–67.
84. Falcon-Lang HJ, Bashforth AR. 2005. Morphology, anatomy, and upland ecology of large cordaitalean trees from the Middle Pennsylvanian of Newfoundland. Review of Palaeobotany and Palynology 135: 223–243.
85. Falcon-Lang HJ, DiMichele WA. 2010. What happened to the coal forests during Pennsylvanian glacial phases? Palaios 25: 611–617.
86. Falcon-Lang HJ, Heckel PH, DiMichele WA, Blake BM, Easterday CR, Eble CF, Elrick S, Gastaldo RA, Greb SF, Martino RL et al. 2011a. No major stratigraphic gap exists near the Middle-Upper Pennsylvanian (Desmoinesian–Missourian) boundary in North America. Palaios 26: 125–139.
87. Falcon-Lang HJ, Jud NA, Nelson WJ, DiMichele WA, Chaney DS, Lucas SG. 2011b. Pennsylvanian coniferopsid forests in sabkha facies reveal the nature of seasonal tropical biome. Geology 39: 371–374.
88. Falcon-Lang HJ, Nelson WJ, Elrick S, Looy CV, Ames PR, DiMichele WA. 2009. Incised channel fills containing conifers indicate that seasonally dry vegetation dominated Pennsylvanian tropical lowlands. Geology 37: 923–926.
89. Feild TS, Brodribb TJ, Iglesias A, Chatelet DS, Baresch A, Upchurch GR, Gomez B, Mohr BAR, Coiffard C, Kvacek J et al. 2011. Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution. Proceedings of the National Academy of Sciences, USA 108: 8363–8366.
90. Feng G, Mi XC, Bøcher PK, Mao LF, Sandel B, Cao M, Ye WH, Hao ZQ, Gong HD, Zhang YT et al. 2014. Relative roles of local disturbance, current climate and paleoclimate in determining phylogenetic and functional diversity in Chinese forests. Biogeosciences 11: 1361–1370.
91. Fielding CR, Frank TD, Birgenheier LP, Rygel MC, Jones AT, Roberts J. 2008. Stratigraphic imprint of the late Palaeozoic ice age in eastern Australia: a record of alternating glacial and nonglacial climate regime. Journal of the Geological Society, London 165: 129–140.
92. 2: an unappreciated central player in photosynthesis. Plant Science 193: 70–84.
93. 2 effects on stomatal size and density over geologic time. Proceedings of the National Academy of Sciences, USA 106: 10343–10347.
94. 2-forced evolution of plant gas exchange capacity and water-use efficiency over the Phanerozoic. Geobiology 7: 227–236.
95. 2 capped at 1000 ppm over the past 300 million years?” by McElwain J.C. et al. [Palaeogeogr. Palaeoclimatol. Palaeoecol. 441 (2016), 653–658]. Palaeogeography, Palaeoclimatology, Palaeoecology 472: 256–259.
96. 2 concentration for the Phanerozoic. Geophysical Research Letters 41: 4685–4694.
97. Friis EM, Crane PR, Pedersen KR, Stampanoni M, Marone F. 2015. Exceptional preservation of tiny embryos documents seed dormancy in early angiosperms. Nature 528: 551–554.
98. Galmé J, Medrano H, Flexas J. 2007. Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. New Phytologist 175: 81–93.
99. Gastaldo RA. 1992. Regenerative growth in fossil horsetails following burial by alluvium. Historical Biology 6: 203–219.
100. Gedney N, Cox PM, Betts RA, Boucher O, Huntingford C, Scott PA. 2006. Detection of a direct carbon dioxide effect in continental river runoff records. Nature 439: 853–858.
101. Giesen P, Berry CM. 2013. Reconstruction and growth of the early tree Calamophyton (Pseudosporochnales, Cladoxylopsida) based on exceptionally complete specimens from Lindlar, Germany (Mid-Devonian): organic connection of Calamophyton branches and Duisbergia trunks. International Journal of Plant Sciences 174: 665–686.
102. Glasspool IJ, Scott AC. 2010. Phanerozoic concentrations of atmospheric oxygen reconstructed from sedimentary charcoal. Nature Geoscience 3: 627–630.
103. Green WA. 2010. The function of the aerenchyma in arborescent lycophytes: evidence of an unfamiliar metabolic strategy. Proceedings of the Royal Society of London B: Biological Sciences 277: 2257–2267.
104. Greguss P. 1968. Xylotomy of the living cycads. Budapest, Hungary: Akademiai Kiado.
105. Hacke UG, Jansen S. 2009. Embolism resistance of three boreal conifer species varies with pit structure. New Phytologist 182: 675–686.
106. Hacke UG, Sperry JS, Pittermann J. 2004. Analysis of circular bordered pit function – II. Gymnosperm tracheids with torus-margo pit membranes. American Journal of Botany 91: 386–400.
107. Hao S, Xue J, Guo D, Wang D. 2010. Earliest rooting system and root: shoot ratio from a new Zosterophyllum plant. New Phytologist 185: 217–225.
108. Heavens NG, Mahowald NM, Soreghan GS, Soreghan MJ, Shields CA. 2012. Glacial- interglacial variability in tropical Pangaean precipitation during the late Paleozoic ice age: simulations with the Community Climate System Model. Climate of the Past Discussion 8: 1915–1972.
109. Heavens NG, Mahowald NM, Soreghan GS, Soreghan MJ, Shields CA. 2015. A model-based evaluation of tropical climate in Pangaea during the late Palaeozoic icehouse. Palaeogeography, Palaeoclimatology, Palaeoecology 425: 109–127.
110. Hernandez-Castillo GR, Stockey RA, Rothwell GW, Mapes G. 2009. Reconstructing Emporia lockardii (Voltziales: Emporiaceae) and initial thoughts on Paleozoic conifer ecology. International Journal of Plant Sciences 170: 1056–1074.
111. 2 enrichment. New Phytologist 162: 387–396.
112. Hetherington AJ, Berry CM, Dolan L. 2016. Networks of highly branched stigmarian rootlets developed on the first giant trees. Proceedings of the National Academy of Sciences, USA 113: 6695–6700.
113. Hetherington AJ, Dolan L. 2017. The evolution of lycopsid rooting structures: conservatism and disparity. New Phytologist. 215: 538–544.
114. Hetherington AM, Woodward FI. 2003. The role of stomata in sensing and driving environmental change. Nature 424: 901–908.
115. Hilton J, Cleal CJ. 2007. The relationship between Euramerican and Cathaysian tropical floras in the Late Palaeozoic: palaeobiogeographical and palaeogeographical implications. Earth-Science Reviews 85: 85–116.
116. Holbrook NM. 1995. Stem water storage. In: Gardner BL, ed. Plant stems: physiology and functional morphology. San Diego, CA, USA: Academic Press, 151–169.
117. Holmes J, Galtier J. 1976. Twin shoots borne on a Botryopteris frond from the British Upper Carboniferous. Review of Palaeobotany and Palynology 22: 207–224.
118. van den Honert TH. 1948. Water transport in plants as a catenary process. Discussions of the Faraday Society 3: 146–153.
119. van Hoof TB, Falcon-Lang HJ, Hartkopf-Fröder C, Kerp H. 2013. Conifer-dominated palynofloras in the Middle Pennsylvanian strata of the De Lutte-6 borehole, The Netherlands: implications for evolution, palaeoecology and biostratigraphy. Review of Palaeobotany and Palynology 188: 18–37.
120. Horton DE, Poulsen CJ. 2009. Paradox of late Paleozoic glacioeustasy. Geology 37: 715–718.
121. Horton DE, Poulsen CJ, Montañez IP, DiMichele WA. 2012. Eccentricity-paced late Paleozoic climate change. Palaeogeography, Palaeoclimatology, Palaeoecology 331: 150–161.
122. Horton DE, Poulsen CJ, Pollard D. 2010. Influence of high-latitude vegetation feedbacks on late Palaeozoic glacial cycles. Nature Geoscience 3: 572–577.
123. Hren MT, Pagani M, Erwin DM, Brandon M. 2010. Biomarker reconstruction of the early Eocene paleotopography and paleoclimate of the northern Sierra Nevada. Geology 38: 7–10.
124. Hueber FM, Galtier J. 2002. Symplocopteris wyattii n. gen. et n. sp.: a zygopterid fern with a false trunk from the Tournaisian (Lower Carboniferous) of Queensland, Australia. Review of Palaeobotany and Palynology 119: 241–273.
125. Jansen S, Choat B, Pletsers A. 2009. Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms. American Journal of Botany 96: 409–419.
126. Jansen S, Sano Y, Choat B, Rabaey D, Lens F, Dute RR. 2007. Pit membranes in tracheary elements of Rosaceae and related families: new records of tori and pseudotori. American Journal of Botany 94: 503–514.
127. Johnson DM, McCulloh KA, Meinzer FC, Woodruff DR, Eissenstat DM. 2011. Hydraulic patterns and safety margins, from stem to stomata, in three eastern US tree species. Tree Physiology 31: 659–668.
128. 2. Journal of Theoretical Biology 253: 638–658.
129. Köppen W. 1936. Das Geographisches System der Klimate. In: Köppen W, Geiger R, eds. Handbuch der Klimatologie v. 1, pt C. Berlin, Germany: Gebrüder, 1–46.
130. Lancashire JR, Ennos AR. 2002. Modelling the hydrodynamic resistance of bordered pits. Journal of Experimental Botany 53: 1485–1493.
131. Laveine J-P. 1986. The size of the frond in the genus Alethopteris Sternberg (Pteridospermopsida, Carboniferous). Geobios 19: 49–59.
132. Lee JE, Oliveira RS, Dawson TE, Fung I. 2005. Root functioning modifies seasonal climate. Proceedings of the National Academy of Sciences, USA 102: 17576–17581.
133. LePage BA, Beauchamp B, Pfefferkorn HW. 2003. Late early Permian plant fossils from the Canadian high Arctic: a rare paleoenvironmental/climatic window into northwest Pangea. Palaeogeography, Palaeoclimatology, Palaeoecology 191: 345–372.
134. Loreto F, Centritto M, Chartzoulakis K. 2003. Photosynthetic limitations in olive cultivars with different sensitivity to salt stress. Plant, Cell & Environment 26: 595–601.
135. 2 flux by three different methods. Plant Physiology 98: 1437–1443.
136. Maire V, Wright IJ, Prentice IC, Batjes NH, Bhaskar R, van Bodegom PM, Cornwell WK, Ellsworth D, Niinemets Ü, Ordonez A et al. 2015. Global effects of soil and climate on leaf photosynthetic traits and rates. Global Ecology and Biogeography 24: 706–717.
137. Manzoni S, Vico G, Katul G, Palmroth S, Jackson RB, Porporato A. 2013. Hydraulic limits on maximum plant transpiration and the emergence of the safety–efficiency trade-off. New Phytologist 198: 169–178.
138. Masselter T, Rowe NP, Speck T. 2007. Biomechanical reconstruction of the carboniferous seed fern Lyginopteris oldhamia: implications for growth form reconstruction and habit. International Journal of Plant Sciences 168: 1177–1189.
139. Matsunaga KK, Tomescu AM. 2016. Root evolution at the base of the lycophyte clade – insights from an Early Devonian lycophyte. Annals of Botany 117: 585–598.
140. McAdam SAM, Brodribb TJ. 2012. Stomatal innovation and the rise of seed plants. Ecology Letters 15: 1–8.
141. McAdam SAM, Brodribb TJ, Ross JJ. 2016. Shoot-derived abscisic acid promotes root growth. Plant, Cell & Environment 39: 652–659.
142. McCulloh KA, Sperry JS, AdlerO FR. 2004. Murray's law and the hydraulic vs mechanical functioning of wood. Functional Ecology 18: 931–938.
143. 2 concentration in the geological past? Philosophical Transactions of the Royal Society of London Series B 353: 83–95.
144. McElwain JC, Chaloner WG. 1995. Stomatal density and index of fossil plants track atmospheric carbon dioxide in the Palaeozoic. Annals of Botany 76: 389–395.
145. 2 capped at 1000 ppm over the past 300 million years? Palaeogeography, Palaeoclimatology, Palaeoecology 441: 653–658.
146. 2 capped at 1000 ppm over the past 300 million years?” [Palaeogeogr. Palaeoclimatol. Palaeoecol. 441 (2016) 653–658]. Palaeogeography, Palaeoclimatology, Palaeoecology 472: 260–263.
147. McElwain JC, Yiotis C, Lawson T. 2016b. Using modern plant trait relationships between observed and theoretical maximum stomatal conductance and vein density to examine patterns of plant macroevolution. New Phytologist 209: 94–103.
148. Meyen SV. 1982. Carboniferous and Permian floras of Angaraland (a synthesis). Biological Memoirs. Lucknow, India: International Publishers.
149. Meyen SV. 1997. Permian conifers of Western Angaraland. Review of Palaeobotany and Palynology 96: 351–447.
150. Montañez IP. 2016. A Late Paleozoic climate window of opportunity. Proceedings of the National Academy of Sciences, USA 113: 2334–2336.
151. 2 and terrestrial carbon cycle linkages during Late Palaeozoic glacial-interglacial cycles. Nature Geoscience 9: 824–828.
152. Montañez IP, Poulsen CJ. 2013. The Late Paleozoic Ice Age: an evolving paradigm. Annual Reviews in Earth and Planetary Sciences 41: 629–656.
153. 2-forced climate instability and linkages to tropical vegetation during Late Paleozoic deglaciation. Science 315: 87–91.
154. Moore LC, Wittry J, DiMichele WA. 2014. The Okmulgee, Oklahoma fossil flora, a Mazon Creek equivalent: spatial conservatism in the composition of Middle Pennsylvanian wetland vegetation over 1100 km. Review of Palaeobotany and Palynology 200: 24–52.
155. Morillon R, Chrispeels MJ. 2001. The role of ABA and the transpiration stream in the regulation of the osmotic water permeability of leaf cells. Proceedings of the National Academy of Sciences, USA 98: 14138–14143.
156. Morris JL, Leake JR, Stein WE, Berry CM, Marshall JE, Wellman CH, Milton JA, Hillier S, Mannolini F, Quirk J et al. 2015. Investigating Devonian trees as geo-engineers of past climates: linking palaeosols to palaeobotany and experimental geobiology. Palaeontology 58: 787–801.
157. Nelsen MP, DiMichele WA, Peters SE, Boyce CK. 2016. Delayed fungal evolution did not cause the Paleozoic peak in coal production. Proceedings of the National Academy of Sciences, USA 113: 2442–2447.
158. Niinemets Ü. 1999. Components of leaf dry mass per area–thickness and density–alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytologist 144: 35–47.
159. Niinemets Ü, Díaz-Espejo A, Flexas J, Galmés J, Warren CR. 2009. Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field. Journal of Experimental Botany 60: 2249–2270.
160. Noblin X, Mahadevan L, Coomaraswamy IA, Weitz DA, Holbrook NM, Zwieniecki MA. 2008. Optimal vein density in artificial and real leaves. Proceedings of the National Academy of Sciences, USA 105: 9140–9144.
161. Nugent KA, Matthews HD. 2012. Drivers of future northern latitude runoff change. Atmosphere-Ocean 50: 197–206.
162. Ogle K, Wolpert RL, Reynolds JF. 2004. Reconstructing plant root area and water uptake profiles. Ecology 85: 1967–1978.
163. Opluštil S, Šimůnek Z, Zajíc J, Mencl V. 2013. Climatic and biotic changes around the Carboniferous/Permian boundary recorded in the continental basins of the Czech Republic. International Journal of Coal Geology 119: 114–151.
164. Pfefferkorn HW, Gillespie WH, Resnick DA, Scheihing MH. 1984. Reconstruction and architecture of medullosan pteridosperms (Pennsylvanian). The Mosasaur (Delaware Valley Paleontological Society) 2: 1–8.
165. Pfefferkorn HW, Thomson MC. 1982. Changes in dominance patterns in Upper Carboniferous plant-fossil assemblages. Geology 10: 641–644.
166. Phillips TL. 1979. Reproduction of heterosporous arborescent lycopods in the Mississippian—Pennsylvanian of Euramerica. Review of Palaeobotany and Palynology 27: 239–289.
167. Phillips TL, DiMichele WA. 1992. Comparative ecology and life-history biology of arborescent lycophytes in Late Carboniferous swamps of Euramerica. Annals of the Missouri Botanical Garden 79: 560–588.
168. Phillips TL, Peppers RA. 1984. Changing patterns of Pennsylvanian coal-swamp vegetation and implications of climatic control on coal occurrence. International Journal of Coal Geology 3: 205–255.
169. Phillips TL, Peppers RA, Avcin MJ, Laughnan PF. 1974. Fossil plants and coal – patterns of change in Pennsylvanian coal swamps of Illinois Basin. Science 184: 1367–1369.
170. Phillips TL, Peppers RA, DiMichele WA. 1985. Stratigraphic and interregional changes in Pennsylvanian coal-swamp vegetation: environmental inferences. International Journal of Coal Geology 5: 43–109.
171. 2 concentrations. Plant, Cell & Environment 19: 182–190.
172. Pittermann J, Choat B, Jansen S, Stuart SA, Lynn L, Dawson TE. 2010. The relationships between xylem safety and hydraulic efficiency in the Cupressaceae: the evolution of pit membrane form and function. Plant Physiology 153: 1919–1931.
173. Plotnick RE, Kenig F, Scott AC, Glasspool IJ, Eble CF, Lang WJ. 2009. Pennsylvanian paleokarst and cave fills from northern Illinois, USA: a window into late Carboniferous environments and landscapes. Palaios 24: 627–637.
174. Poulsen CJ, Pollard D, Montañez IP, Rowley D. 2007. Late Paleozoic tropical climate response to Gondwanan deglaciation. Geology 35: 771–774.
175. Poulsen CJ, Tabor C, White JD. 2015. Long-term climate forcing by atmospheric oxygen concentrations. Science 348: 1238–1241.
176. Prado K, Maurel C. 2013. Regulation of leaf hydraulics: from molecular to whole plant levels. Frontiers in Plant Science 4: 255.
177. Pratt RB, Jacobsen AL, Ewers FW, Davis SD. 2007. Relationships among xylem transport, biomechanics and storage in stems and roots of nine Rhamnaceae species of the California chaparral. New Phytologist 174: 787–798.
178. Pryer KM, Schuettpelz E, Wolf PG, Schneider H, Smith AR, Cranfill R. 2004. Phylogeny and evolution of ferns (monilophytes) with a focus on the early leptosporangiate divergences. American Journal of Botany 91: 1582–1598.
179. Qiu Y-L, Lee J, Bernasconi-Quadroni F, Soltis DE, Soltis PS, Zanis M, Zimmer EA, Chen Z, Savolainen V, Chase MW. 1999. The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402: 404–407.
180. Ramírez M, Rodríguez J, Peredo M, Valenzuela S, Mendonça R. 2009. Wood anatomy and biometric parameters variation of Eucalyptus globulus clones. Wood Science and Technology 43: 131–141.
181. Rathgeber CB, Decoux V, Leban JM. 2006. Linking intra-tree-ring wood density variations and tracheid anatomical characteristics in Douglas fir (Pseudotsuga menziesii (Mirb.) Franco). Annals of Forest Science 63: 699–706.
182. Raven JA. 1998. Into the voids: the distribution, function, development and maintenance of gas spaces in plants. Annals of Botany 78: 137–142.
183. Raymond A, Costanza S. 2007. Are wind-pollinated groups less diverse and longer ranging than insect-pollinated groups? Geological Society of America Abstracts with Programs 39: 565.
184. Raymond A, Lambert L, Costanza S, Slone EJ, Cutlip PC. 2010. Cordaiteans in paleotropical wetlands: an ecological re-evaluation. International Journal of Coal Geology 83: 248–265.
185. Raymond A, Wehner M, Costanza SH. 2014. Permineralized Alethopteris ambigua (Lesquereux) white: a medullosan with relatively long-lived leaves, adapted for sunny habitats in mires and floodplains. Review of Palaeobotany and Palynology 200: 82–96.
186. Ricardi-Branco F, Sampaio Costa J, Cristiano de Souza IC, Ronh R, Longhim M, Faria RS. 2013. Bryophytes associated with Pennsylvanian periglacial environments of the southern Gondwana (Sao Paulo State, Itarare Group, Parana Basin) – Brazil. Bulletin of the New Mexico Museum of Natural History and Science 60: 343–347.
187. Rößler R. 2000. The late Palaeozoic tree fern Psaronius—an ecosystem unto itself. Review of Palaeobotany and Palynology 108: 55–74.
188. Rothwell GW, Mapes G, Mapes RH. 1997. Late Paleozoic conifers of North America: structure, diversity and occurrences. Review of Palaeobotany and Palynology 95: 95–113.
189. Rothwell GW, Warner S. 1984. Cordaixylon dumusum n. sp. (Cordaitales). I. Vegetative structures. Botanical Gazette 145: 275–291.
190. Rowe NP, Speck T. 1998. Biomechanics of plant growth forms: the trouble with fossil plants. Review of Palaeobotany and Palynology 102: 43–62.
191. Rowe NP, Speck T, Galtier J. 1993. Biomechanical analysis of a Paleozoic gymnosperm stem. Proceedings of the Royal Society of London Series B 252: 19–28.
192. Sachse D, Billault I, Bowen GJ, Chikaraishi Y, Dawson TE, Feakins SJ, Freeman KH, Magill CR, McInerney FA, van der Meer MTJ et al. 2012. Molecular paleohydrology: Interpreting the hydrogen-isotopic composition of lipid biomarkers from photosynthesizing organisms. Annual Reviews of Earth Planetary Science Letters 40: 221–249.
193. Sack L, Holbrook NM. 2006. Leaf hydraulics. Annual Review of Plant Biology 57: 361–381.
194. 2 physiological forcing in shaping future daily-scale precipitation. Journal of Climatology 30: 2319–2340.
195. Soreghan GS, Sweet DE, Heavens NG. 2014. Upland glaciation in tropical Pangaea: geologic evidence and implications for late Paleozoic climate modeling. Journal of Geology 122: 137–163.
196. Soria A, Meyer-Berthaud B. 2004. Tree fern growth strategy in the Late Devonian cladoxylopsid species Pietzschia levis from the study of its stem and root system. American Journal of Botany 91: 10–23.
197. Spatz HC, Rowe N, Speck T, Daviero V. 1998. Biomechanics of hollow stemmed sphenopsids: II. Calamites – to have or not to have secondary xylem. Review of Palaeobotany and Palynology 102: 63–77.
198. Sperry JS, Hacke UG. 2004. Analysis of circular bordered pit function – I. Angiosperm vessels with homogenous pit membranes. American Journal of Botany 91: 369–385.
199. Sperry JS, Hacke UG, Oren R, Comstock JP. 2002. Water deficits and hydraulic limits to leaf water supply. Plant, Cell & Environment 25: 251–263.
200. Steidtmann WE. 1944. The anatomy and affinities of Medullosa noei Steidtmann, and associated foliage, roots, and seeds. Contributions from the Museum of Paleontology University of Michigan 6: 131–166.
201. 2 concentrations and perturbations in the hydrological cycle via drop in plant transpiration. Geology 40: 815–818.
202. Strullu-Derrien C, Kenrick P, Tafforeau P, Cochard H, Bonnemain J-L, Le Hérissé A, Lardeux H, Badel E. 2014. The earliest wood and its hydraulic properties documented in c. 407-million-year-old fossils using synchrotron microtomography. Botanical Journal of the Linnean Society 175: 423–437.
203. Sun Q, Rost TL, Matthews MA. 2006. Pruning-induced tylose development in stems of current-year shoots of Vitis vinifera (Vitaceae). American Journal of Botany 93: 1567–1576.
204. Swann ALS, Fung IY, Chiang JCH. 2012. Mid-latitude afforestation shifts general circulation and tropical precipitation. Proceedings of the National Academy of Sciences, USA 109: 712–716.
205. Tabor NJ, DiMichele WA, Montañez IP, Chaney DS. 2013. Late Paleozoic continental warming of a cold tropical basin and floristic change in western Pangea. International Journal of Coal Geology 119: 177–186.
206. Taylor EL, Taylor TN, Krings M. 2009. Paleobotany: the biology and evolution of fossil plants, 2nd edn. New York, USA: Academic Press.
207. 2 diffusion. Plant Physiology 156: 90–105.
208. Thomas BA. 2014. In situ stems: preservation states and growth habits of the Pennsylvanian (Carboniferous) calamitaleans based upon new studies of Calamites Sternberg, 1820 in the Duckmantian at Brymbo, North Wales, UK. Palaeontology 57: 21–36.
209. Thomas BA, Cleal CJ. 2017. Distinguishing Pennsylvanian-age lowland, extra-basinal and upland vegetation. Palaeobiodiveristy and Palaeoenvironments 97: 1–21.
210. Tidwell WD, Ash SR. 2004. Synopsis of the flora in the Red Tanks Formation, Carrizo Arroyo, New Mexico. New Mexico Museum of Natural History and Science Bulletin 25: 97–103.
211. 2 across species: quantitative limitations and scaling up by models. Journal of Experimental Botany 64: 2269–2281.
212. 2 diffusion as a key trait. New Phytologist 209: 1576–1590.
213. Tyree MT, Ewers FW. 1991. Tansley Review No. 34. The hydraulic architecture of trees and other woody plants. New Phytologist 119: 345–360.
214. Tyree MT, Sperry JS. 1989. Vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Plant Molecular Biology 40: 19–38.
215. Veromann-Jürgenson LL, Tosens T, Laanisto L, Niinemets Ü. 2017. Extremely thick cell walls and low mesophyll conductance: welcome to the world of ancient living!. Journal of Experimental Botany 68: 1639–1653.
216. Wagner RH, Lyons PC. 1997. A critical analysis of the higher Pennsylvanian megafloras of the Appalachian region. Review of Palaeobotany and Palynology 95: 255–283.
217. Walter H. 1985. Vegetation of the earth and ecological systems of the geo-biosphere, 3rd edn. New York, USA: Springer.
218. Wang J, Pfefferkorn HW, Zhang Y, Feng Z. 2012. Permian vegetational Pompeii from Inner Mongolia and its implications for landscape paleoecology and paleobiogeography of Cathaysia. Proceedings of the National Academy of Sciences, USA 109: 4927–4932.
219. Williams JW, Jackson ST. 2007. Novel climates, no-analog communities, and ecological surprises. Frontiers in Ecology and the Environment. 5: 475–482.
220. nd edn. Oxford, UK: Oxford University Press.
221. Wilson JP. 2013. Modeling 400 million years of plant hydraulics. Paleontological Society Papers 19: 175–194.
222. Wilson JP. 2016. Hydraulics of Psilophyton and evolutionary trends in plant water transport after terrestrialization. Review of Palaeobotany and Palynology 227: 65–76.
223. Wilson JP, Fischer WW. 2011. Hydraulics of Asteroxylon mackei, an early Devonian vascular plant, and the early evolution of water transport tissue in terrestrial plants. Geobiology 9: 121–130.
224. Wilson JP, Knoll AH. 2010. A physiologically explicit morphospace for tracheid-based water transport in modern and extinct seed plants. Paleobiology 36: 335–355.
225. Wilson JP, Knoll AH, Holbrook NM, Marshall CR. 2008. Modeling fluid flow in Medullosa, an anatomically unusual Carboniferous seed plant. Paleobiology 34: 472–493.
226. Wilson JP, White JD, DiMichele WA, Hren MT, Poulsen CJ, McElwain JC, Montañez IP. 2015. Reconstructing extinct plant water use for understanding vegetation–climate feedbacks: methods, synthesis, and a case study using the Paleozoic-era medullosan seed ferns. Paleontological Society Papers 21: 167–195.
227. Wnuk C. 1996. The development of floristic provinciality during the Middle and Late Paleozoic. Review of Palaeobotany and Palynology 90: 5–40.
228. 2 from pre-industrial levels. Nature 327: 617–618.
229. Xue J, Deng Z, Huang P, Huang K, Benton MJ, Cui Y, Wang D, Liu J, Shen B, Basinger JF et al. 2016. Belowground rhizomes in paleosols: the hidden half of an Early Devonian vascular plant. Proceedings of the National Academy of Sciences, USA 113: 9451–9456.
230. Zazzaro S. 2006. Plasticity in response to changing light environment for red spruce and balsam fir. Doctoral dissertation, The University of Maine, ME, USA.
231. Zhang Y-J, Meinzer FC, Qi G-H, Goldstein G, Cao KF. 2013. Midday stomatal conductance is more related to stem rather than leaf water status in subtropical deciduous and evergreen broadleaf trees. Plant, Cell & Environment 36: 149–158.
232. Zhou YL, Wang SJ, Hilton J, Tian BL. 2008. Anatomically preserved lepidodendralean plants from lower Permian coal balls of northern China: Achlamydocarpon intermedium sp. nov. Plant Systematics and Evolution 273: 71–85.
233. Zimmermann MH. 1983. Xylem structure and the ascent of sap. Berlin, Germany: Springer-Verlag.