Grasses are major agricultural products worldwide and they are critical to ecosystem function in many terrestrial habitats. Despite their global importance, we know relatively little about their defenses against herbivory. Grasses tend to be tolerant of leaf loss because their valuable meristems are located underground, out of reach for above ground herbivores. Many grasses have unidirectional leaf hairs, prickles, and spines that make moving up the leaf blade easy, but make moving down, toward the meristem, difficult. We tested the hypothesis that unidirectional grass hairs direct small arthropod herbivores away from the meristems. In a field survey of the distribution of herbivore damage, we found that leaf tips received five times more damage than leaf bases for Avena barbata. Early-instar grasshoppers fed three times as often on leaf tops as on leaf bases of pubescent individuals in a common garden laboratory experiment. This effect was not observed for glabrous individuals where grasshoppers damaged leaf bases as often as leaf tops. A common generalist caterpillar, Heliothus virescens, was more than twice as likely to turn in the direction of the hairs, away from the meristems, when it encountered pubescent leaves of A. barbata. However, larger caterpillars of the generalist feeder Arctia virginalis showed no directional bias when they encountered pubescent leaves. In common garden experiments, selection on pubescence was weak and inconsistent over space and time. Under some circumstances, individuals of A. barbata with pubescent leaves were more likely to produce seeds than were individuals with fewer hairs. The surveys, behavioral experiments with small insects, and estimates of lifetime reproduction all support the hypothesis that unidirectional leaf hairs on A. barbata, and perhaps other grasses, serve as an unstudied defense that direct small herbivores away from the meristems.
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Allard RW, Babbel GR, Kahler AL, Clegg MT (1972) Evidence for coadaptation in Avena barbata. Proc Natl Acad Sci (USA) 69:3043–3048
Blair J, Nippert J, Briggs J (2014) Grassland ecology. In: Monson RK (ed) Ecology and the environment, the plant sciences, vol 8. Springer Science + Business Media, New York, pp 389–423
Clay K (1990) Fungal endophytes of grasses. Annu Rev Ecol Syst 21:275–297
Clegg MT, Allard RW (1972) Patterns of genetic differentiation in slender wild oat species Avena barbata. Proc Natl Acad Sci 69:1820–1824
Eaton KM, Karban R (2014) Effects of trichomes on the behavior and distribution of Platyprepia virginalis caterpillars. Entomol Exp Appl 151:144–151
Epstein E (1999) Silicon. Annu Rev Plant Physiol Plant Mol Biol 50:641–664
Farmer EE (2014) Leaf defense. Oxford University Press, Oxford
Gardner KM, Latta RG (2008) Heritable variation and genetic correlation of quantitative traits within and between ecotypes of Avena barbata. J Evol Biol 21:737–748
Hartley SE, DeGabriel JL (2016) The ecology of herbivore-induced silicon defences in grasses. Funct Ecol 30:1311–1322
Jennings DL (1962) Some evidence on the influence of the morphology of raspberry canes upon their liability to be attacked by certain fungi. Hortic Res 1:100–111
Johnson HB (1975) Plant pubescence: an ecological perspective. Bot Rev 41:233–258
Jungner JR (1891) Anpassungen der pflanzen an das klima in den gegenden der regenreichen kamerungebirge. Botanisches Centralblatt 47:353–360
Karban R, Takabayashi J (2019) Chewing and other cues induce grass spines that protect meristems. Arthropod-Plant Interact. https://doi.org/10.1007/s11829-018-9666-1
Karban R, Karban C, Huntzinger M, Pearse IS, Crutsinger G (2010) Diet mixing enhances the performance of a generalist caterpillar, Platyprepia virginalis. Ecol Entomol 35:92–99
Krimmel BA, Pearse IS (2013) Sticky plant traps insects to enhance indirect defense. Ecol Lett 16:219–224
Latta RG (2009) Testing for local adaptation in Avena barbata: a classic example of ecotypic divergence. Mol Ecol 18:3781–3791
Latta RG, McCain C (2009) Path analysis of natural selection via survival and fecundity across contrasting environments in Avena barbata. J Evol Biol 22:2458–2469
Levin DA (1973) The role of trichomes in plant defense. Q Rev Biol 48:3–15
LoPresti EF, Pearse IS, Charles GK (2015) The siren song of a sticky plant: columbines provision mutualist arthropods by attracting and killing passerby insects. Ecology 96:2862–2869
Marquis RJ (1992) A bite is a bite is a bite? Constraints on response to folivory in Piper arieianum (Piperaceae). Ecology 73:143–152
Marshall DR, Jain SK (1969) Genetic polymorphism in natural populations of Avena fatua and A. barbata. Nature 221:276–278
Massey FP, Ennos AR, Hartley SE (2006) Silica in grasses as a defence against insect herbivores: contrasting effects on folivores and a phloem feeder. J Anim Ecol 75:595–603
Mauricio R, Bowers MD, Bazzaz FA (1993) Pattern of leaf damage affects fitness of the annual plant Raphanus sativus (Brassicaceae). Ecology 74:2066–2071
McKinney KB (1938) Physical characteristics of the foliage of beans and tomatoes that tend to control some small insects. J Econ Entomol 31:630–631
McNaughton SJ (1979) Grazing as an optimization process: grass ungulate relationships in the Serengeti. Am Nat 113:691–703
McNaughton SJ, Tarrants JL (1983) Grass leaf silicification: natural selection for an inducible defense against herbivores. Proc Natl Acad Sci 80:790–791
Metcalfe CR (1960) Anatomy of the monocotyledons. I. Gramineae. Oxford University Press, Oxford
Meyer GA (1998) Pattern of defoliation and its effect on photosynthesis and growth of goldenrod. Funct Ecol 12:270–279
Moore BD, Johnson SN (2017) Get tough, get toxic, or get a bodyguard: identifying candidate traits conferring belowground resistance to herbivores in grasses. Front Plant Sci 7:1925
Sokal RR, Rohlf FJ (1969) Biometry. Freeman, San Francisco
Stuart W (1906) Disease resistance of potatoes. Utah Agric Exp Stn Bull 122:105–136
van der Meijden E, Wijn M, Verkaar HJ (1988) Defense and regrowth, alternative plant strategies in the struggle against herbivores. Oikos 51:355–363
Vermeij GJ (2015) Plants that lead: do some surface features direct enemy traffic on leaves and stems? Biol J Linn Soc 116:288–294
Vicari M, Bazely DR (1993) Do grasses fight back? The case for antiherbivore defences. Trends Ecol Evol 8:137–141
Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle River
We thank Mikaela Huntzinger, Claire Karban, Jesse Karban, Katherine Toll, and Phil Ward for help with fieldwork. Ellen Dean identified the grasses. Mikaela Huntzinger and an anonymous reviewer improved the manuscript. The field studies were conducted at the UC McLaughlin Reserve, Hopland Research and Extension Center and Sierra Foothills Research and Extension Center, and we thank the staff for facilitating our work. We were supported by USDA multistate Grants NC-7 and NE-1501.
Communicated by Colin Mark Orians.
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Karban, R., LoPresti, E., Vermeij, G.J. et al. Unidirectional grass hairs usher insects away from meristems. Oecologia 189, 711–718 (2019). https://doi.org/10.1007/s00442-019-04355-7
- Leaf hairs