Investigating Devonian trees as geo-engineers of past climates: Linking palaeosols to palaeobotany and experimental geobiology

Palaeontology

Volumn 58, Issue 5, 2015, Pages 787-801

  Morris, Jennifer L ^a   Leake, Jonathan R ^a   Stein, William E ^b   Berry, Christopher M ^c   Marshall, John E A ^d   Wellman, Charles H ^a   Milton, J Andrew ^d   Hillier, Stephen ^e,f   Mannolini, Frank ^g   Quirk, Joe ^a   Beerling, David J ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b BINGHAMTON UNIVERSITY   (United States)

^c CARDIFF UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^e SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^f SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^g NEW YORK STATE MUSEUM   (United States)

Author keywords

Arbuscular mycorrhiza; Climate change; Devonian plant hypothesis; Devonian trees; Land plant evolution; Mineral weathering

Indexed keywords

ARBUSCULAR MYCORRHIZA; CARBON CYCLE; CHEMICAL WEATHERING; CLIMATE VARIATION; DEVONIAN; PALEOBOTANY; PALEOENVIRONMENT; PALEOSOL;

GREENE COUNTY [NEW YORK]; NEW YORK [UNITED STATES]; UNITED STATES;

EMBRYOPHYTA; FUNGI;

EID: 84940103678     PISSN: 00310239     EISSN: 14754983     Source Type: Journal    
DOI: 10.1111/pala.12185     Document Type: Article

References (104)

1. Algeo, T. J. and Scheckler, S. E. 1998. Terrestrial-marine teleconnections in the Devonian: links between the evolution of land plants, weathering processes, and marine anoxic events. Philosophical Transactions of the Royal Society, London B, 353, 113-130.
2. Algeo, T. J., Scheckler, S. E. and Maynard, J. B. 2001. Effects of the Middle to Late Devonian spread of vascular land plants on weathering regimes, marine biotas, and global climate. 213-236. In Gensel, P. G. and Edwards, D. (eds). Plants invade the land: evolutionary and environmental perspectives. Columbia University Press, New York, 304 pp.
3. Andrist-Rangel, Y., Edwards, A. C., Hillier, S. and Öborn, I. 2007. Long-term K dynamics in organic and conventional mixed cropping systems related to management and soil properties. Agriculture, Ecosystems & Environment, 122, 413-426.
4. Beerling, D. J. 2007. The emerald planet: how plants changed Earth's history. Oxford University Press, Oxford, 288 pp.
5. 2. Proceedings of the National Academy of Sciences of the United States of America, 102, 1302-1305.
6. Berbee, M. L. and Taylor, J. W. 1993. Dating the evolutionary radiations of the true fungi. Canadian Journal of Botany, 71, 1114-1127.
7. 2. Science, 276, 544-546.
8. 2. Oxford University Press, New York, 158 pp.
9. 2. Geochimica et Cosmochimica Acta, 70, 5653-5664.
10. 2 over Phanerozoic time. American Journal of Science, 301, 182-204.
11. Berner, R. A., Berner, E. K. and Moulton, K. L. 2003. Plants and mineral weathering: present and past. Treatise on Geochemistry, 5, 169-188.
12. Berry, C. M. and Fairon-Demaret, M. 2002. The architecture of Pseudosporochnus nodosus Leclercq et Banks: a Middle Devonian Cladoxylopsid from Belgium. International Journal of Plant Sciences, 163 (5), 699-713.
13. Bond, D., Wignall, P. B. and Racki, G. 2004. Extent and duration of marine anoxia during the Frasnian-Famennian (Late Devonian) mass extinction in Poland, Germany, Austria and France. Geological Magazine, 141 (2), 173-193.
14. Bonfante, P. and Genre, A. 2008. Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends in Plant Science, 13, 492-498.
15. Bonfante, P. and Genre, A. 2010. Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nature Communications, 1, 48. doi:10.1038/ncomms1046
16. Caputo, M. V. 1985. Late Devonian glaciation in South America. Palaeogeography, Palaeoclimatology, Palaeoecology, 51, 291-317.
17. Cox, J. E., Railsback, L. B. and Gordon, E. A. 2001. Evidence from Catskill pedogenic carbonates for a rapid Late Devonian decrease in atmospheric carbon dioxide concentrations. Northeastern Geology & Environmental Sciences, 23, 91-102.
18. Davies, N. S. and Gibling, M. R. 2010. Paleozoic vegetation and the Siluro-Devonian rise of fluvial lateral accretion sets. Geology, 38, 51-54.
19. Driese, S. G., Mora, C. I., Cotter, E. and Foreman, J. L. 1992. Paleopedology and stable isotope chemistry of Late Silurian vertic paleosols, Bloomsburg Formation, Central Pennsylvania. Journal of Sedimentary Petrology, 62, 825-841.
20. Driese, S. G., Mora, C. I. and Elick, J. M. 1997. Morphology and taphonomy of root and stump casts of the earliest trees (Middle to Late Devonian), Pennsylvania and New York, U.S.A. Palaios, 12, 524-537.
21. Edwards, D. 1994. Towards an understanding of pattern and process in the growth of early vascular plants. 39-59. In Ingram, D. S. (ed.). Shape and form in plants and fungi. Linnean Society, London, 380 pp.
22. Edwards, D. 1996. New insights into early land ecosystems: a glimpse of a Lilliputian world. Review of Palaeobotany & Palynology, 90, 159-174.
23. Edwards, D. and Selden, P. A. 1992. The development of early terrestrial ecosystems. Botanical Journal of Scotland, 46, 337-366.
24. 2). Geology, 26, 143-146.
25. Feakes, C. R. and Retallack, G. J. 1988. Recognition and chemical characterization of fossil soils developed on alluvium; a Late Ordovician example. 35-48. In Reinhardt, J. and Sigleo, W. R. (eds). Paleosols and weathering through geologic time: principles and applications. Geological Society of America Special Paper, 216, 181 pp.
26. 2. New Phytologist, 205, 743-756.
27. Gensel, P. G. and Andrews, H. N. 1984. Plant life in the Devonian. Praeger Publishers, New York, 380 pp.
28. Gibling, M. R. and Davies, N. S. 2012. Palaeozoic landscapes shaped by plant evolution. Nature Geoscience, 5, 99-105.
29. Giesen, P. and Berry, C. M. 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.
30. Hibbett, D. S. and Matheny, B. P. 2009. The relative ages of ectomycorrhizal mushrooms and their plant hosts estimated using Bayesian relaxed molecular clock analyses. BMC Biology, 7, 1-13.
31. Hillier, S. 2006. Formation and alteration of clay materials. 29-71. In Reeves, G. M., Sims, I. and Cripps, J. C. (eds). Clay materials used in construction. Geological Society of London, Engineering Geology Special Publications, 21, 511 pp.
32. Humphreys, C. P., Franks, P. J., Rees, M., Bidartondo, M. I., Leake, J. R. and Beerling, D. 2010. Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants. Nature Communications, 1, 103. doi:10.1038/ncomms1105
33. Joachimski, M. M. and Buggisch, W. 1993. Anoxic events in the late Frasnian - causes of the Frasnian-Famennian faunal crisis? Geology, 21, 675-678.
34. 18O signatures indicate climatic cooling as a trigger of the Late Devonian mass extinction. Geology, 30, 711-714.
35. Joachimski, M. M., Pancost, R. D., Freeman, K. H., Ostertag-Henning, C. and Buggisch, W. 2002. Carbon isotope geochemistry of the Frasnian-Famennian transition. Palaeogeography, Palaeoclimatology, Palaeoecology, 181, 91-109.
36. Jobbágy, E. G. and Jackson, R. B. 2001. The distribution of soil nutrients with depth: global patterns and the imprint of plants. Biogeochemistry, 53, 51-77.
37. Johnson, D., Leake, J. R. and Read, D. J. 2001. Novel in-growth core system enables functional studies of grassland mycorrhizal mycelial networks. New Phytologist, 152, 555-562.
38. Kennedy, M. J., Chadwick, O. A., Vitousek, P. M., Derry, L. A. and Hendricks, D. M. 1998. Changing sources of base cations during ecosystem development, Hawaiian Islands. Geology, 26, 1015-1018.
39. Kennedy, M., Droser, M., Mayer, L. M., Pevear, D. and Mrofka, D. 2006. Late Precambrian oxygenation; inception of the clay mineral factory. Science, 311, 1446-1449.
40. Kennedy, K. L., Gibling, M. R., Eble, C. F., Gastaldo, R. A., Gensel, P. G., Wener-Zwanziger, U. and Wilson, R. A. 2013. Lower Devonian coaly shales of Northern New Brunswick, Canada: plant accumulations in the early stages of terrestrial colonization. Journal of Sedimentary Research, 83, 1202-1215.
41. Kenrick, P. and Strullu-Derrien, C. 2014. The origin and early evolution of roots. Plant Physiology, 166, 570-580.
42. Kerp, H., Hass, H. and Mossbrugger, V. 2001. New data on Nothia aphylla Lyon 1964 ex El-Saadawy et. Lacey 1979, a poorly known plant from the Lower Devonian Rhynie Chert. 52-82. In Gensel, P. G. and Edwards, D. (eds). Plants invade the land: evolutionary and environmental perspectives. Columbia University Press, New York, 304 pp.
43. Koele, N., Dickie, I. A., Blum, J. D., Gleason, J. D. and de Graff, L. 2014. Ecological significance of mineral weathering in ectomycorrhizal and arbuscular mycorrhizal ecosystems from a field-based comparison. Soil Biology & Biochemistry, 69, 63-70.
44. Kraus, M. J. and Hasiotis, S. T. 2006. Significance of different modes of rhizolith preservation to interpreting paleoenvironmental and paleohydrologic settings: examples from Paleogene paleosols, Bighorn Basin, Wyoming, U.S.A. Journal of Sedimentary Research, 76, 633-646.
45. Krings, M., Taylor, T. N., Hass, H., Kerp, H., Dotzler, N. and Hermsen, E. J. 2007. Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytologist, 174, 648-657.
46. Lambers, H., Mougel, C., Jaillard, B. and Hinsinger, P. 2009. Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective. Plant & Soil, 321, 83-115.
47. Leake, J. R., Duran, A. L., Hardy, K. E., Johnson, I., Beerling, D. J., Banwart, S. A. and Smits, M. M. 2008. Biological weathering in soil: the role of symbiotic root-associated fungi biosensing minerals and directing photosynthate-energy into grain-scale mineral weathering. Mineralogical Magazine, 72, 85-89.
48. LePage, B., Currah, R., Stockey, R. and Rothwell, G. 1997. Fossil ectomycorrhizae from the Middle Eocene. American Journal of Botany, 84, 410-412.
49. McElwain, J. C. and Chaloner, W. G. 1995. Stomatal density and index of fossil plants track atmospheric carbon dioxide in the Palaeozoic. Annals of Botany, 76, 389-395.
50. Meyer-Berthaud, B., Scheckler, S. E. and Wendt, J. 1999. Archaeopteris is the earliest known modern tree. Nature, 398, 700-701.
51. Meyer-Berthaud, B., Soria, A. and Decombeix, A.-L. 2010. The land plant cover in the Devonian: a reassessment of the evolution of the tree habit. 59-70. In Vecoli, M., Clément, G. and Meyer-Berthaud, B. (eds). The terrestrialization process: modelling complex interactions at the biosphere-geosphere interface. Geological Society, London, Special Publications, 339, 192 pp.
52. Meyer-Berthaud, B., Decombeix, A.-L. and Ermacora, X. 2013. Archaeopterid root anatomy and architecture: new information from permineralized specimens of Famennian age from Anti-Atlas (Morocco). International Journal of Plant Sciences, 174, 364-381.
53. Mintz, J. S., Driese, S. G. and White, J. D. 2010. Environmental and ecological variability of Middle Devonian (Givetian) forests in Appalachian Basin paleosols, New York, United States. Palaios, 25, 85-96.
54. Mora, C. I. and Driese, S. G. 1999. Palaeoenvironment, palaeoclimate and stable carbon isotopes of Palaeozoic red-bed palaeosols, Appalachian Basin, USA and Canada. Special Publications of the International Association of Sedimentologists, 27, 61-84.
55. Mora, C. I., Driese, S. G. and Seager, P. A. 1991. Carbon dioxide in the Paleozoic atmosphere: evidence from carbon-isotope composition of pedogenic carbonate. Geology, 19, 1017-1020.
56. 2 levels from soil carbonate and organic matter. Science, 271, 1105-1107.
57. Morris, J. L. and Edwards, D. 2014. An analysis of vegetational change in the Lower Devonian: new data from the Lochkovian of the Welsh Borderland, U.K. Review of Palaeobotany & Palynology, 211, 28-54.
58. Murphy, A. E., Sageman, B. B. and Hollander, D. J. 2000. Eutrophication by decoupling of the marine biogeochemical cycles of C, N, and P: a mechanism for the Late Devonian mass extinction. Geology, 28, 427-430.
59. Neaman, A., Chorover, J. and Brantley, S. L. 2005. Element mobility patterns record organic ligands in soils on early Earth. Geology, 33, 117-120.
60. Neaman, A., Chorover, J. and Brantley, S. L. 2006. Effects of organic ligands on granite dissolution in batch experiments at pH 6. American Journal of Science, 306, 451-473.
61. Omotoso, O., McCarty, D. K., Hillier, S. and Kleeberg, R. 2006. Some successful approaches to quantitative mineral analysis as revealed by the 3rd Reynolds Cup Contest. Clay & Clay Minerals, 54, 748-760.
62. Pate, J. S. and Verboom, W. H. 2009. Contemporary biogenic formation of clay pavements by eucalypts: further support for the phytotarium concept. Annals of Botany, 103, 673-685.
63. 86Sr ratios as tracers of Ca and Sr cycling in the Rio Icacos watershed, Luquillo Mountains, Puerto Rico. Chemical Geology, 267, 32-45.
64. Pirozynski, K. A. and Malloch, D. W. 1975. The origin of land plants: a matter of mycotropism. Biosystems, 6, 153-165.
65. Popp, B. N., Anderson, T. F. and Sandberg, P. A. 1986. Brachiopods as indicators of original isotopic compositions in some Palaeozoic limestones. Geological Society of America Bulletin, 97, 1262-1269.
66. Quirk, J., Beerling, D. J., Banwart, S. A., Kakonyi, G., Romero-Gonzalez, M. E. and Leake, J. R. 2012. Evolution of trees and mycorrhizal fungi intensifies silicate mineral weathering. Biology Letters, 8, 1006-1011.
67. 2 atmospheres enhance mineral weathering through increased below-ground carbon-energy fluxes. Biology Letters, 10, 20140375.
68. 2 decline. Biogeosciences, 11, 321-331.
69. Raven, J. A. and Edwards, D. 2001. Roots: evolutionary origins and biogeochemical significance. Journal of Experimental Botany, 52, 381-401.
70. Remy, W., Taylor, T. N., Hass, H. and Kerp, H. 1994. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proceedings of the National Academy of Sciences, 91, 11841-11843.
71. Retallack, G. J. 1985. Fossil soils as grounds for interpreting the advent of large plants and animals on land. Philosophical Transactions of the Royal Society, London B, 309, 105-142.
72. Retallack, G. J. 1986. The fossil record of soils. 1-57. In Wright, V. P. (ed.). Paleosols: their recognition and interpretation. Blackwell Scientific Publications, Oxford, 315 pp.
73. Retallack, G. J. 1988. Field recognition of paleosols. Geological Society of America, Special Paper, 216, 1-20.
74. Retallack, G. J. 1997. Early forest soils and their role in Devonian global change. Science, 276, 583.
75. Retallack, G. J. 2003. Soils and global change in the carbon cycle over geological time. Treatise on Geochemistry, 5 (5.18), 1-28.
76. Retallack, G. J. and Huang, C. 2011. Ecology and evolution of Devonian trees in New York, USA. Palaeogeography, Palaeoclimatology, Palaeoecology, 299, 110-128.
77. Rubinstein, C. V., Gerrienne, P., de la Puente, G. S., Astini, R. A. and Steemans, P. 2010. Early Middle Ordovician evidence for land plants in Argentina (eastern Gondwana). New Phytologist, 188, 365-369.
78. Sandberg, C. A., Ziegler, W., Dreesen, R. and Butler, J. L. 1988. Late Frasnian mass extinction: conodont event stratigraphy, global changes, and possible causes. Courier Forschunginstitut Senckenberg, 102, 263-307.
79. Sarwar, G. and Friedman, G. M. 1995. Post-Devonian sediment cover over New York State: evidence from fluid-inclusion, organic maturation, clay diagenesis and stable isotope studies. Lecture Notes in Earth Sciences, 58, Springer, Berlin, 113 pp.
80. Schußler, A., Schwarzott, D. and Walker, C. 2001. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycological Research, 105, 1413-1421.
81. Schumm, S. A. 1968. Speculations concerning paleohydrologic controls of terrestrial sedimentation. Geological Society of America Bulletin, 79, 1573-1588.
82. Schwendemann, A. B., Decombeix, A.-L., Taylor, T. N., Taylor, E. L. and Krings, M. 2011. Morphological and functional stasis in mycorrhizal root nodules as exhibited by a Triassic conifer. Proceedings of the National Academy of Sciences, 108, 13630-13634.
83. Sheldon, N. H. and Tabor, N. J. 2009. Quantitative paleoenvironmental and paleoclimatic reconstruction using paleosols. Earth-Science Reviews, 95, 1-52.
84. Simon, L., Bousquet, J., Levesque, R. C. and Lalonde, M. 1993. Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature, 363, 67-69.
85. Smeck, N. E. 1985. Phosphorus dynamics in soils and landscapes. Geoderma, 36, 185-199.
86. Smith, S. E. and Read, D. J. 2008. Mycorrhizal symbiosis. Third edition. Academic Press, Amsterdam, London, 800 pp.
87. Stein, W. E., Mannolini, F., Hernick, L. V., Landing, E. and Berry, C. M. 2007. Giant cladoxylopsid trees resolve the enigma of the Earth's earliest forest stumps at Gilboa. Nature, 446, 904-907.
88. Stein, W. E., Berry, C. M., Hernick, L. V. and Mannolini, F. 2012. Surprisingly complex community discovered in the mid-Devonian fossil forest at Gilboa. Nature, 483, 78-81.
89. Stockey, R. A., Rothwell, G. W., Addy, H. D. and Currah, R. S. 2001. Mycorrhizal association of the extinct conifer Metasequoia milleri. Mycological Research, 105, 202-205.
90. Strullu-Derrien, C. and Strullu, D.-G. 2007. Mycorrhization of fossil and living plants. Comptes Rendus Palevol, 6, 483-494.
91. Strullu-Derrien, C., Kenrick, P., Pressel, S., Duckett, J. G., Rioult, J.-P. and Strullu, D.-G. 2014. Fungal associations in Horneophyton ligneri from the Rhynie Chert (c. 407 million years ago) closely resemble those in extant lower land plants: novel insights into ancestral plant-fungus symbioses. New Phytologist, 203, 964-979.
92. Taylor, T. N., Klavins, S. D., Krings, M., Taylor, E. L., Kerp, H. and Hass, H. 2004. Fungi from the Rhynie Chert: a view from the dark side. Transactions of the Royal Society of Edinburgh: Earth Sciences, 94, 457-473.
93. Taylor, L. L., Leake, J. R., Quirk, J., Hardy, K., Banwart, S. A. and Beerling, D. J. 2009. Biological weathering and the long-term carbon cycle: integrating mycorrhizal evolution and function into the current paradigm. Geobiology, 7, 171-191.
94. Tosca, N. J., Johnston, D. T., Mushegian, A., Rothman, D. H., Summons, R. E. and Knoll, A. H. 2010. Clay mineralogy, organic carbon burial, and redox evolution in Proterozoic oceans. Geochimica et Cosmochimica Acta, 74, 1579-1592.
95. Turner, B. L., Lambers, H., Condron, L. M., Cramer, M. D., Leake, J. R., Richardson, A. E. and Smith, S. E. 2013. Soil microbial biomass and the fate of phosphorus during long-term ecosystem development. Plant & Soil, 367, 225-234.
96. Verboom, W. H., Pate, J. S. and Aspandiar, M. 2010. Neoformation of clay in lateral root catchments of mallee eucalypts: a chemical perspective. Annals of Botany, 105, 23-36.
97. Walker, T. W. and Syers, J. K. 1976. The fate of Phosphorus during pedogenesis. Geoderma, 15, 1-19.
98. Wang, B. and Qiu, Y. L. 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza, 16, 299-363.
99. Wardle, D. A., Walker, L. R. and Bardgett, R. D. 2004. Ecosystem properties and forest decline in contrasting long-term chronosequences. Science, 305, 509-513.
100. Weaver, C. E. 1989. Clays, muds, and shales. Developments in Sedimentology, 44, Elsevier, Amsterdam, 820 pp.
101. Woodrow, D. L. and Sevon, W. D. 1985. The Catskill Delta. Geological Society of America Special Paper, 201, 246 pp.
102. Wright, V. P. 1992. Paleosol recognition: a guide to early diagenesis in terrestrial settings. Chapter 12. 591-620. In Wolf, K. H. and Chilingarian, G. V. (eds). Diagenesis, III. Developments in Sedimentology, 47, Elsevier, Amsterdam.
103. Yanai, R. D., Blum, J. D., Hamburg, S. P., Arthur, M. A., Nezat, C. A. and Siccama, T. G. 2005. New insights into calcium depletion in Northeastern Forests. Journal of Forestry, 103, 14-20.
104. Zehetner, F., Lair, G. J., Graf, M. and Gerzabek, M. H. 2009. Rates of biogeochemical phosphorus and cooper redistribution in young floodplain soils. Biogeosciences, 6, 2949-2956.