Plant palatability and trait responses to experimental warming.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
29 06 2020
Historique:
received: 13 08 2019
accepted: 08 06 2020
entrez: 1 7 2020
pubmed: 1 7 2020
medline: 15 12 2020
Statut: epublish

Résumé

Climate warming is expected to significantly affect plant-herbivore interactions. Even though direct effects of temperature on herbivores were extensively studied, indirect effects of temperature (acting via changes in host plant quality) on herbivore performance have rarely been addressed. We conducted multiple-choice feeding experiments with generalist herbivore Schistocerca gregaria feeding on six species of genus Impatiens cultivated at three different temperatures in growth chambers and a common garden. We also studied changes in leaf morphology and chemistry. We tested effects of temperature on plant palatability and assessed whether the effects could be explained by changes in the leaf traits. The leaves of most Impatiens species experienced the highest herbivory when cultivated at the warmest temperature. Traits related to leaf morphology (specific leaf area, leaf dry matter content and leaf area), but not to leaf chemistry, partly mediated the effects of temperature on plant palatability. Herbivores preferred smaller leaves with lower specific leaf area and higher leaf dry matter content. Our study suggests that elevated temperature will lead to changes in leaf traits and increase their palatability. This might further enhance the levels of herbivory under the increased herbivore pressure, which is forecasted as a consequence of climate warming.

Identifiants

pubmed: 32601471
doi: 10.1038/s41598-020-67437-0
pii: 10.1038/s41598-020-67437-0
pmc: PMC7324391
doi:

Banques de données

figshare
['10.6084/m9.figshare.9438722.v1']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

10526

Références

Ali, J. G. & Agrawal, A. A. Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci. 17, 293–302 (2012).
pubmed: 22425020
Maron, J. L. & Crone, E. Herbivory: Effects on plant abundance, distribution and population growth. Proc. R. Soc. B Biol. Sci. 273, 2575–2584 (2006).
Pachauri, R. K. et al. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. (IPCC, 2014).
Robinet, C. & Roques, A. Direct impacts of recent climate warming on insect populations. Integr. Zool. 5, 132–142 (2010).
pubmed: 21392331
Lemoine, N. P., Drews, W. A., Burkepile, D. E. & Parker, J. D. Increased temperature alters feeding behavior of a generalist herbivore. Oikos 122, 1669–1678 (2013).
Lemoine, N. P., Burkepile, D. E. & Parker, J. D. Variable effects of temperature on insect herbivory. PeerJ 2, e376 (2014).
pubmed: 24860701 pmcid: 4017821
Bale, J. S. et al. Herbivory in global climate change research: Direct effects of rising temperature on insect herbivores. Glob. Change Biol. 8, 1–16 (2002).
Dostálek, T., Rokaya, M. B. & Münzbergová, Z. Altitude, habitat type and herbivore damage interact in their effects on plant population dynamics. PLoS ONE 13, e0209149 (2018).
pubmed: 30557339 pmcid: 6296709
Descombes, P., Kergunteuil, A., Glauser, G., Rasmann, S. & Pellissier, L. Plant physical and chemical traits associated with herbivory in situ and under a warming treatment. J. Ecol. 108, 733–749 (2020).
Bidart-Bouzat, M. G. & Imeh-Nathaniel, A. Global change effects on plant chemical defenses against insect herbivores. J. Integr. Plant Biol. 50, 1339–1354 (2008).
pubmed: 19017122
Pellissier, L., Roger, A., Bilat, J. & Rasmann, S. High elevation Plantago lanceolata plants are less resistant to herbivory than their low elevation conspecifics: Is it just temperature?. Ecography 37, 950–959 (2014).
Dostálek, T. et al. Trade-off among different anti-herbivore defence strategies along an altitudinal gradient. AoB Plants 8, plw026 (2016).
pubmed: 27169609 pmcid: 4940502
Knappová, J. et al. Population differentiation related to climate of origin affects the intensity of plant–herbivore interactions in a clonal grass. Basic Appl. Ecol. 28, 76–86 (2018).
Mason, C. M. et al. Macroevolution of leaf defenses and secondary metabolites across the genus Helianthus. New Phytol. 209, 1720–1733 (2016).
pubmed: 26583880
Reich, P. B. & Oleksyn, J. Global patterns of plant leaf N and P in relation to temperature and latitude. Proc. Natl. Acad. Sci. 101, 11001–11006 (2004).
pubmed: 15213326
Backhaus, S., Wiehl, D., Beierkuhnlein, C., Jentsch, A. & Wellstein, C. Warming and drought do not influence the palatability of Quercus pubescens Willd leaves of four European provenances. Arthropod-Plant Interact. 8, 329–337 (2014).
Zhang, P. et al. Effects of rising temperature on the growth, stoichiometry, and palatability of aquatic plants. Front. Plant Sci. 9, 8 (2019).
Bossdorf, O. et al. Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144, 1–11 (2005).
pubmed: 15891837
Núñez-Farfán, J. & Schlichting, C. D. Evolution in changing environments: The ‘Synthetic’ work of Clausen, Keck, and Hiesey. Q. Rev. Biol. 76, 433–457 (2001).
pubmed: 11783397
Münzbergová, Z. & Skuhrovec, J. Effect of habitat conditions and plant traits on leaf damage in the carduoideae subfamily. PLoS ONE 8, e64639 (2013).
pubmed: 23717643 pmcid: 3661506
Kuglerová, M., Skuhrovec, J. & Münzbergová, Z. Relative importance of drought, soil quality, and plant species in determining the strength of plant–herbivore interactions. Ecol. Entomol. 44, 665–677 (2019).
Rathinasabapathi, B. et al. Arsenic hyperaccumulation in the Chinese brake fern (Pteris vittata) deters grasshopper (Schistocerca americana) herbivory. New Phytol. 175, 363–369 (2007).
pubmed: 17587384
Akiyama, S. & Ohba, H. Studies of impatiens (Balsaminaceae) of Nepal 3. Impatiens scabrida and Allied species. Bull. Natl. Mus. Nat. Sci. Ser. B Bot. 42, 121–130 (2016).
Press, J. R., Shrestha, K. K. & Sutton, D. A. Annotated checklist of the flowering plants of Nepal (The Natural History Museum, London, 2000).
Gruntman, M., Segev, U., Glauser, G. & Tielbörger, K. Evolution of plant defences along an invasion chronosequence: Defence is lost due to enemy release—but not forever. J. Ecol. 105, 255–264 (2017).
Najberek, K., Solarz, W. & Chmura, D. Do local enemies attack alien and native impatiens alike?. Acta Soc. Bot. Pol. 86, 20 (2017).
Suzuki, M. et al. Flowering phenology and survival of two annual plants Impatiens noli-tangere and Persicaria thunbergii co-occurring in streamside environments. Ecol. Res. 22, 496–501 (2007).
Laube, J., Sparks, T. H., Bässler, C. & Menzel, A. Small differences in seasonal and thermal niches influence elevational limits of native and invasive Balsams. Biol. Conserv. 191, 682–691 (2015).
Adamowski, W. Impatiens balfourii as an emerging invader in Europe. in Biological Invasions: Towards a Synthesis, Proceedings (eds. Pysek, P. & Pergl, J.) vol. 8 183–194 (Institut Ecology Tu Berlin, 2009).
Čuda, J., Skálová, H., Janovský, Z. & Pyšek, P. Habitat requirements, short-term population dynamics and coexistence of native and invasive Impatiens species: A field study. Biol. Invasions 16, 177–190 (2014).
Čuda, J. et al. Invasive herb Impatiens glandulifera has minimal impact on multiple components of temperate forest ecosystem function. Biol. Invasions 19, 3051–3066 (2017).
Florianová, A. & Münzbergová, Z. Drivers of natural spread of invasive Impatiens parviflora differ between life-cycle stages. Biol. Invasions 20, 2121–2140 (2018).
Rokaya, M. B., Dostálek, T. & Münzbergová, Z. Plant-herbivore interactions along elevational gradient: Comparison of field and common garden data. Acta Oecol. 77, 168–175 (2016).
Veselá, A., Dostálek, T., Rokaya, M. & Münzbergová, Z. Seed mass and plant origin interact to determine species germination patterns. bioRxiv https://doi.org/10.1101/841114 (2019).
doi: 10.1101/841114
Tatebe, H. et al. The initialization of the MIROC climate models with hydrographic data assimilation for decadal prediction. J. Meteorol. Soc. Jpn. 90A, 275–294 (2012).
Aryal, A. et al. Predicting the distributions of predator (snow leopard) and prey (blue sheep) under climate change in the Himalaya. Ecol. Evol. 6, 4065–4075 (2016).
pubmed: 27516864 pmcid: 4875782
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).
Grime, J. P., Cornelissen, J., Hans, H. C., Thompson, K. & Hodgson, J. G. Evidence of a causal connection between anti-herbivore defence and the decomposition rate of leaves. Oikos 77, 489–494 (1996).
Joern, A. & Mole, S. The plant stress hypothesis and variable responses by blue grama grass (Bouteloua gracilis) to water, mineral nitrogen, and insect herbivory. J. Chem. Ecol. 31, 2069–2090 (2005).
pubmed: 16132213
Kautz, S., Trisel, J. A. & Ballhorn, D. J. Jasmonic acid enhances plant cyanogenesis and resistance to herbivory in lima bean. J. Chem. Ecol. 40, 1186–1196 (2014).
pubmed: 25399357
Massey, F. P., Ennos, A. R. & Hartley, S. E. Silica in grasses as a defence against insect herbivores: Contrasting effects on folivores and a phloem feeder. J. Anim. Ecol. 75, 595–603 (2006).
pubmed: 16638012
Mainguet, A. M., Louveaux, A., Sayed, G. E. & Rollin, P. Ability of a generalist insect, Schistocerca gregaria, to overcome thioglucoside defense in desert plants: tolerance or adaptation?. Entomol. Exp. Appl. 94, 309–317 (2000).
Bernays, E. A. & Lewis, A. C. The effect of wilting on palatability of plants to Schistocerca gregaria, the desert locust. Oecologia 70, 132–135 (1986).
pubmed: 28311298
McLeod, A. R., Rey, A., Newsham, K. K., Lewis, G. C. & Wolferstan, P. Effects of elevated ultraviolet radiation and endophytic fungi on plant growth and insect feeding in Lolium perenne, Festuca rubra, F. arundinacea and F. pratensis. J. Photochem. Photobiol. B 62, 97–107 (2001).
pubmed: 11693372
Kempel, A., Schädler, M., Chrobock, T., Fischer, M. & van Kleunen, M. Tradeoffs associated with constitutive and induced plant resistance against herbivory. Proc. Natl. Acad. Sci. 108, 5685–5689 (2011).
pubmed: 21389269
Fraser, L. H. & Grime, J. P. Interacting effects of herbivory and fertility on a synthesized plant community. J. Ecol. 87, 514–525 (1999).
Ehrenberger, F. & Gorbach, S. Methoden der organischen Elementar- und Spurenanalyse (Verlag Chemie, Weinhiem, 1973).
Olsen, S. R. & Dean, L. A. Phosphorus. in Page AL (ed): Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties (viz Pánková et al. 2008) 1035–1049 (1982).
Andrew, N. R. & Hughes, L. Herbivore damage along a latitudinal gradient: Relative impacts of different feeding guilds. Oikos 108, 176–182 (2005).
R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (ISBN 3–900051–07–0, 2015).
Crawley, M. J. Statistical computingan introduction to data analysis using S-Plus. (Wiley, 2002).
Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest Package: Tests in linear mixed effects models. J. Stat. Softw. 82, 2 (2017).
Naimi, B. usdm: Uncertainty analysis for species distribution models. R Package Version 1, 1–12 (2015).
Zuur, A. F., Ieno, E. N. & Elphick, C. S. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1, 3–14 (2010).
Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (Springer, Berlin, 2002). https://doi.org/10.1007/b97636
Barton, K. Package ‘MuMIn’. Model selection and model averaging base on information criteria. R package version 3.2. 3. (Vienna: R Foundation for Statistical Computing, 2016).
Zvereva, E. L. & Kozlov, M. V. Consequences of simultaneous elevation of carbon dioxide and temperature for plant–herbivore interactions: a metaanalysis. Glob. Change Biol. 12, 27–41 (2006).
Veteli, T. O., Kuokkanen, K., Julkunen-Tiitto, R., Roininen, H. & Tahvanainen, J. Effects of elevated CO
Atkin, O. K., Loveys, B. R., Atkinson, L. J. & Pons, T. L. Phenotypic plasticity and growth temperature: understanding interspecific variability. J. Exp. Bot. 57, 267–281 (2006).
pubmed: 16371402
Rosbakh, S., Römermann, C. & Poschlod, P. Specific leaf area correlates with temperature: New evidence of trait variation at the population, species and community levels. Alp. Bot. 125, 79–86 (2015).
Fontana, V. et al. Decomposing the land-use specific response of plant functional traits along environmental gradients. Sci. Total Environ. 599–600, 750–759 (2017).
pubmed: 28499223
Poorter, H., Niinemets, Ü, Walter, A., Fiorani, F. & Schurr, U. A method to construct dose–response curves for a wide range of environmental factors and plant traits by means of a meta-analysis of phenotypic data. J. Exp. Bot. 61, 2043–2055 (2010).
pubmed: 20048331
Loveys, B. R., Scheurwater, I., Pons, T. L., Fitter, A. H. & Atkin, O. K. Growth temperature influences the underlying components of relative growth rate: An investigation using inherently fast- and slow-growing plant species. Plant Cell Environ. 25, 975–987 (2002).
Kichenin, E., Wardle, D. A., Peltzer, D. A., Morse, C. W. & Freschet, G. T. Contrasting effects of plant inter- and intraspecific variation on community-level trait measures along an environmental gradient. Funct. Ecol. 27, 1254–1261 (2013).
Otieno, D. O., Schmidt, M. W. T., Adiku, S. & Tenhunen, J. Physiological and morphological responses to water stress in two Acacia species from contrasting habitats. Tree Physiol. 25, 361–371 (2005).
pubmed: 15631984
Wright, I. J. et al. Global climatic drivers of leaf size. Science 357, 917–921 (2017).
pubmed: 28860384
Münzbergová, Z. et al. Plant origin, but not phylogeny, drive species ecophysiological response to projected climate. Front. Plant Sci. 11, 2 (2020).
Coley, P. D. & Barone, J. A. Herbivory and plant defenses in tropical forests. Annu. Rev. Ecol. Syst. 1, 305–335 (1996).
Danet, A., Anthelme, F., Gross, N. & Kéfi, S. Effects of indirect facilitation on functional diversity, dominance and niche differentiation in tropical alpine communities. J. Veg. Sci. 29, 835–846 (2018).
Ibanez, S., Lavorel, S., Puijalon, S. & Moretti, M. Herbivory mediated by coupling between biomechanical traits of plants and grasshoppers. Funct. Ecol. 27, 479–489 (2013).
Cornelissen, T., Fernandes, G. W. & Vasconcellos-Neto, J. Size does matter: Variation in herbivory between and within plants and the plant vigor hypothesis. Oikos 117, 1121–1130 (2008).
Zava, P. C. & Cianciaruso, M. V. Can we use plant traits and soil characteristics to predict leaf damage in savanna woody species?. Plant Ecol. 215, 625–637 (2014).
Price, P. W. The plant vigor hypothesis and herbivore attack. Oikos 62, 244–251 (1991).
Santos, J. C., Tavares, C. B. & Almeida-Cortez, J. S. Plant Vigor Hypothesis refuted: Preference-performance linkage of a gall-inducing weevil on small-sized host plant resources. Braz. J. Biol. 71, 65–69 (2011).
pubmed: 21437400
Albrectsen, B. R., Gardfjell, H., Orians, C. M., Murray, B. & Fritz, R. S. Slugs, willow seedlings and nutrient fertilization: Intrinsic vigor inversely affects palatability. Oikos 105, 268–278 (2004).
Baskett, C. A. & Schemske, D. W. Latitudinal patterns of herbivore pressure in a temperate herb support the biotic interactions hypothesis. Ecol. Lett. 21, 578–587 (2018).
pubmed: 29466840
Loranger, J. et al. Predicting invertebrate herbivory from plant traits: Evidence from 51 grassland species in experimental monocultures. Ecology 93, 2674–2682 (2012).
pubmed: 23431597
Carmona, D., Lajeunesse, M. J. & Johnson, M. T. J. Plant traits that predict resistance to herbivores. Funct. Ecol. 25, 358–367 (2011).
Todd, G. W., Richardson, P. E. & Sengupta, S. P. Leaf and stem anatomical anomalies in a drought-susceptible species, impatiens Balsamina, under conditions of drought stress. Bot. Gaz. 135, 121–126 (1974).
Tabak, N. M. & von Wettberg, E. Native and introduced jewelweeds of the Northeast. Northeast. Nat. 15, 159–176 (2008).
Kaarlejärvi, E., Eskelinen, A. & Olofsson, J. Herbivory prevents positive responses of lowland plants to warmer and more fertile conditions at high altitudes. Funct. Ecol. 3, 1244–1253 (2016).
Kieltyk, P. & Delimat, A. Impact of the alien plant Impatiens glandulifera on species diversity of invaded vegetation in the northern foothills of the Tatra Mountains, Central Europe. Plant Ecol. 220, 1–12 (2019).
Gaggini, L., Rusterholz, H.-P. & Baur, B. The invasion of an annual exotic plant species affects the above- and belowground plant diversity in deciduous forests to a different extent. Perspect. Plant Ecol. Evol. Syst. 38, 74–83 (2019).
Yuan, Y.-M. et al. Phylogeny and biogeography of Balsaminaceae inferred from ITS sequences. Taxon 53, 391–403 (2004).

Auteurs

Tomáš Dostálek (T)

Institute of Botany, The Czech Academy of Sciences, Zámek 1, 252 43, Průhonice, Czech Republic. tomas.dostalek@ibot.cas.cz.
Department of Botany, Faculty of Science, Charles University, Benátská 2, 128 01, Prague, Czech Republic. tomas.dostalek@ibot.cas.cz.

Maan Bahadur Rokaya (MB)

Department of Botany, Faculty of Science, Charles University, Benátská 2, 128 01, Prague, Czech Republic.
Department of Biodiversity Research, Global Change Research Centre, The Czech Academy of Sciences, Bělidla 4a, 603 00, Brno, Czech Republic.

Zuzana Münzbergová (Z)

Institute of Botany, The Czech Academy of Sciences, Zámek 1, 252 43, Průhonice, Czech Republic.
Department of Botany, Faculty of Science, Charles University, Benátská 2, 128 01, Prague, Czech Republic.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH