Functions of phytoliths in vascular plants: an evolutionary perspective

Functional Ecology

Volumn 30, Issue 8, 2016, Pages 1286-1297

  Strömberg, Caroline A E ^a   Di Stilio, Verónica S ^a   Song, Zhaoliang ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b TIANJIN UNIVERSITY   (China)

Author keywords

adaptation; evolution; herbivore defence; phytoliths; plant silica; structural support

Indexed keywords

ADAPTATION; ANTAGONISM; BIOMECHANICS; CENOZOIC; DEFENSE MECHANISM; EVOLUTION; HERBIVORE; LIGNIN; NUTRIENT AVAILABILITY; PHYLOGENETICS; PHYLOGENY; PHYTOLITH; SILICA; VASCULAR PLANT;

EMBRYOPHYTA; MAMMALIA; POACEAE; TRACHEOPHYTA;

EID: 84978971005     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12692     Document Type: Article

References (87)

1. Baker, G., Jones, L.H.P. & Wardrop, I.D. (1959) Cause of wear in sheeps’ teeth. Nature, 184, 1583–1584.
2. 4 grasses and savanna adapted ungulates. Global Change Biology, 15, 2397–2417.
3. Calandra, I., Zub, K., Szafrańska, P.A., Zalewski, A. & Merceron, G. (2016) Silicon-based plant defences, tooth wear and voles. Journal of Experimental Biology, 219, 501–507.
4. Carter, J.A. (1999) Late Devonian, Permian and Triassic phytoliths from Antarctica. Micropaleontology, 45, 56–61.
5. Chapman, R.F. (1964) The structure and wear of the mandibles in some African grasshoppers. Proceedings of the Zoological Society of London, 142, 107–121.
6. Christin, P.-A., Spriggs, E., Osborne, C.P., Strömberg, C.A.E., Salamin, N. & Edwards, E.J. (2014) Molecular dating, evolutionary rates, and the age of the grasses. Systematic Biology, 63, 153–165.
7. Cid, M.S., Detling, J.K., Whicker, A.D. & Brizuela, M.A. (1990) Silicon uptake and distribution in Agropyron smithii as related to grazing history and defoliation. Journal of Range Management, 43, 344–346.
8. Ciochon, R.L., Piperno, D.R. & Thompson, R.G. (1990) Opal phytoliths found on the teeth of the extinct ape Gigantopithecus blacki: implications for paleodietary studies. Proceedings of the National Academy of Sciences of the United States of America, 87, 8120–8124.
9. Conley, D.J. & Carey, J.C. (2015) Biogeochemistry: silica cycling over geologic time. Nature Geoscience, 8, 431–432.
10. Cooke, J. & Leishman, M.R. (2012) Tradeoffs between foliar silicon and carbon-based defences: evidence from vegetation communities of contrasting soil types. Oikos, 121, 2052–2060.
11. Coughenour, M.B. (1985) Graminoid responses to grazing by large herbivores: adaptations, exaptations, and interacting processes. Annals of the Missouri Botanical Garden, 72, 852–863.
12. Craine, J.M. (2009) Resource Strategies of Wild Plants. Princeton University Press, Princeton, NJ, USA.
13. Damuth, J. & Janis, C.M. (2014) A comparison of observed molar wear rates in extant herbivorous mammals. Annales Zoologici Fennici, 51, 188–200.
14. Deshmukh, R. & Bélanger, R.R. (2016) Molecular evolution of aquaporins and silicon influx in plants. Functional Ecology, 30, 1277–1285.
15. Dorweiler, J.E. & Doebley, J. (1997) Developmental analysis of Teosinte Glume Architecture1: a key locus in the evolution of maize (Poaceae). American Journal of Botany, 84, 1313–1322.
16. Dunn, R.E., Strömberg, C.A.E., Madden, R.H., Kohn, M.J. & Carlini, A.A. (2015) Linked canopy, climate and faunal evolution in the Cenozoic of Patagonia. Science, 347, 258–261.
17. Epstein, E. (1999) Silicon. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 641–664.
18. Erickson, K.L. (2014) Prairie grass phytolith hardness and the evolution of ungulate hypsodonty. Historical Biology, 26, 737–744.
19. Erickson, G.M., Krick, B.A., Hamilton, M., Bourne, G.R., Norell, M.A., Lilleodden, E. et al. (2012) Complex dental structure and wear biomechanics in hadrosaurid dinosaurs. Science, 338, 98–101.
20. Felton, G.W. & Eichenseer, H. (1999) Herbivore saliva and its effects on plant defense against herbivores and pathogens. Induced Plant Defenses Against Pathogens and Herbivores: Biochemistry, Ecology, and Agriculture (eds A.A. Agrawal, S. Tuzun & E. Bent), pp. 19–36. American Phytopathological Society Press, St. Paul, MN, USA.
21. Fox, C.L., Juan, J. & Albert, R.M. (1996) Phytolith analysis on dental calculus, enamel surface, and burial soil: information about diet and paleoenvironment. American Journal of Physical Anthropology, 101, 101–113.
22. Georgiadis, N.J. & McNaughton, S.J. (1990) Elemental and fibre contents of savanna grasses: variation with grazing, soil type, season and species. Journal of Applied Ecology, 27, 623–634.
23. Grégoire, C., Rémus-Borel, W., Vivancos, J., Labbé, C., Belzile, F. & Bélanger, R.R. (2012) Discovery of a multigene family of aquaporin silicon transporters in the primitive plant Equisetum arvense. The Plant Journal, 72, 320–330.
24. Grimaldi, D. & Engel, M.S. (2005) Evolution of the Insects. Cambridge University Press, New York, NY, USA.
25. Gügel, I.L., Grupe, G. & Kunzelmann, K.H. (2001) Simulation of dental microwear: characteristic traces by opal phytoliths give clues to ancient human dietary behavior. American Journal of Physical Anthropology, 114, 124–138.
26. Hanley, M.E., Lamont, B.B., Fairbanks, M.M. & Rafferty, C.M. (2007) Plant structural traits and their role in anti-herbivore defence. Perspectives in Plant Ecology Evolution and Systematics, 8, 157–178.
27. Hartley, S.E. & DeGabriel, J.L. (2016) The ecology of herbivore-induced silicon defences in grasses. Functional Ecology, 30, 1311–1322.
28. Hartley, S.E., Fitt, R.N., McLamon, E.L. & Wade, R.N. (2015) Defending the leaf surface: intra- and inter-specific differences in silicon deposition in grasses in response to damage and silicon supply. Frontiers in Plant Science, 6, Article 35, 1–8.
29. Hodson, M.J., White, P.J., Mead, A. & Broadley, M.R. (2005) Phylogenetic variation in the silicon composition of plants. Annals of Botany, 96, 1027–1046.
30. Hunt, J.W., Dean, A.P., Webster, R.E., Johnson, G.N. & Ennos, A.R. (2008) A novel mechanism by which silica defends grasses against herbivory. Annals of Botany, 102, 653–656.
31. Jardine, P.E., Janis, C.M., Sahney, S. & Benton, M.J. (2012) Grit not grass: concordant patterns of early origin of hypsodonty in Great Plains ungulates and Glires. Palaeogeography Palaeoclimatology Palaeoecology, 365–366, 1–10.
32. Kaiser, T.M., Mueller, D.W.H., Fortelius, M., Schulz, E., Codron, D. & Clauss, M. (2013) Hypsodonty and tooth facet development in relation to diet and habitat in herbivorous ungulates: implications for understanding tooth wear. Mammal Review, 43, 34–46.
33. Katz, O. (2015) Silica phytoliths in angiosperms: phylogeny and early evolutionary history. New Phytologist, 2015, 1–4.
34. Katz, O., Lev-Yadun, S. & Bar, P. (2014) Do phytoliths play an antiherbivory role in southwest Asian Asteraceae species and to what extent? Flora, 209, 349–358.
35. Labandeira, C.C. (2006) The four phases of plant-arthropod associations in deep time. Geologica Acta, 4, 409–438.
36. Law, C. & Exley, C. (2011) New insight into silica deposition in horsetail (Equisetum arvense). BMC Plant Biology, 11, 112.
37. Lewin, J. & Reimann, B.E.F. (1969) Silicon and plant growth. Annual Review of Plant Physiology, 20, 289–304.
38. Lucas, P.W., Omar, R., Al-Fadhalah, K., Almusallam, A.S., Henry, A.G., Michael, S. et al. (2013) Mechanisms and causes of wear in tooth enamel: implications for hominin diets. Journal of the Royal Society Interface, 10, 20120923.
39. Ma, J.F., Nishimura, K. & Takahashi, E. (1989) Effect of silicon on the growth of rice plant at different growth-stages. Soil Science and Plant Nutrition, 35, 347–356.
40. Ma, J.F. & Takahashi, E. (2002) Soil, Fertilizer, and Plant Silicon Research in Japan. Elsevier Science, Amsterdam, the Netherlands.
41. Ma, J.F. & Yamaji, N. (2015) A cooperative system of silicon transport in plants. Trends in Plant Science, 20, 435–442.
42. MacFadden, B.J. (1997) Origin and evolution of the grazing guild in New World terrestrial mammals. Trends in Ecology and Evolution, 12, 182–187.
43. Madden, R.H. (2014) Hypsodonty in Mammals. Evolution, Geomorphology, and the Role of Earth Surface Processes. Cambridge University Press, Cambridge, UK.
44. Maddison, W.P. & Maddison, D.R. (2010) Mesquite: a modular system for evolutionary analysis. http://www.mesquiteproject.org.
45. Magallón, S., Hilu, K.W. & Quandt, D. (2013) Land plant evolutionary timeline: gene effects are secondary to fossil constraints in relaxed clock estimation of age and substitution rates. American Journal of Botany, 100, 556–573.
46. Massey, F.P. & Hartley, S.E. (2009) Physical defences wear you down: progressive and irreversible impacts of silica on insect herbivores. Journal of Animal Ecology, 78, 281–291.
47. Massey, F.P., Massey, K., Ennos, A.R. & Hartley, S.E. (2009) Impacts of silica-based defences in grasses on the feeding preferences of sheep. Basic and Applied Ecology, 10, 622–630.
48. 4 grasslands in North America: stable carbon isotope ratios of fossil phytoliths. Paleobiology, 37, 23–49.
49. McNaughton, S.J., Tarrants, J.L., McNaughton, M. & Davis, R.H. (1985) Silica as a defense against herbivory and a growth promotor in African grasses. Ecology, 66, 528–535.
50. Merceron, G., Costeur, L., Maridet, O., Ramdarshan, A. & Gohlich, U.B. (2012) Multi-proxy approach detects heterogeneous habitats for primates during the Miocene climatic optimum in Central Europe. Journal of Human Evolution, 63, 150–161.
51. Mihlbachler, M.C., Rivals, F., Solounias, N. & Semprebon, G.M. (2011) Dietary change and evolution of horses in North America. Science, 331, 1178–1181.
52. Müller, J., Clauss, M., Codron, D., Schulz, E., Hummel, J., Fortelius, M. et al. (2014) Growth and wear of incisor and cheek teeth in domestic rabbits (Oryctolagus cuniculus) fed diets of different abrasiveness. Journal of Experimental Zoology Part A-Ecological Genetics and Physiology, 321, 283–298.
53. Müller, J., Clauss, M., Codron, D., Schulz, E., Hummel, J., Kircher, P. et al. (2015) Tooth length and incisal wear and growth in guinea pigs (Cavia porcellus) fed diets of different abrasiveness. Journal of Animal Physiology and Animal Nutrition, 99, 591–604.
54. O'Reagain, P.J. & Mentis, M.T. (1989) Leaf silification in grasses – a review. Journal of the Grassland Society of South Africa, 6, 37–43.
55. Ozaki Kubo, M. & Yamada, E. (2014) The inter-relationship between dietary and environmental properties and tooth wear: comparisons of mesowear, molar wear rate, and hypsodonty index of extant sika deer populations. PLoS ONE, 9, 1–12.
56. Padian, K. (1987) A comparative phylogenetic and functional approach to the origin of vertebrate flight. Recent Advances in the Study of Bats (eds M.B. Fenton, P. Racey & J.M.V. Rayner), pp. 3–22. Cambridge University Press, Cambridge, UK.
57. Piperno, D.R. (1989) The occurrence of phytoliths in the reproductive structures of selected tropical angiosperms and their significance in tropical paleoecology, paleoethnobotany and systematics. Review of Palaeobotany and Palynology, 61, 147–173.
58. Piperno, D.R. (2006) Phytoliths: A Comprehensive Guide for Archaeologists and Paleoecologists, 1st edn. AltaMira Press, New York, New York, USA.
59. Prasad, V., Strömberg, C.A.E., Alimohammadian, H. & Sahni, A. (2005) Dinosaur coprolites and the early evolution of grasses and grazers. Science, 310, 1177–1180.
60. Quigley, K.M. & Anderson, T.M. (2014) Leaf silica concentration in Serengeti grasses increases with watering but not clipping: insights from a common garden study and literature review. Frontiers in Plant Science, 5, 568.
61. Rabenhold, D. & Pearson, O.M. (2014) Scratching the surface: a critique of Lucas et al. (2013)'s conclusion that phytoliths do not abrade enamel. Journal of Human Evolution, 74, 130–133.
62. Raven, J.A. (1983) The transport and function of silicon in plants. Biological Reviews, 58, 179–207.
63. Reisz, R.R. & Sues, H.-D. (2005) Herbivory in late Paleozoic and Triassic terrestrial vertebrates. Evolution of Herbivory in Terrestrial Vertebrates: Perspectives From the Fossil Record (ed. H.-D. Sues), pp. 9–41. Cambridge University Press, Cambridge, UK.
64. Reynolds, O.L., Keeping, M.G. & Meyer, J.H. (2009) Silicon-augmented resistance of plants to herbivorous insects: a review. Annals of Applied Biology, 155, 171–186.
65. 2 during the Phanerozoic: tools, patterns, and impacts. Treatise on Geochemistry Volume 6:The Atmosphere – History (ed. J. Farquhar), pp. 251–267, 2nd edn. Elsevier, Amsterdam, the Netherlands.
66. Sacała, E. (2009) Role of silicon in plant resistance to water stress. Journal of Elementology, 14, 619–630.
67. Sangster, A.G., Hodson, M.J. & Tubb, H.J. (2001) Silicon deposition in higher plants. Silicon in Agriculture (eds L.E. Datnoff, G.H. Snyder & G.H. Korndörfer), pp. 85–113. Elsevier, Amsterdam, the Netherlands.
68. Sanson, G.D., Kerr, S.A. & Gross, K.A. (2007) Do silica phytoliths really wear mammalian teeth? Journal of Archaeological Science, 34, 526–531.
69. Schoelynck, J., Bal, K., Backx, H., Okruszko, T., Meire, P. & Struyf, E. (2010) Silica uptake in aquatic and wetland macrophytes: a strategic choice between silica, lignin and cellulose? New Phytologist, 186, 385–391.
70. Schulter, D., Price, T., Mooers, A.O. & Ludwig, D. (1997) Likelihood of ancestor states in adaptive radiation. Evolution, 51, 1699–1711.
71. Schulz, E., Piotrowski, V., Clauss, M., Mau, M., Merceron, G. & Kaiser, T.M. (2013) Dietary abrasiveness is associated with variability of microwear and dental surface texture in rabbits. PLoS ONE, 8, e56167.
72. Scotese, C.R. (2002) http://www.scotese.com (PALEOMAP website).
73. Solounias, N. & Semprebon, G.M. (2002) Advances in the reconstruction of ungulate ecomorphology with application to early fossil equids. American Museum Novitates, 3366, 1–49.
74. Song, H., Amédégnato, C., Cigliano, M.M., Desutter-Grandcolas, L., Heads, S.W., Huang, Y. et al. (2015) 300 million years of diversification: elucidating the patterns of orthopteran evolution based on comprehensive taxon and gene sampling. Cladistics, 2015, 1–31.
75. Stebbins, G.L. (1981) Coevolution of grasses and herbivores. Annals of the Missouri Botanical Garden, 68, 75–86.
76. Strömberg, C.A.E. (2005) Decoupled taxonomic radiation and ecological expansion of open-habitat grasses in the Cenozoic of North America. Proceedings of the National Academy of Sciences of the United States of America, 102, 11980–11984.
77. Strömberg, C.A.E. (2006) The evolution of hypsodonty in equids: testing a hypothesis of adaptation. Paleobiology, 32, 236–258.
78. Strömberg, C.A.E. (2011) Evolution of grasses and grassland ecosystems. Annual Review of Earth and Planetary Sciences, 39, 517–544.
79. Strömberg, C.A.E., Werdelin, L., Friis, E.M. & Saraç, G. (2007) The spread of grass-dominated habitats in Turkey and surrounding areas during the Cenozoic: phytolith evidence. Palaeogeography, Palaeoclimatology, Palaeoecology, 250, 18–49.
80. Trembath-Reichert, E., Wilson, J.P., McGlynn, S.E. & Fischer, W.W. (2015) Four hundred million years of silica biomineralization in land plants. Proceedings of the National Academy of Sciences of the United States of America, 112, 5449–5454.
81. Tweet, J.S., Chin, K., Braman, D.R. & Murphy, N.L. (2008) Probable gut contents within a specimen of Brachylophosaurus canadensis (Dinosauria: Hadrosauridae) from the Upper Cretaceous Judith River Formation of Montana. Palaios, 23, 624–635.
82. Vermeij, G.J. (2015) Plants that lead: do some surface features direct enemy traffic on leaves and stems? Biological Journal of the Linnean Society, 116, 288–294.
83. Williams, V.S., Barrett, P.M. & Purnell, M.A. (2009) Quantitative analysis of dental microwear in hadrosaurid dinosaurs, and the implications for hypotheses of jaw mechanics and feeding. Proceedings of the National Academy of Sciences of the United States of America, 106, 11194–11199.
84. Williams, S.H. & Kay, R.F. (2001) A comparative test of adaptive explanations for hypsodonty in ungulates and rodents. Journal of Mammalian Evolution, 8, 207–229.
85. Wings, O. & Sander, P.M. (2007) No gastric mill in sauropod dinosaurs: new evidence from analysis of gastrolith mass and function in ostriches. Proceedings of the Royal Society B, 274, 635–640.
86. Zachos, J., Pagani, M., Sloan, L., Thomas, E. & Billups, K. (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science, 292, 686–693.
87. Zheng, Y., Dong, Y., Matsui, A., Udatsu, T. & Fujiwara, H. (2003) Molecular genetic basis of determining subspecies of ancient rice using the shape of phytoliths. Journal of Archaeological Science, 30, 1215–1221.