The ecology of herbivore-induced silicon defences in grasses

Functional Ecology

Volumn 30, Issue 8, 2016, Pages 1311-1322

  Hartley, Susan E ^a   DeGabriel, Jane L ^b  

^a UNIVERSITY OF YORK   (United Kingdom)

^b WESTERN SYDNEY UNIVERSITY   (Australia)

Author keywords

defence induction; herbivory; insect; landscape scale; mammal; physical defences; plant herbivore interactions; silica

Indexed keywords

ABIOTIC FACTOR; BIOTIC FACTOR; BODY SIZE; CLIPPING; EXPERIMENT; FEEDING BEHAVIOR; FIELD METHOD; GRASS; GRAZING; HERBIVORE; HERBIVORY; INSECT; LANDSCAPE; MARSUPIAL; PHENOLOGY; PLANT COMMUNITY; PLANT-HERBIVORE INTERACTION; RODENT; SILICON; SOIL TYPE; UNGULATE; WATER AVAILABILITY;

HEXAPODA; MAMMALIA; METATHERIA; POACEAE; RODENTIA; UNGULATA;

EID: 84978471436     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12706     Document Type: Article

References (111)

1. Alborn, H.T., Turlings, T.C.J., Jones, T.H., Stenhagen, G., Loughrin, J.H. & Tumlinson, J.H. (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science, 276, 945–949.
2. Banuelos, M.J. & Obeso, J.R. (2000) Effect of grazing history, experimental defoliation, and genotype on patterns of silicification in Agrostis tenuis Sibth. Ecoscience, 7, 45–50.
3. Bazely, D.R., Vicari, M., Emmerich, S., Filip, L., Lin, D. & Inman, A. (1997) Interactions between herbivores and endophyte-infected Festuca rubra from the Scottish islands of St. Kilda, Benbecula and Rum. Journal of Applied Ecology, 34, 847–860.
4. Beckwith, R.S. & Reeve, R. (1964) Studies on soluble silica in soils. II. The release of monosilicic acid from soils. Australian Journal of Soil Research, 2, 157–168.
5. Bell, R.H.V. (1970) The use of the herb layer by grazing ungulates in the Serengeti. Animal Populations and Relations to their Food Resources (ed. A. Watson), pp. 111–124. Blackwell, Oxford, UK.
6. Bonaventure, G. (2012) Perception of insect feeding by plants. Plant Biology, 14, 872–880.
7. Bonaventure, G., VanDoorn, A. & Baldwin, I.T. (2011) Herbivore-associated elicitors: FAC signaling and metabolism. Trends in Plant Science, 16, 294–299.
8. Brizuela, M.A., Detling, J.K. & Cid, M.S. (1986) Silicon concentration of grasses growing in sites with different grazing histories. Ecology, 67, 1098–1101.
9. Calandra, I., Zub, K., Szafranska, P.A., Zalewski, A. & Merceron, G. (2016) Silicon-based plant defences, tooth wear and voles. Journal of Experimental Biology, 219, 501–507.
10. Cid, M.S., Detling, J.K., Brizuela, M.A. & Whicker, A.D. (1989) Patterns in grass silicification: response to grazing history and defoliation. Oecologia, 80, 268–271.
11. 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.
12. Cooke, J. & Leishman, M.R. (2011) Is plant ecology more siliceous than we realise? Trends in Plant Science, 16, 61–68.
13. Cotterill, J.V., Watkins, R.W., Brennon, C.B. & Cowan, D.P. (2007) Boosting silica levels in wheat leaves reduces grazing by rabbits. Pest Management Science, 63, 247–253.
14. Currie, H.A. & Perry, C.C. (2007) Silica in plants: Biological, biochemical and chemical studies. Annals of Botany, 100, 1383–1389.
15. Damuth, J. & Janis, C.M. (2011) On the relationship between hypsodonty and feeding ecology in ungulate mammals, and its utility in palaeoecology. Biological Reviews, 86, 733–758.
16. DeGabriel, J.L., Moore, B.D., Foley, W.J. & Johnson, C.N. (2009) The effects of plant defensive chemistry on nutrient availability predict reproductive success in a mammal. Ecology, 90, 711–719.
17. DeGabriel, J.L., Moore, B.D., Felton, A.M., Ganzhorn, J.U., Stolter, C., Wallis, I.R. et al. (2014) Translating nutritional ecology from the laboratory to the field: milestones in linking plant chemistry to population regulation in mammalian browsers. Oikos, 123, 298–308.
18. Deshmukh, R.K. & Belanger, R.R. (2016) Molecular evolution of aquaporins and silicon influx in plants. Functional Ecology, 30, 1277–1285.
19. Detling, J.K. & Painter, E.L. (1983) Defoliation responses of western wheatgrass populations with diverse histories of prairie dog grazing. Oecologia, 57, 65–71.
20. Ehrlich, H., Demadis, K.D., Pokrovsky, O.S. & Koutsoukos, P.G. (2010) Modern views on desilicification: biosilica and abiotic silica dissolution in natural and artificial environments. Chemical Reviews, 110, 4656–4689.
21. Epstein, E. (1999) Silicon. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 641–664.
22. Ergon, T., Lambin, X. & Stenseth, N.C. (2001) Life-history traits of voles in a fluctuating population respond to the immediate environment. Nature, 411, 1043–1045.
23. Ergon, T., Ergon, R., Begon, M., Telfer, S. & Lambin, X. (2011) Delayed density-dependent onset of spring reproduction in a fluctuating population of field voles. Oikos, 120, 934–940.
24. Erickson, K.L. (2014) Prairie grass phytolith hardness and the evolution of ungulate hypsodonty. Historical Biology, 26, 737–744.
25. Eswaran, A. & Manivannan, K. (2007) Effect of foliar application of lignite fly ash on the management of papaya leaf curl disease. Acta Horticulturae, 740, 271–275.
26. Faisal, S., Callis, K.L., Slot, M. & Kitajima, K. (2012) Transpiration-dependent passive silica accumulation in cucumber (Cucumis sativus) under varying soil silicon availability. Botany-Botanique, 90, 1058–1064.
27. Farmer, E. (2014) Leaf Defence. Oxford University Press, Oxford, UK.
28. Fauteux, F., Chain, F., Belzile, F., Menzies, J.G. & Belanger, R.R. (2006) The protective role of silicon in the Arabidopsis-powdery mildew pathosystem. Proceedings of the National Academy of Sciences of the United States of America, 103, 17554–17559.
29. Fenner, M., Lee, W.G. & Duncan, S.J. (1993) Chemical features of Chionochloa species in relation to grazing by ruminants in South Island, New Zealand. New Zealand Journal of Ecology, 17, 35–40.
30. Foley, W., Iason, G. & Makkar, H. (2007) Transdisciplinary studies of plant secondary metabolites: Lessons from ecology for animal science and vice versa. Proceedings of the 7th International Symposium on the Nutrition of Herbivores (eds Q.X. Meng, J.X. Liu & W.Y. Zhu). Beijing.
31. Gali-Muhtasib, H.U., Smith, C.C. & Higgins, J.J. (1992) The effect of silica in grasses on the feeding behavior of the prairie vole Microtus ochrogaster. Ecology, 73, 1724–1729.
32. Garbuzov, M., Reidinger, S. & Hartley, S.E. (2011) Interactive effects of plant-available soil silicon and herbivory on competition between two grass species. Annals of Botany, 108, 1355–1363.
33. Georgiadis, N.J. & McNaughton, S.J. (1990) Elemental and fiber contents of savanna grasses: variation with grazing, soil type, season and species. Journal of Applied Ecology, 27, 623–634.
34. Gomes, F.B., de Moraes, J.C., dos Santos, C.D. & Goussain, M.M. (2005) Resistance induction in wheat plants by silicon and aphids. Scientia Agricola, 62, 547–551.
35. Goussain, M.M., Prado, E. & Moraes, J.C. (2005) Effect of silicon applied to wheat plants on the biology and probing behaviour of the greenbug Schizaphis graminum (Rond.) (Hemiptera : Aphididae). Neotropical Entomology, 34, 807–813.
36. Griffin, M., Hogan, B. & Schmidt, O. (2015) Silicon reduces slug feeding on wheat seedlings. Journal of Pest Science, 88, 17–24.
37. Harbers, L.H., Raiten, D.J. & Paulsen, G.M. (1981) The role of plant epidermal silica as a structural inhibitor of rumen microbial digestion in steers. Nutrition Reports International, 24, 1057–1066.
38. Harbers, L.H. & Thouvenelle, M.L. (1980) Digestion of corn and sorghum silage observed by scanning electron microscopy. Journal of Animal Science, 50, 514–526.
39. Hartley, S.E. (2015) Round and round in cycles? Silicon-based plant defences and vole population dynamics. Functional Ecology, 29, 151–153.
40. Hartley, S.E. & DeGabriel, J.L. (2016) Data from: The ecology of herbivore-induced silicon defences in grasses. Dryad Digital Repository, http://dx.doi.org/10.5061/dryad.kd5s9.
41. Hartley, S.E. & Lawton, J.H. (1987) Effects of different types of damage on the chemistry of birch foliage, and the responses of birch feeding insects. Oecologia, 74, 432–437.
42. Hartley, S.E. & Lawton, J.H. (1991) Biochemical aspects and significance of the rapidly induced accumulation of phenolics in birch foliage. Phytochemical Induction by Herbivores (eds D.W. Tallamy & M.J. Raupp), pp. 105–132. Wiley, New York, NY.
43. 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, 35.
44. Haukioja, E. & Neuvonen, S. (1985) Induced long-term resistance of birch foliage against defoliators – defensive or incidental? Ecology, 66, 1303–1308.
45. Heil, M. & Ton, J. (2008) Long-distance signalling in plant defence. Trends in Plant Science, 13, 264–272.
46. 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.
47. Huitu, O., Forbes, K.M., Helander, M., Julkunen-Tiitto, R., Lambin, X., Saikkonen, K. et al. (2014) Silicon, endophytes and secondary metabolites as grass defenses against mammalian herbivores. Frontiers in Plant Science, 5, 478.
48. Hummel, J., Findeisen, E., Suedekum, K.-H., Ruf, I., Kaiser, T.M., Bucher, M. et al. (2011) Another one bites the dust: faecal silica levels in large herbivores correlate with high-crowned teeth. Proceedings of the Royal Society B-Biological Sciences, 278, 1742–1747.
49. 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.
50. Jarman, P.J. (1974) Social organization of antelope in relation to their ecology. Behaviour, 48, 215–267.
51. Karban, R. & Baldwin, I.T. (1997) Induced Responses to Herbivory. The University of Chicago Press, Chicago, IL, USA.
52. Katz, O. (2015) Silica phytoliths in angiosperms: phylogeny and early evolutionary history. New Phytologist, 208, 642–646.
53. Keeping, M.G., Meyer, J.H. & Sewpersad, C. (2013) Soil silicon amendments increase resistance of sugarcane to stalk borer Eldana saccharina Walker (Lepidoptera: Pyralidae) under field conditions. Plant and Soil, 363, 297–318.
54. Keeping, M.G., Miles, N. & Sewpersad, C. (2014) Silicon reduces impact of plant nitrogen in promoting stalk borer (Eldana saccharina) but not sugarcane thrips (Fulmekiola serrata) infestations in sugarcane. Frontiers in Plant Science, 5, 289.
55. Keeping, M.G. & Reynolds, O.L. (2009) Silicon in agriculture: new insights, new significance and growing application. Annals of Applied Biology, 155, 153–154.
56. Kindomihou, V., Sinsin, B. & Meerts, P. (2006) Effect of defoliation on silica accumulation in five tropical fodder grass species in Benin. Belgian Journal of Botany, 139, 87–102.
57. Korth, K.L. & Dixon, R.A. (1997) Evidence for chewing insect-specific molecular events distinct from a general wound response in leaves. Plant Physiology, 115, 1299–1305.
58. Kvedaras, O.L. & Keeping, M.G. (2007) Silicon impedes stalk penetration by the borer Eldana saccharina in sugarcane. Entomologia Experimentalis Et Applicata, 125, 103–110.
59. Kvedaras, O.L., Keeping, M.G., Goebel, F.R. & Byrne, M.J. (2007) Larval performance of the pyralid borer Eldana saccharina Walker and stalk damage in sugarcane: Influence of plant silicon, cultivar and feeding site. International Journal of Pest Management, 53, 183–194.
60. Kvedaras, O.L., Byrne, M.J., Coombes, N.E. & Keeping, M.G. (2009) Influence of plant silicon and sugarcane cultivar on mandibular wear in the stalk borer Eldana saccharina. Agricultural and Forest Entomology, 11, 301–306.
61. Lindroth, R.L. & Batzli, G.O. (1986) Inducible plant chemical defences – a cause of vole population cycles. Journal of Animal Ecology, 55, 431–449.
62. Lucas, P.W., van Casteren, A., Al-Fadhalah, K., Almusallam, A.S., Henry, A.G., Michael, S. et al. (2014) The role of dust, grit and phytoliths in tooth wear. Annales Zoologici Fennici, 51, 143–152.
63. Ma, J.F. (2004) Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Science and Plant Nutrition, 50, 11–18.
64. Ma, J.F. (2009) Silicon uptake and translocation in plants. The Proceedings of the International Plant Nutrition Colloquium XVI. Department of Plant Sciences, UC Davis, Davis, CA, USA.
65. Ma, J.F. & Yamaji, N. (2006) Silicon uptake and accumulation in higher plants. Trends in Plant Science, 11, 392–397.
66. Ma, J.F. & Yamaji, N. (2015) A cooperative system of silicon transport in plants. Trends in Plant Science, 20, 435–442.
67. Ma, J.F., Tamai, K., Yamaji, N., Mitani, N., Konishi, S., Katsuhara, M. et al. (2006) A silicon transporter in rice. Nature, 440, 688–691.
68. Massey, F.P., Ennos, A.R. & Hartley, S.E. (2006) Silica in grasses as a defence against insect herbivores: contrasting effects on folivores and a phloem feeder. Journal of Animal Ecology, 75, 595–603.
69. Massey, F.P., Ennos, A.R. & Hartley, S.E. (2007a) Grasses and the resource availability hypothesis: the importance of silica-based defences. Journal of Ecology, 95, 414–424.
70. Massey, F.P., Ennos, A.R. & Hartley, S.E. (2007b) Herbivore specific induction of silica-based plant defences. Oecologia, 152, 677–683.
71. Massey, F.P. & Hartley, S.E. (2006) Experimental demonstration of the antiherbivore effects of silica in grasses: impacts on foliage digestibility and vole growth rates. Proceedings of the Royal Society B-Biological Sciences, 273, 2299–2304.
72. 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.
73. Massey, F.P., Smith, M.J., Lambin, X. & Hartley, S.E. (2008) Are silica defences in grasses driving vole population cycles? Biology Letters, 4, 419–422.
74. 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.
75. McArt, S.H., Spalinger, D.E., Collins, W.B., Schoen, E.R., Stevenson, T. & Bucho, M. (2009) Summer dietary nitrogen availability as a potential bottom-up constraint on moose in south-central Alaska. Ecology, 90, 1400–1411.
76. McArthur, C. (2014) Do we ditch digestive physiology in explaining the classic relationship between herbivore body size diet and diet quality? Functional Ecology, 28, 1059–1060.
77. McColloch, J.W. & Salmon, S.C. (1923) The resistance of wheat to the Hessian Fly – a progress report. Journal of Economic Entomology, 16, 293–298.
78. McNaughton, S.J. & Tarrants, J.L. (1983) Grass leaf silicification – natural selection for an inducible defense against herbivores. Proceedings of the National Academy of Sciences of the United States of America, 80, 790–791.
79. McNaughton, S.J., Tarrants, J.L., McNaughton, M.M. & Davis, R.H. (1985) Silica as a defense against herbivory and a growth promotor in African grasses. Ecology, 66, 528–535.
80. Moraes, J.C., Goussain, M.M., Basagli, M.A.B., Carvalho, G.A., Ecole, C.C. & Sampaio, M.V. (2004) Silicon influence on the tritrophic interaction: Wheat plants, the greenbug Schizaphis graminum (Rondani) (Hemiptera : Aphididae), and its natural enemies, Chrysoperla externa (Hagen) (Neuroptera : Chrysopidae) and Aphidius colemani viereck (Hymenoptera : Aphidiidae). Neotropical Entomology, 33, 619–624.
81. Piperno, D.R. (2006) Pytoliths: A comprehensive Guide for Archaeologists and Palaeoecologists. AltaMira Press, Oxford, UK.
82. Ponnaiya, B. (1951) Studies on the genus Sorghum. II The cause of resistance in sorghum to the insect pest Atherigona indica M. Madras University Journal, 21, 203–217.
83. 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.
84. Rabenold, D. & Pearson, O.M. (2011) Abrasive, silica phytoliths and the evolution of thick molar enamel in primates, with implications for the diet of Paranthropus boisei. PLoS ONE, 6, e28379.
85. Raven, J.A. (1983) The transport and function of silicon in plants. Biological Reviews of the Cambridge Philosophical Society, 58, 179–207.
86. Redmond, C.T. & Potter, D.A. (2006) Silicon fertilization does not enhance creeping bentgrass resistance to cutworms and white grubs. Applied Turfgrass Science [Online], 6, 1–7.
87. Reidinger, S., Ramsey, M.H. & Hartley, S.E. (2012) Rapid and accurate analyses of silicon and phosphorus in plants using a portable X-ray fluorescence spectrometer. New Phytologist, 195, 699–706.
88. Reymond, P., Weber, H., Damond, M. & Farmer, E.E. (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell, 12, 707–719.
89. Reynolds, O.L., Keeping, M.G. & Meyer, J.H. (2009) Silicon-augmented resistance of plants to herbivorous insects: a review. The Annals of Applied Biology, 155, 171–186.
90. Reynolds, J.J.H., Lambin, X., Massey, F.P., Reidinger, S., Sherratt, J.A., Smith, M.J. et al. (2012) Delayed induced silica defences in grasses and their potential for destabilising herbivore population dynamics. Oecologia, 170, 445–456.
91. Rivals, F., Takatsuki, S., Maria Albert, R. & Macia, L. (2014) Bamboo feeding and tooth wear of three sika deer (Cervus nippon) populations from northern Japan. Journal of Mammalogy, 95, 1043–1053.
92. 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. Korndorfer), pp. 85–113. Elsevier Science, Amsterdam, the Netherlands.
93. Sanson, G.D., Kerr, S.A. & Gross, K.A. (2007) Do silica phytoliths really wear mammalian teeth? Journal of Archaeological Science, 34, 526–531.
94. Sasamoto, K. (1953) Studies on the relation between insect pests and silica content in rice plant (II). On the injury of the second generation larvae of rice stem borer. Oyo Kontyu, 9, 108–110.
95. Seastedt, T.R., Ramundo, R.A. & Hayes, D.C. (1989) Silica, nitrogen and phosphorus dynamics of tallgrass prairie. 11th North American Prairie Conference, pp. 205–210. University of Nebraska Press, Lincoln, NE, USA.
96. 3 grasses – effects on forage quality and sheep preference. Journal of Range Management, 42, 122–127.
97. Smith, M.J., White, A., Lambin, X., Sherratt, J.A. & Begon, M. (2006) Delayed density-dependent season length alone can lead to rodent population cycles. The American Naturalist, 167, 695–704.
98. Soininen, E.M., Brathen, K.A., Jusdado, J.G.H., Reidinger, S. & Hartley, S.E. (2013) More than herbivory: levels of silica-based defences in grasses vary with plant species, genotype and location. Oikos, 122, 30–41.
99. Stam, J.M., Kroes, A., Li, Y., Gols, R., van Loon, J.J.A., Poelman, E.H. et al. (2014) Plant interactions with multiple insect herbivores: From community to genes. Annual Review of Plant Biology, 65, 689–713.
100. Steuer, P., Suedekum, K.-H., Tuetken, T., Mueller, D.W.H., Kaandorp, J., Bucher, M. et al. (2014) Does body mass convey a digestive advantage for large herbivores? Functional Ecology, 28, 1127–1134.
101. Strömberg, C., Di Stilio, V. & Song, Z. (2016) Functions of phytoliths in vascular plants: an evolutionary perspective. Functional Ecology, 30, 1286–1297.
102. Tanentzap, A.J., Vicari, M. & Bazely, D.R. (2014) Ungulate saliva inhibits a grass-endophyte mutualism. Biology Letters, 10, 20140460.
103. Tian, D., Peiffer, M., Shoemaker, E., Tooker, J., Haubruge, E., Francis, F. et al. (2012) Salivary glucose oxidase from caterpillars mediates the induction of rapid and delayed-induced defenses in the tomato plant. PLoS ONE, 7, e36168.
104. Valkama, E., Koricheva, J., Ossipov, V., Ossipova, S., Haukioja, E. & Pihlaja, K. (2005) Delayed induced responses of birch glandular trichomes and leaf surface lipophilic compounds to mechanical defoliation and simulated winter browsing. Oecologia, 146, 385–393.
105. Vicari, M. & Bazely, D.R. (1993) Do grasses fight back? The case for antiherbivore defences. Trends in Ecology & Evolution, 8, 137–141.
106. Walters, D. (2010) Plant Defense: Warding off Attack by Pathogens, Herbivores and Parasitic Plants, Wiley-Blackwell, Chichester, UK.
107. Watling, K.M., Parr, J.F., Rintoul, L., Brown, C.L. & Sullivan, L.A. (2011) Raman, infrared and XPS study of bamboo phytoliths after chemical digestion. Spectrochimica Acta. Part A, Molecular and Biomolecular Spectroscopy, 80, 106–111.
108. Wieczorek, M., Szafranska, P.A., Labecka, A.M., Lazaro, J. & Konarzewski, M. (2015a) Effect of the abrasive properties of sedges on the intestinal absorptive surface and resting metabolic rate of root voles. Journal of Experimental Biology, 218, 309–315.
109. Wieczorek, M., Zub, K., Szafranska, P.A., Ksiazek, A. & Konarzewski, M. (2015b) Plant-herbivore interactions: silicon concentration in tussock sedges and population dynamics of root voles. Functional Ecology, 29, 187–194.
110. Yamaji, N., Sakurai, G., Mitani-Ueno, N. & Ma, J.F. (2015) Orchestration of three transporters and distinct vascular structures in node for intervascular transfer of silicon in rice. Proceedings of the National Academy of Sciences of the United States of America, 112, 11401–11406.
111. Ye, M., Song, Y., Long, J., Wang, R., Baerson, S.R., Pan, Z. et al. (2013) Priming of jasmonate-mediated antiherbivore defense responses in rice by silicon. Proceedings of the National Academy of Sciences of the United States of America, 110, E3631–E3639.