How plant traits respond to and affect vertebrate and invertebrate herbivores-Are measurements comparable across herbivore types?
animals
ecosystem
grassland
herbivory
nitrogen
Journal
Plant, cell & environment
ISSN: 1365-3040
Titre abrégé: Plant Cell Environ
Pays: United States
ID NLM: 9309004
Informations de publication
Date de publication:
Jan 2024
Jan 2024
Historique:
revised:
28
09
2023
received:
11
06
2023
accepted:
05
10
2023
medline:
5
12
2023
pubmed:
19
10
2023
entrez:
19
10
2023
Statut:
ppublish
Résumé
Despite plants realistically being affected by vertebrate and invertebrate herbivores simultaneously, fundamental differences in the ecology and evolution of these two herbivore guilds often means their impacts on plants are studied separately. A synthesis of the literature is needed to understand the types of plant traits examined and their response to, and effect on (in terms of forage selection) vertebrate and invertebrate herbivory, and to identify associated knowledge gaps. Focusing on grassland systems and species, we found 138 articles that met our criteria: 39 invertebrate, 97 vertebrate and 2 focussed on both vertebrate and invertebrate herbivores. Our study identified invertebrate focussed research, research conducted in the Southern Hemisphere and research on nondomesticated herbivores was significantly underrepresented based on our search and should be a focus of future research. Differences in study focus (trait response or trait effect), along with differences in the types of traits examined, led to limited opportunity for comparison between the two herbivore guilds. This review therefore predominantly discusses the response and effect of plant traits to each herbivore guild separately. In future studies, we suggest this review be used as a guide for trait selection, to improve comparability and the broader significance of results.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
5-23Subventions
Organisme : Australian Research Council
Informations de copyright
© 2023 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd.
Références
Ackerly, D.D., Dudley, S.A., Sultan, S.E., Schmitt, J., Coleman, J.S., Linder, C.R. et al. (2000) The evolution of plant ecophysiological traits: recent advances and future directions. BioScience, 50(11), 979-995. Available from: https://doi.org/10.1641/0006-3568(2000)050[0979:Teopet]2.0.Co;2
Agrawal, A.A. & Fishbein, M. (2006) Plant defense syndromes. Ecology, 87, S132-S149. https://doi.org/10.1890/0012-9658(2006)87[132:pds]2.0.co;2
Allegretti, L., Sartor, C., Paez Lama, S., Egea, V., Fucili, M. & Passera, C. (2012) Effect of the physiological state of Criollo goats on the botanical composition of their diet in NE Mendoza, Argentina. Small Ruminant Research, 103(2-3), 152-157. Available from: https://doi.org/10.1016/j.smallrumres.2011.09.018
Alvarenga, R., Auad, A.M., Moraes, J.C. & Silva, S.E. (2019) Do silicon and nitric oxide induce resistance to Mahanarva spectabilis (Hemiptera: Cercopidae) in forage grasses? Pest Management Science, 75(12), 3282-3292. Available from: https://doi.org/10.1002/ps.5450
Ameye, M., Allmann, S., Verwaeren, J., Smagghe, G., Haesaert, G., Schuurink, R.C. et al. (2018) Green leaf volatile production by plants: a meta-analysis. New Phytologist, 220(3), 666-683. Available from: https://doi.org/10.1111/nph.14671
Amiaud, B., Touzard, B., Bonis, A. & Bouzillé, J.-B. (2007) After grazing exclusion, is there any modification of strategy for two guerrilla species: Elymus repens (L.) Gould and Agrostis stolonifera (L.)? Plant Ecology, 197(1), 107-117. Available from: https://doi.org/10.1007/s11258-007-9364-z
An, H. & Li, G. (2014) Differential effects of grazing on plant functional traits in the desert grassland. Polish Journal of Ecology, 62(2), 239-251. Available from: https://doi.org/10.3161/104.062.0205
Andrew, N.R., Evans, M.J., Svejcar, L., Prendegast, K., Mata, L., Gibb, H. et al. (2022) What's hot and what's not-identifying publication trends in insect ecology. Austral Ecology, 47(1), 5-16. Available from: https://doi.org/10.1111/aec.13052
Axelrod, D.I. (1985) Rise of the grassland biome, central North America. The Botanical Review, 51(2), 163-201.
Baer, S.G., Kitchen, D.J., Blair, J.M. & Rice, C.W. (2002) Changes in ecosystem structure and function along a chronosequence of restored grasslands. Ecological Applications, 12(6), 1688-1701.
Bagella, S., Satta, A., Floris, I., Caria, M.C., Rossetti, I. & Podani, J. (2013) Effects of plant community composition and flowering phenology on honeybee foraging in M editerranean sylvo-pastoral systems. Applied Vegetation Science, 16(4), 689-697.
Baldwin, I.T., Kessler, A. & Halitschke, R. (2002) Volatile signaling in plant-plant-herbivore interactions: what is real? Current Opinion in Plant Biology, 5(4), 351-354. Available from: https://doi.org/10.1016/S1369-5266(02)00263-7
Baldwin, I.T. & Preston, C. (1999) The eco-physiological complexity of plant responses to insect herbivores. Planta, 203, 137-145. https://doi.org/10.1007/s004250050543
Bañuelos, M.J. & Obeso, J.R. (2000) Effect of grazing history, experimental defoliation, and genotype on patterns of silicification in Agrostis tenuis Sibth. Écoscience, 7(1), 45-50.
Barton, K.E. (2016) Tougher and thornier: general patterns in the induction of physical defence traits. Functional Ecology, 30(2), 181-187. Available from: https://doi.org/10.1111/1365-2435.12495
Bedoya-Pérez, M.A., Isler, I., Banks, P.B. & McArthur, C. (2014) Roles of the volatile terpene, 1,8-cineole, in plant-herbivore interactions: a foraging odor cue as well as a toxin. Oecologia, 174(3), 827-837. Available from: https://doi.org/10.1007/s00442-013-2801-x
De Bello, F., LEPŠ, J. & SEBASTIÀ, M.T. (2005) Predictive value of plant traits to grazing along a climatic gradient in the Mediterranean. Journal of Applied Ecology, 42(5), 824-833. Available from: https://doi.org/10.1111/j.1365-2664.2005.01079.x
Björkman, C., Dalin, P. & Ahrné, K. (2008) Leaf trichome responses to herbivory in willows: induction, relaxation and costs. New Phytologist, 179(1), 176-184.
Borer, E.T., Seabloom, E.W., Gruner, D.S., Harpole, W.S., Hillebrand, H., Lind, E.M. et al. (2014) Herbivores and nutrients control grassland plant diversity via light limitation. Nature, 508(7497), 517-520. Available from: https://doi.org/10.1038/nature13144
Bråthen, K.A., Pugnaire, F.I. & Bardgett, R.D. (2021) The paradox of forbs in grasslands and the legacy of the mammoth steppe. Frontiers in Ecology and the Environment, 19(10), 584-592. Available from: https://doi.org/10.1002/fee.2405
Briske, D.D. (1996) Strategies of plant survival in grazed systems: a functional interpretation. In: Hodgson, J. & Illius A.W. (Eds.), The ecology and management of grazing systems. Wallingford, United Kingdom: CAB International, pp. 3.
Briske, D.D. (1999) Plant traits determining grazing resistance: why have they proved so elusive? [People and rangelands building the future, vols 1 and 2]. In: VIth International Rangeland Congress, Jul 19-23, Townsville, Australia.
Briske, D.D., Boutton, T.W. & Wang, Z. (1996) Contribution of flexible allocation priorities to herbivory tolerance in C4 perennial grasses: an evaluation with 13C labeling. Oecologia, 105(2), 151-159. Available from: https://doi.org/10.1007/bf00328540
Capó, M., Roig-Oliver, M., Cardona, C., Cursach, J., Bartolomé, J., Rita, J. et al. (2021) Historic exposure to herbivores, not constitutive traits, explains plant tolerance to herbivory in the case of two Medicago species (Fabaceae). Plant Science, 307, 110890.
Carlucci, M.B., Brancalion, P.H.S., Rodrigues, R.R., Loyola, R. & Cianciaruso, M.V. (2020) Functional traits and ecosystem services in ecological restoration. Restoration Ecology, 28(6), 1372-1383. Available from: https://doi.org/10.1111/rec.13279
Carmona, D., Lajeunesse, M.J. & Johnson, M.T.J. (2011) Plant traits that predict resistance to herbivores. Functional Ecology, 25(2), 358-367.
Carson, W.P. & Root, R.B. (1999) Top-down effects of insect herbivores during early succession: influence on biomass and plant dominance. Oecologia, 121(2), 260-272. Available from: https://doi.org/10.1007/s004420050928
Chen, F., Tholl, D., D'Auria, J.C., Farooq, A., Pichersky, E. & Gershenzon, J. (2003) Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. The Plant Cell, 15(2), 481-494.
Christensen, S.A., Nemchenko, A., Borrego, E., Murray, I., Sobhy, I.S., Bosak, L. et al. (2013) The maize lipoxygenase, ZmLOX10, mediates green leaf volatile, jasmonate and herbivore-induced plant volatile production for defense against insect attack. The Plant Journal, 74(1), 59-73. Available from: https://doi.org/10.1111/tpj.12101
Clarke, D.A., York, P.H., Rasheed, M.A. & Northfield, T.D. (2017) Does biodiversity-ecosystem function literature neglect tropical ecosystems? Trends in Ecology & Evolution, 32(5), 320-323.
Coley, P.D., Bryant, J.P. & Chapin, III, F.S. (1985) Resource availability and plant antiherbivore defense. Science, 230(4728), 895-899.
Cook, G.D. & Dias, L. (2006) It was no accident: deliberate plant introductions by Australian government agencies during the 20th century. Australian Journal of Botany, 54(7), 601-625. Available from: https://doi.org/10.1071/BT05157
Cousins, S.A.O. & Eriksson, O. (2008) After the hotspots are gone: land use history and grassland plant species diversity in a strongly transformed agricultural landscape. Applied Vegetation Science, 11(3), 365-374.
Coverdale, T.C., McGeary, I.J., O'Connell, R.D., Palmer, T.M., Goheen, J.R., Sankaran, M. et al. (2019) Strong but opposing effects of associational resistance and susceptibility on defense phenotype in an African savanna plant. Oikos, 128(12), 1772-1782. Available from: https://doi.org/10.1111/oik.06644
Crawley, M.J. (2019) The relative importance of vertebrate and invertebrate herbivores in plant population dynamics. In: Bernays, E.A. (Ed.), Insect-plant interactions. Boca Raton, Florida, USA: CRC press, pp. 45-71.
Deák, B., Valkó, O., Nagy, D.D., Török, P., Torma, A., Lőrinczi, G. et al. (2020) Habitat islands outside nature reserves-threatened biodiversity hotspots of grassland specialist plant and arthropod species. Biological Conservation, 241, 108254.
Deraison, H., Badenhausser, I., Loeuille, N., Scherber, C. & Gross, N. (2015) Functional trait diversity across trophic levels determines herbivore impact on plant community biomass. Ecology Letters, 18(12), 1346-1355. Available from: https://doi.org/10.1111/ele.12529
Díaz, S., Lavorel, S., McIntyre, S., Falczuk, V., Casanoves, F., Milchunas, D.G. et al. (2007) Plant trait responses to grazing-a global synthesis. Global Change Biology, 13(2), 313-341. Available from: https://doi.org/10.1111/j.1365-2486.2006.01288.x
Díaz, S., Noy-Meir, I. & Cabido, M. (2001) Can grazing response of herbaceous plants be predicted from simple vegetative traits? Journal of Applied Ecology, 38(3), 497-508. Available from: https://doi.org/10.1046/j.1365-2664.2001.00635.x
Dixon, A.P., Faber-Langendoen, D., Josse, C., Morrison, J. & Loucks, C.J. (2014) Distribution mapping of world grassland types. Journal of Biogeography, 41(11), 2003-2019. Available from: https://doi.org/10.1111/jbi.12381
Dronova, I. & Taddeo, S. (2022) Remote sensing of phenology: towards the comprehensive indicators of plant community dynamics from species to regional scales. Journal of Ecology, 110(7), 1460-1484.
Effah, E., Barrett, D.P., Peterson, P.G., Godfrey, A., Potter, M.A., Holopainen, J.K. et al. (2020) Natural variation in volatile emissions of the invasive weed Calluna vulgaris in New Zealand. Plants (Basel, Switzerland), 9, 283. Available from: https://doi.org/10.3390/plants9020283
Egea, A.V., Allegretti, L., Paez Lama, S., Grilli, D., Sartor, C., Fucili, M. et al. (2014) Selective behavior of Creole goats in response to the functional heterogeneity of native forage species in the central Monte desert, Argentina. Small Ruminant Research, 120(1), 90-99. Available from: https://doi.org/10.1016/j.smallrumres.2014.04.005
Eggleton, P. (2020) The state of the world's insects. Annual Review of Environment and Resources, 45, 61-82.
Eisenhauer, N., Bonn, A. & A. Guerra, C. (2019) Recognizing the quiet extinction of invertebrates. Nature Communications, 10(1), 50. Available from: https://doi.org/10.1038/s41467-018-07916-1
Eisenring, M., Glauser, G., Meissle, M. & Romeis, J. (2018) Differential impact of herbivores from three feeding guilds on systemic secondary metabolite induction, phytohormone levels and plant-mediated herbivore interactions. Journal of Chemical Ecology, 44(12), 1178-1189. Available from: https://doi.org/10.1007/s10886-018-1015-4
Firn, J., Schütz, M., Nguyen, H. & Risch, A.C. (2017) Herbivores sculpt leaf traits differently in grasslands depending on life form and land-use histories. Ecology, 98(1), 239-252. Available from: https://doi.org/10.1002/ecy.1637
Freeman, R.S., Brody, A.K. & Neefus, C.D. (2003) Flowering phenology and compensation for herbivory in Ipomopsis aggregata. Oecologia, 136(3), 394-401. Available from: https://doi.org/10.1007/s00442-003-1276-6
Frier, D.J.P., Hernández, S.C.V. & Tiessen, A. (2012) Friend or foe? Exploring the factors that determine the difference between positive and negative effects on photosynthesis in response to insect herbivory. In: Najafpour M.M. (Ed.), Artificial photosynthesis. Rijeka, Croatia: InTech, pp. 155-206.
Funk, J.L., Larson, J.E., Ames, G.M., Butterfield, B.J., Cavender-Bares, J., Firn, J. et al. (2017) Revisiting the Holy Grail: using plant functional traits to understand ecological processes. Biological Reviews, 92(2), 1156-1173. Available from: https://doi.org/10.1111/brv.12275
Göldel, B., Araujo, A.C., Kissling, W.D. & Svenning, J.C. (2016) Impacts of large herbivores on spinescence and abundance of palms in the Pantanal, Brazil. Botanical Journal of the Linnean Society, 182(2), 465-479. Available from: https://doi.org/10.1111/boj.12420
Grime, J.P. (1998) Benefits of plant diversity to ecosystems: immediate, filter and founder effects. Journal of Ecology, 86(6), 902-910. Available from: https://doi.org/10.1046/j.1365-2745.1998.00306.x
Habel, J.C., Dengler, J., Janišová, M., Török, P., Wellstein, C. & Wiezik, M. (2013) European grassland ecosystems: threatened hotspots of biodiversity. Biodiversity and Conservation, 22(10), 2131-2138.
Hall, C.R., Waterman, J.M., Vandegeer, R.K., Hartley, S.E. & Johnson, S.N. (2019) The role of silicon in antiherbivore phytohormonal signalling. Frontiers in Plant Science, 10, 1132.
Hamann, E., Blevins, C., Franks, S.J., Jameel, M.I. & Anderson, J.T. (2021) Climate change alters plant-herbivore interactions. New Phytologist, 229(4), 1894-1910. Available from: https://doi.org/10.1111/nph.17036
Hanley, M.E., Shannon, R.W.R., Lemoine, D.G., Sandey, B., Newland, P.L. & Poppy, G.M. (2018) Riding on the wind: volatile compounds dictate selection of grassland seedlings by snails. Annals of Botany, 122(6), 1075-1083. Available from: https://doi.org/10.1093/aob/mcy190
Hjältén, J., Danell, K., Ericson, L. & Hjalten, J. (1996) Food selection by two vole species in relation to plant growth strategies and plant chemistry. Oikos, 76(1), 181-190. Available from: https://doi.org/10.2307/3545760
Hodgson, J.G., Wilson, P.J., Hunt, R., Grime, J.P. & Thompson, K. (1999) Allocating CSR plant functional types: a soft approach to a hard problem. Oikos, 85, 282-294.
Hughes, B.B., Beas-Luna, R., Barner, A.K., Brewitt, K., Brumbaugh, D.R., Cerny-Chipman, E.B. et al. (2017) Long-term studies contribute disproportionately to ecology and policy. BioScience, 67(3), 271-281. Available from: https://doi.org/10.1093/biosci/biw185
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. Available from: https://doi.org/10.3389/fpls.2014.00478
Hulme, P.E. (1996) Herbivores and the performance of grassland plants: a comparison of arthropod, mollusc and rodent herbivory. The Journal of Ecology, 84, 43-51.
Hulshof, C.M., Violle, C., Spasojevic, M.J., McGill, B., Damschen, E., Harrison, S. et al. (2013) Intra-specific and inter-specific variation in specific leaf area reveal the importance of abiotic and biotic drivers of species diversity across elevation and latitude. Journal of Vegetation Science, 24(5), 921-931. Available from: https://doi.org/10.1111/jvs.12041
Ibanez, S., Lavorel, S., Puijalon, S. & Moretti, M. (2013) Herbivory mediated by coupling between biomechanical traits of plants and grasshoppers. Functional Ecology, 27(2), 479-489. Available from: https://doi.org/10.1111/1365-2435.12058
Irving, L. (2015) Carbon assimilation, biomass partitioning and productivity in grasses. Agriculture (London), 5(4), 1116-1134. https://www.mdpi.com/2077-0472/5/4/1116
Johnson, M.T.J., Campbell, S.A. & Barrett, S.C.H. (2015) Evolutionary interactions between plant reproduction and defense against herbivores. Annual Review of Ecology, Evolution, and Systematics, 46(1), 191-213. Available from: https://doi.org/10.1146/annurev-ecolsys-112414-054215
Jones, A.S., Lamont, B.B., Fairbanks, M.M. & Rafferty, C.M. (2003) Kangaroos avoid eating seedlings with or near others with volatile essential oils. Journal of Chemical Ecology, 29(12), 2621-2635. Available from: https://doi.org/10.1023/b:Joec.0000008008.91498.62
Kempel, A., Razanajatovo, M., Stein, C., Unsicker, S.B., Auge, H., Weisser, W.W. et al. (2015) Herbivore preference drives plant community composition. Ecology, 96(11), 2923-2934. Available from: https://doi.org/10.1890/14-2125.1
Kessler, A. & Baldwin, I.T. (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science, 291(5511), 2141-2144.
Kigathi, R.N., Unsicker, S.B., Reichelt, M., Kesselmeier, J., Gershenzon, J. & Weisser, W.W. (2009) Emission of volatile organic compounds after herbivory from Trifolium pratense (L.) under laboratory and field conditions. Journal of Chemical Ecology, 35(11), 1335-1348. Available from: https://doi.org/10.1007/s10886-009-9716-3
Knappová, J., Židlická, D., Kadlec, T., Knapp, M., Haisel, D., Hadincová, V. et al. (2018) Population differentiation related to climate of origin affects the intensity of plant-herbivore interactions in a clonal grass. Basic and Applied Ecology, 28, 76-86. Available from: https://doi.org/10.1016/j.baae.2018.02.011
Kotanen, P.M. & Rosenthal, J.P. (2000) Tolerating herbivory: does the plant care if the herbivore has a backbone. Evolutionary Ecology, 14(4-6), 537-549. Available from: https://doi.org/10.1023/A:1010862201331
Landsberg, J., Lavorel, S. & Stol, J. (1999) Grazing response groups among understorey plants in arid rangelands. Journal of Vegetation Science, 10(5), 683-696.
Lau, J.A., Strengbom, J., Stone, L.R., Reich, P.B. & Tiffin, P. (2008) Direct and indirect effects of CO2, nitrogen, and community diversity on plant-enemy interactions. Ecology, 89(1), 226-236. Available from: https://doi.org/10.1890/07-0423.1
Lavorel, S. & Garnier, E. (2002) Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Functional Ecology, 16(5), 545-556. Available from: https://doi.org/10.1046/j.1365-2435.2002.00664.x
Lavorel, S., Storkey, J., Bardgett, R.D., de Bello, F., Berg, M.P., Le Roux, X. et al. (2013) A novel framework for linking functional diversity of plants with other trophic levels for the quantification of ecosystem services. Journal of Vegetation Science, 24(5), 942-948. Available from: https://doi.org/10.1111/jvs.12083
Lemaire, G., Wilkins, R. & Hodgson, J. (2005) Challenges for grassland science: managing research priorities. Agriculture, Ecosystems & Environment, 108(2), 99-108. Available from: https://doi.org/10.1016/j.agee.2005.01.003
Lemoine, N.P., Doublet, D., Salminen, J.-P., Burkepile, D.E. & Parker, J.D. (2017) Responses of plant phenology, growth, defense, and reproduction to interactive effects of warming and insect herbivory. Ecology, 98(7), 1817-1828. Available from: https://doi.org/10.1002/ecy.1855
Lind, E.M., Borer, E., Seabloom, E., Adler, P., Bakker, J.D., Blumenthal, D.M. et al. (2013) Life-history constraints in grassland plant species: a growth-defence trade-off is the norm. Ecology Letters, 16(4), 513-521.
Lindenmayer, D.B., Likens, G.E., Andersen, A., Bowman, D., Bull, C.M., Burns, E. et al. (2012) Value of long-term ecological studies. Austral Ecology, 37(7), 745-757. Available from: https://doi.org/10.1111/j.1442-9993.2011.02351.x
Loranger, J., Meyer, S.T., Shipley, B., Kattge, J., Loranger, H., Roscher, C. et al. (2012) Predicting invertebrate herbivory from plant traits: evidence from 51 grassland species in experimental monocultures. Ecology, 93(12), 2674-2682.
Lunt, I.D., Eldridge, D.J., Morgan, J.W. & Witt, G.B. (2007) A framework to predict the effects of livestock grazing and grazing exclusion on conservation values in natural ecosystems in Australia. Australian Journal of Botany, 55(4), 401-415. Available from: https://doi.org/10.1071/BT06178
Mäntylä, E., Alessio, G.A., Blande, J.D., Heijari, J., Holopainen, J.K., Laaksonen, T. et al. (2008) From plants to birds: higher avian predation rates in trees responding to insect herbivory. PLoS One, 3(7), e2832. Available from: https://doi.org/10.1371/journal.pone.0002832
Maron, J.L., Agrawal, A.A. & Schemske, D.W. (2019) Plant-herbivore coevolution and plant speciation. Ecology, 100(7), e02704. Available from: https://doi.org/10.1002/ecy.2704
Marsh, K.J., Wallis, I.R., Kulheim, C., Clark, R., Nicolle, D., Foley, W.J. et al. (2020) New approaches to tannin analysis of leaves can be used to explain in vitro biological activities associated with herbivore defence. New Phytologist, 225(1), 488-498. Available from: https://doi.org/10.1111/nph.16117
de Mazancourt, C., Loreau, M. & Abbadie, L. (1998) Grazing optimization and nutrient cycling: when do herbivores enhance plant production? Ecology, 79(7), 2242-2252. Available from: https://doi.org/10.1890/0012-9658(1998)079[2242:GOANCW]2.0.CO;2
McNaughton, S. & Sabuni, G. (1988) Large African mammals as regulators of vegetation structure. In: Werger, M.J.A., van der Aart, P.J.M., During, H.J. & Verhoeven J.T.A. (Eds.), Plant form and vegetation structure. The Hague, Netherlands: SPB Academic Publishing, pp. 339-354.
McNaughton, S.J. (1984) Grazing lawns: animals in herds, plant form, and coevolution. The American Naturalist, 124(6), 863-886.
Moles, A.T., Peco, B., Wallis, I.R., Foley, W.J., Poore, A.G.B., Seabloom, E.W. (2013) Correlations between physical and chemical defences in plants: tradeoffs, syndromes, or just many different ways to skin a herbivorous cat? New Phytologist, 198, 252-263. https://doi.org/10.1111/nph.12116
Muchlinski, A., Chen, X., Lovell, J.T., Köllner, T.G., Pelot, K.A., Zerbe, P. et al. (2019) Biosynthesis and emission of stress-induced volatile terpenes in roots and leaves of switchgrass (Panicum virgatum L.). Frontiers in Plant Science, 10, 1144. Available from: https://doi.org/10.3389/fpls.2019.01144
Nabity, P.D., Zavala, J.A. & DeLucia, E.H. (2008) Indirect suppression of photosynthesis on individual leaves by arthropod herbivory. Annals of Botany, 103(4), 655-663. Available from: https://doi.org/10.1093/aob/mcn127
Noy-Meir, I., Gutman, M. & Kaplan, Y. (1989) Responses of Mediterranean grassland plants to grazing and protection. The Journal of Ecology, 77, 290-310.
Núñez-Farfán, J., Fornoni, J. & Valverde, P.L. (2007) The evolution of resistance and tolerance to herbivores. Annual Review of Ecology, Evolution, and Systematics, 38, 541-566.
Oduor, A.M.O., Gómez, J.M. & Strauss, S.Y. (2010) Exotic vertebrate and invertebrate herbivores differ in their impacts on native and exotic plants: a meta-analysis. Biological Invasions, 12(2), 407-419. Available from: https://doi.org/10.1007/s10530-009-9622-1
Paige, K.N. (1992) Overcompensation in response to mammalian herbivory: from mutulastic to antagonistic interactions. Ecology, 73(6), 2076-2085. Available from: https://doi.org/10.2307/1941456
Peisley, R.K., Saunders, M.E. & Luck, G.W. (2015) A systematic review of the benefits and costs of bird and insect activity in agroecosystems. Springer Science Reviews, 3, 113-125.
Pérez-Harguindeguy, N., Díaz, S., Garnier, E., Lavorel, S., Poorter, H., Jaureguiberry, P. et al. (2016) Corrigendum to: new handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany, 64(8), 715-716.
Peterson, R.K.D., Higley, L.G., Haile, F.J. & Barrigossi, J.A.F. (1998) Mexican bean beetle (Coleoptera: Coccinellidae) injury affects photosynthesis of Glycine max and Phaseolus vulgaris. Environmental Entomology, 27(2), 373-381. Available from: https://doi.org/10.1093/ee/27.2.373
Petit Bon, M., Inga, K.G., Utsi, T.A., Jónsdóttir, I.S. & Bråthen, K.A. (2022) Forage quality in tundra grasslands under herbivory: silicon-based defences, nutrients and their ratios in grasses. Journal of Ecology, 110(1), 129-143.
Rasmann, S., Agrawal, A.A., Cook, S.C. & Erwin, A.C. (2009) Cardenolides, induced responses, and interactions between above- and belowground herbivores of milkweed (Asclepias spp.). Ecology, 90(9), 2393-2404. Available from: https://doi.org/10.1890/08-1895.1
Rawal, D.S., Kasel, S., Keatley, M.R. & Nitschke, C.R. (2015) Environmental effects on germination phenology of co-occurring eucalypts: implications for regeneration under climate change. International Journal of Biometeorology, 59, 1237-1252.
Ribeiro, S.P., Londe, V., Bueno, A.P., Barbosa, J.S., Corrêa, T.L., Soeltl, T. et al. (2017) Plant defense against leaf herbivory based on metal accumulation: examples from a tropical high altitude ecosystem. Plant Species Biology, 32(2), 147-155. Available from: https://doi.org/10.1111/1442-1984.12136
Risch, A.C., Haynes, A.G., Busse, M.D., Filli, F. & Schütz, M. (2013) The response of soil CO2 fluxes to progressively excluding vertebrate and invertebrate herbivores depends on ecosystem type. Ecosystems, 16, 1192-1202.
Risch, A.C., Ochoa-Hueso, R., van der Putten, W.H., Bump, J.K., Busse, M.D., Frey, B. et al. (2018) Size-dependent loss of aboveground animals differentially affects grassland ecosystem coupling and functions. Nature Communications, 9(1), 3684.
Roohigohar, S., Clarke, A.R., Strutt, F., van der Burg, C.A. & Prentis, P.J. (2022) Fruit fly larval survival in picked and unpicked tomato fruit of differing ripeness and associated gene expression patterns. Insects, 13(5), 451. https://www.mdpi.com/2075-4450/13/5/451
Sala, O.E., Oesterheld, M., León, R.J.C. & Soriano, A. (1986) Grazing effects upon plant community structure in subhumid grasslands of Argentina. Vegetatio, 67, 27-32.
Salminen, J.-P. & Karonen, M. (2011) Chemical ecology of tannins and other phenolics: we need a change in approach. Functional Ecology, 25(2), 325-338. Available from: https://doi.org/10.1111/j.1365-2435.2010.01826.x
Santos, J.C., Alves-Silva, E., Cornelissen, T.G. & Fernandes, G.W. (2013) The effect of fluctuating asymmetry and leaf nutrients on gall abundance and survivorship. Basic and Applied Ecology, 14(6), 489-495. Available from: https://doi.org/10.1016/j.baae.2013.06.005
Saunders, M.E. (2018) Ecosystem services in agriculture: understanding the multifunctional role of invertebrates. Agricultural and Forest Entomology, 20(2), 298-300. Available from: https://doi.org/10.1111/afe.12248
Sayre, R., Karagulle, D., Frye, C., Boucher, T., Wolff, N.H., Breyer, S. et al. (2020) An assessment of the representation of ecosystems in global protected areas using new maps of world climate regions and world ecosystems. Global Ecology and Conservation, 21, e00860. Available from: https://doi.org/10.1016/j.gecco.2019.e00860
Scholtz, R. & Twidwell, D. (2022) The last continuous grasslands on earth: identification and conservation importance. Conservation Science and Practice, 4(3), e626. Available from: https://doi.org/10.1111/csp2.626
Scurlock, J.M.O. & Hall, D.O. (1998) The global carbon sink: a grassland perspective. Global Change Biology, 4(2), 229-233.
Shen, H., Dong, S., Li, S., Xiao, J., Han, Y., Yang, M. et al. (2019) Grazing enhances plant photosynthetic capacity by altering soil nitrogen in alpine grasslands on the Qinghai-Tibetan plateau. Agriculture, Ecosystems & Environment, 280, 161-168. Available from: https://doi.org/10.1016/j.agee.2019.04.029
Simon, M.F., Grether, R., de Queiroz, L.P., Skema, C., Pennington, R.T. & Hughes, C.E. (2009) Recent assembly of the Cerrado, a neotropical plant diversity hotspot, by in situ evolution of adaptations to fire. Proceedings of the National Academy of Sciences, 106(48), 20359-20364.
Stutz, R.S., Banks, P.B., Proschogo, N. & McArthur, C. (2016) Follow your nose: leaf odour as an important foraging cue for mammalian herbivores. Oecologia, 182(3), 643-651. Available from: https://doi.org/10.1007/s00442-016-3678-2
Suding, K.N., Lavorel, S., Chapin, iii, F.S., Cornelissen, J.H.C., Díaz, S., Garnier, E. et al. (2008) Scaling environmental change through the community-level: a trait-based response-and-effect framework for plants. Global Change Biology, 14(5), 1125-1140. Available from: https://doi.org/10.1111/j.1365-2486.2008.01557.x
Thomson, V.P., Cunningham, S.A., Ball, M.C. & Nicotra, A.B. (2003) Compensation for herbivory by Cucumis sativus through increased photosynthetic capacity and efficiency. Oecologia, 134(2), 167-175. Available from: https://doi.org/10.1007/s00442-002-1102-6
Tian, D., Tooker, J., Peiffer, M., Chung, S.H. & Felton, G.W. (2012) Role of trichomes in defense against herbivores: comparison of herbivore response to woolly and hairless trichome mutants in tomato (Solanum lycopersicum). Planta, 236(4), 1053-1066. Available from: https://doi.org/10.1007/s00425-012-1651-9
Tscharntke, T. & Greiler, H.-J. (1995) Insect communities, grasses, and grasslands. Annual Review of Entomology, 40(1), 535-558.
Umina, P.A., Kemp, S., Babineau, M., Maino, J.L., Roberts, I., Govender, A. et al. (2021) Pests of Australian dairy pastures: distribution, seasonality and potential impacts on pasture production. Austral Entomology, 60(4), 763-781.
Velikova, V., Salerno, G., Frati, F., Peri, E., Conti, E., Colazza, S. et al. (2010) Influence of feeding and oviposition by phytophagous pentatomids on photosynthesis of herbaceous plants. Journal of Chemical Ecology, 36(6), 629-641. Available from: https://doi.org/10.1007/s10886-010-9801-7
Villalba, J.J., Provenza, F.D., Hall, J.O. & Lisonbee, L.D. (2010) Selection of tannins by sheep in response to gastrointestinal nematode infection. Journal of Animal Science, 88(6), 2189-2198. Available from: https://doi.org/10.2527/jas.2009-2272
Vivaldo, G., Masi, E., Taiti, C., Caldarelli, G. & Mancuso, S. (2017) The network of plants volatile organic compounds. Scientific Reports, 7(1), 11050. Available from: https://doi.org/10.1038/s41598-017-10975-x
De Vries, F.T., Van Groenigen, J.W., Hoffland, E. & Bloem, J. (2011) Nitrogen losses from two grassland soils with different fungal biomass. Soil Biology and Biochemistry, 43(5), 997-1005.
Wakatsuki, Y., Nishizawa, K. & Mori, A.S. (2021) Leaf trait variability explains how plant community composition changes under the intense pressure of deer herbivory. Ecological Research, 36(3), 521-532. Available from: https://doi.org/10.1111/1440-1703.12224
Wari, D., Kabir, M.A., Mujiono, K., Hojo, Y., Shinya, T., Tani, A. et al. (2019) Honeydew-associated microbes elicit defense responses against brown planthopper in rice. Journal of Experimental Botany, 70(5), 1683-1696. Available from: https://doi.org/10.1093/jxb/erz041
Weidlich, E.W.A., Flórido, F.G., Sorrini, T.B. & Brancalion, P.H.S. (2020) Controlling invasive plant species in ecological restoration: a global review. Journal of Applied Ecology, 57(9), 1806-1817. Available from: https://doi.org/10.1111/1365-2664.13656
Weiher, E., Van Der Werf, A., Thompson, K., Roderick, M., Garnier, E. & Eriksson, O. (1999) Challenging Theophrastus: a common core list of plant traits for functional ecology. Journal of Vegetation Science, 10(5), 609-620.
White, R., Murray, S. & Rohweder, M. (2000) Pilot analysis of global ecosystems: grassland ecosystems technical report, Washington, DC. https://files.wri.org/d8/s3fs-public/pdf/page_grasslands.pdf
Whitworth-Hulse, J.I., Cingolani, A.M., Zeballos, S.R., Poca, M. & Gurvich, D.E. (2016) Does grazing induce intraspecific trait variation in plants from a sub-humid mountain ecosystem? Austral Ecology, 41(7), 745-755. Available from: https://doi.org/10.1111/aec.12361
Wilson, K.A., Auerbach, N.A., Sam, K., Magini, A.G., Moss, A.S.L., Langhans, S.D. et al. (2016) Conservation research is not happening where it is most needed. PLoS Biology, 14(3), e1002413. Available from: https://doi.org/10.1371/journal.pbio.1002413
Winkler, K., Fuchs, R., Rounsevell, M. & Herold, M. (2021) Global land use changes are four times greater than previously estimated. Nature Communications, 12(1), 2501. Available from: https://doi.org/10.1038/s41467-021-22702-2
Woodward, A. & Coppock, D.L. (1995) Role of plant defense in the utilization of native browse in southern Ethiopia. Agroforestry Systems, 32, 147-161.
Wray, J.C. & Elle, E. (2015) Flowering phenology and nesting resources influence pollinator community composition in a fragmented ecosystem. Landscape Ecology, 30, 261-272.
Wright, I.J., Reich, P.B., Westoby, M., Ackerly, D.D., Baruch, Z., Bongers, F. et al. (2004) The worldwide leaf economics spectrum. Nature, 428(6985), 821-827. Available from: https://doi.org/10.1038/nature02403
Young, T.P. (1987) Increased thorn length in Acacia depranolobium-an induced response to browsing. Oecologia, 71(3), 436-438.
Zalucki, M.P., Malcolm, S.B., Paine, T.D., Hanlon, C.C., Brower, L.P. & Clarke, A.R. (2001) It's the first bites that count: survival of first-instar monarchs on milkweeds. Austral Ecology, 26(5), 547-555. Available from: https://doi.org/10.1046/j.1442-9993.2001.01132.x
Zhang, R., Zhang, W., Zuo, Z., Li, R., Wu, J. & Gao, Y. (2014) Inhibition effects of volatile organic compounds from Artemisia frigida Willd. on the pasture grass intake by lambs. Small Ruminant Research, 121(2-3), 248-254. Available from: https://doi.org/10.1016/j.smallrumres.2014.06.001
Zhu, F., Heinen, R., van der Sluijs, M., Raaijmakers, C., Biere, A. & Bezemer, T.M. (2018) Species-specific plant-soil feedbacks alter herbivore-induced gene expression and defense chemistry in Plantago lanceolata. Oecologia, 188(3), 801-811. Available from: https://doi.org/10.1007/s00442-018-4245-9
Züst, T. & Agrawal, A.A. (2017) Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis. Annual Review of Plant Biology, 68(1), 513-534.