Altitude, habitat type and herbivore damage interact in their effects on plant population dynamics
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
30557339
PubMed Central
PMC6296709
DOI
10.1371/journal.pone.0209149
PII: PONE-D-18-19368
Knihovny.cz E-zdroje
- MeSH
- býložravci * MeSH
- chování zvířat * MeSH
- ekosystém * MeSH
- nadmořská výška * MeSH
- populační dynamika MeSH
- šalvěj růst a vývoj MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Insects represent one of the most abundant groups of herbivores, and many of them have significant impacts on the dynamics of plant populations. As insects are very sensitive to changes in climatic conditions, we hypothesize that their effects on plant population dynamics will depend on climatic conditions. Knowledge of the variation in herbivore effects on plant population dynamics is, however, still rather sparse. We studied population dynamics and herbivore damage at the individual plant level of Salvia nubicola along a wide altitudinal gradient representing a range of climatic conditions. Using integral projection models, we estimated the effect of changes in herbivore pressure on plant populations in different climates and habitat types. Since we recorded large differences in the extent of herbivore damage along the altitudinal gradient, we expected that the performance of plants from different altitudes would be affected to different degrees by herbivores. Indeed, we found that populations from low altitudes were better able to withstand increased herbivore damage, while populations from high altitudes were suppressed by herbivores. However, the pattern described above was evident only in populations from open habitats. In forest habitats, the differences in population dynamics between low and high altitudes were largely diminished. The effects of herbivores on plants from different altitudes were thus largely habitat specific. Our results indicate potential problems for plant populations from high altitudes in open habitats because of increased herbivore damage. However, forest habitats may provide refuges for the plants at these high altitudes.
Department of Botany Faculty of Science Charles University Prague Czech Republic
Institute of Botany the Czech Academy of Sciences Průhonice Czech Republic
Zobrazit více v PubMed
Hartley SE, Jones CG. Plant Chemistry and Herbivory, or Why the World is Green Plant Ecology. John Wiley & Sons, Ltd; 2009. pp. 284–324. 10.1002/9781444313642.ch10 DOI
Myers JH, Sarfraz RM. Impacts of Insect Herbivores on Plant Populations. Annu Rev Entomol. 2017;62: 207–230. 10.1146/annurev-ento-010715-023826 PubMed DOI
Maron JL, Crone E. Herbivory: effects on plant abundance, distribution and population growth. Proc R Soc B Biol Sci. 2006;273: 2575–2584. 10.1098/rspb.2006.3587 PubMed DOI PMC
Schoonhoven LM, Loon JJA van, Dicke M. Insect-plant biology. 2005; xvii + 421 pp.
Zidorn C. Altitudinal variation of secondary metabolites in flowering heads of the Asteraceae: trends and causes. Phytochem Rev. 2010;9: 197–203. 10.1007/s11101-009-9143-7 DOI
Dicke M, Baldwin IT. The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help.’ Trends Plant Sci. 2010;15: 167–175. 10.1016/j.tplants.2009.12.002 PubMed DOI
Rasmann S, Buri A, Gallot-Lavallée M, Joaquim J, Purcell J, Pellissier L. Differential allocation and deployment of direct and indirect defences by Vicia sepium along elevation gradients. J Ecol. 2014;102: 930–938. 10.1111/1365-2745.12253 DOI
Dostálek T, Rokaya MB, Maršík P, Rezek J, Skuhrovec J, Pavela R, et al. Trade-off among different anti-herbivore defence strategies along an altitudinal gradient. AoB Plants. 2016;8: plw026 10.1093/aobpla/plw026 PubMed DOI PMC
Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM, Brown VK, et al. Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Change Biol. 2002;8: 1–16. 10.1046/j.1365-2486.2002.00451.x DOI
Sauby KE, Kilmer J, Christman MC, Holt RD, Marsico TD. The influence of herbivory and weather on the vital rates of two closely related cactus species. Ecol Evol. 2017;7: 6996–7009. 10.1002/ece3.3232 PubMed DOI PMC
Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD. Shifting plant phenology in response to global change. Trends Ecol Evol. 2007;22: 357–365. 10.1016/j.tree.2007.04.003 PubMed DOI
Jamieson MA, Trowbridge AM, Raffa KF, Lindroth RL. Consequences of Climate Warming and Altered Precipitation Patterns for Plant-Insect and Multitrophic Interactions. Plant Physiol. 2012;160: 1719–1727. 10.1104/pp.112.206524 PubMed DOI PMC
Van der Putten WH, Macel M, Visser ME. Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels. Philos Trans R Soc B Biol Sci. 2010;365: 2025–2034. 10.1098/rstb.2010.0037 PubMed DOI PMC
Körner C. The use of ‘altitude’ in ecological research. Trends Ecol Evol. 2007;22: 569–574. 10.1016/j.tree.2007.09.006 PubMed DOI
Fisher M. Decline in the juniper woodlands of Raydah Reserve in southwestern Saudi Arabia: a response to climate changes? Glob Ecol Biogeogr Lett. 1997; 379–386.
Zheng J, Ge Q, Hao Z, Wang W-C. Spring Phenophases in Recent Decades Over Eastern China and Its Possible Link to Climate Changes. Clim Change. 2006;77: 449–462. 10.1007/s10584-005-9038-6 DOI
Van Mantgem PJ, Stephenson NL. Apparent climatically induced increase of tree mortality rates in a temperate forest. Ecol Lett. 2007;10: 909–916. 10.1111/j.1461-0248.2007.01080.x PubMed DOI
Hovenden MJ, Wills KE, Chaplin RE, Vander Schoor JK, Williams AL, Osanai Y, et al. Warming and elevated CO2 affect the relationship between seed mass, germinability and seedling growth in Austrodanthonia caespitosa, a dominant Australian grass. Glob Change Biol. 2008;14: 1633–1641. 10.1111/j.1365-2486.2008.01597.x DOI
Verheyen K, Adriaenssens S, Gruwez R, Michalczyk IM, Ward LK, Rosseel Y, et al. Juniperus communis: victim of the combined action of climate warming and nitrogen deposition? Plant Biol. 2009;11: 49–59. 10.1111/j.1438-8677.2009.00214.x PubMed DOI
Montesinos D, García-Fayos P, Verdú M. Relictual distribution reaches the top: Elevation constrains fertility and leaf longevity in Juniperus thurifera. Acta Oecologica. 2010;36: 120–125. 10.1016/j.actao.2009.10.010 DOI
Yang LH, Rudolf VHW. Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecol Lett. 2010;13: 1–10. 10.1111/j.1461-0248.2009.01402.x PubMed DOI
Caswell H. Matrix population models: construction, analysis, and interpretation. Sinauer Associates; 2001.
Münzbergová Z. Effect of population size on the prospect of species survival. Folia Geobot. 2006;41: 137–150. 10.1007/BF02806475 DOI
Brodie JF, Helmy OE, Brockelman WY, Maron JL. Functional differences within a guild of tropical mammalian frugivores. Ecology. 2009;90: 688–698. PubMed
Nicolè F, Dahlgren JP, Vivat A, Till-Bottraud I, Ehrlén J. Interdependent effects of habitat quality and climate on population growth of an endangered plant. J Ecol. 2011;99: 1211–1218. 10.1111/j.1365-2745.2011.01852.x DOI
Kim E, Donohue K. Demographic, developmental and life-history variation across altitude in Erysimum capitatum. J Ecol. 2011;99: 1237–1249. 10.1111/j.1365-2745.2011.01831.x DOI
Maron JL, Baer KC, Angert AL. Disentangling the drivers of context-dependent plant–animal interactions. J Ecol. 2014;102: 1485–1496. 10.1111/1365-2745.12305 DOI
Garcia-Camacho R, Albert MJ, Escudero A. Small-scale demographic compensation in a high-mountain endemic: the low edge stands still. Plant Ecol Divers. 2012;5: 37–44. 10.1080/17550874.2012.662534 DOI
Pollnac FW, Maxwell BD, Taper ML, Rew LJ. The demography of native and non-native plant species in mountain systems: examples in the Greater Yellowstone Ecosystem. Popul Ecol. 2014;56: 81–95. 10.1007/s10144-013-0391-4 DOI
Ehrlén J. Demography of the Perennial Herb Lathyrus Vernus. II. Herbivory and Population Dynamics. J Ecol. 1995;83: 297–308.
Rose KE, Russell FL, Louda SM. Integral projection model of insect herbivore effects on Cirsium altissimum populations along productivity gradients. Ecosphere. 2011;2: 1–19. 10.1890/ES11-00096.1 DOI
Aikens ML, Roach DA. Potential impacts of tolerance to herbivory on population dynamics of a monocarpic herb. Am J Bot. 2015;102: 1901–1911. 10.3732/ajb.1500198 PubMed DOI
Katz DSW. The effects of invertebrate herbivores on plant population growth: a meta-regression analysis. Oecologia. 2016;182: 43–53. 10.1007/s00442-016-3602-9 PubMed DOI
Kurkjian HM, Carothers SK, Jules ES. Seed predation has the potential to drive a rare plant to extinction. J Appl Ecol. 2017;54: 862–871. 10.1111/1365-2664.12808 DOI
Miller TEX, Louda SM, Rose KA, Eckberg JO. Impacts of insect herbivory on cactus population dynamics: experimental demography across an environmental gradient. Ecol Monogr. 2009;79: 155–172. 10.1890/07-1550.1 DOI
Rokaya MB, Münzbergová Z, Dostálek T. Sustainable harvesting strategy of medicinal plant species in Nepal–results of a six-year study. Folia Geobot. 2017;52: 239–252. 10.1007/s12224-017-9287-y DOI
Hough-Goldstein J, LaCoss SJ. Interactive effects of light environment and herbivory on growth and productivity of an invasive annual vine, Persicaria perfoliata. Arthropod-Plant Interact. 2012;6: 103–112. 10.1007/s11829-011-9158-z DOI
Rokaya MB, Dostálek T, Münzbergová Z. Plant-herbivore interactions along elevational gradient: Comparison of field and common garden data. Acta Oecologica. 2016;77: 168–175. 10.1016/j.actao.2016.10.011 DOI
Press JR, Shrestha KK, Sutton DA. Annotated checklist of the flowering plants of Nepal. London, UK: The Natural History Museum; 2000.
Bhattarai KR, Vetaas OR, Grytnes JA. Relationship between plant species richness and biomass in an arid sub-alpine grassland of the central Himalayas, Nepal. Folia Geobot. 2004;39: 57–71. 10.1007/BF02803264 DOI
Miehe G. Vegetationsgeographische Untersuchungen im Dhaulagiri-und Annapurna-Himalaya. Diss Bot. 1982;66: 1–224.
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.
Merow C, Dahlgren JP, Metcalf CJE, Childs DZ, Evans MEK, Jongejans E, et al. Advancing population ecology with integral projection models: a practical guide. Methods Ecol Evol. 2014;5: 99–110. 10.1111/2041-210X.12146 DOI
Easterling MR, Ellner SP, Dixon PM. Size-Specific Sensitivity: Applying a New Structured Population Model. Ecology. 2000;81: 694–708.
Dahlgren JP, Bengtsson K, Ehrlén J. The demography of climate-driven and density-regulated population dynamics in a perennial plant. Ecology. 2016;97: 899–907. 10.1890/15-0804.1 PubMed DOI
Harrell FE. Regression Modeling Strategies Springer; N Y. 2001;
Efron B, Tibshirani R. An introduction to the bootstrap. New York: Chapman & Hall; 1993.
Alvarez-Buylla ER, Slatkin M. Finding Confidence Limits on Population Growth Rates: Three Real Examples Revised. Ecology. 1994;75: 255–260. PubMed
Schlinkert H, Westphal C, Clough Y, Ludwig M, Kabouw P, Tscharntke T. Feeding damage to plants increases with plant size across 21 Brassicaceae species. Oecologia. 2015;179: 455–466. 10.1007/s00442-015-3353-z PubMed DOI
Price PW. The Plant Vigor Hypothesis and Herbivore Attack. Oikos. 1991;62: 244–251. 10.2307/3545270 DOI
Louda SM, Rodman JE. Insect Herbivory as a Major Factor in the Shade Distribution of a Native Crucifer (Cardamine Cordifolia A. Gray, Bittercress). J Ecol. 1996;84: 229–237. 10.2307/2261358 DOI
Bruelheide H, Scheidel U. Slug herbivory as a limiting factor for the geographical range of Arnica montana. J Ecol. 1999;87: 839–848. 10.1046/j.1365-2745.1999.00403.x DOI
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. 2014;37: 950–959. 10.1111/ecog.00833 DOI
Rasmann S, Pellissier L, Defossez E, Jactel H, Kunstler G. Climate-driven change in plant–insect interactions along elevation gradients. Funct Ecol. 2014;28: 46–54. 10.1111/1365-2435.12135 DOI
Reich PB, Wright IJ, Cavender‐Bares J, Craine JM, Oleksyn J, Westoby M, et al. The Evolution of Plant Functional Variation: Traits, Spectra, and Strategies. Int J Plant Sci. 2003;164: S143–S164. 10.1086/374368 DOI
Selakovic SD, Stanisavljevic NS, Vujic VD, Rubinjoni LZ, Jovanovic ZS, Radovic SR, et al. Light and sex interplay: differential herbivore damage in sun and shade in dioecious Mercurialis perennis. Arch Biol Sci. 2018;70: 469–479. 10.2298/ABS171207007S DOI
Roberts MR, Paul ND. Seduced by the dark side: integrating molecular and ecological perspectives on the influence of light on plant defence against pests and pathogens. New Phytol. 2006;170: 677–699. 10.1111/j.1469-8137.2006.01707.x PubMed DOI
Crawley M. Plant Ecology. John Wiley & Sons; 2009.
Münzbergová Z. Determinants of species rarity: population growth rates of species sharing the same habitat. Am J Bot. 2005;92: 1987–1994. 10.3732/ajb.92.12.1987 PubMed DOI
Maron JL, Kauffman MJ. Habitat-Specific Impacts of Multiple Consumers on Plant Population Dynamics. Ecology. 2006;87: 113–124. 10.1890/05-0434 PubMed DOI
Buckley YM, Ramula S, Blomberg SP, Burns JH, Crone EE, Ehrlén J, et al. Causes and consequences of variation in plant population growth rate: a synthesis of matrix population models in a phylogenetic context. Ecol Lett. 2010;13: 1182–1197. 10.1111/j.1461-0248.2010.01506.x PubMed DOI
Paige KN, Whitham TG. Overcompensation in Response to Mammalian Herbivory: The Advantage of Being Eaten. Am Nat. 1987;129: 407–416. 10.1086/284645 DOI
Lennartsson T, Tuomi J, Nilsson P. Evidence for an Evolutionary History of Overcompensation in the Grassland Biennial Gentianella campestris (Gentianaceae). Am Nat. 1997;149: 1147–1155. 10.1086/286043 PubMed DOI
Siddappaji MH, Scholes DR, Bohn M, Paige KN. Overcompensation in Response to Herbivory in Arabidopsis thaliana: the Role of Glucose-6-Phosphate Dehydrogenase and the Oxidative Pentose-Phosphate Pathway. Genetics. 2013; genetics.113.154351. 10.1534/genetics.113.154351 PubMed DOI PMC
Cornelissen T, Fernandes GW, Vasconcellos‐Neto J. Size does matter: variation in herbivory between and within plants and the plant vigor hypothesis. Oikos. 2008;117: 1121–1130. 10.1111/j.0030-1299.2008.16588.x DOI
Salgado-Luarte C, Gianoli E. Herbivory on Temperate Rainforest Seedlings in Sun and Shade: Resistance, Tolerance and Habitat Distribution. PLOS ONE. 2010;5: e11460 10.1371/journal.pone.0011460 PubMed DOI PMC
Münzbergová Z, Skuhrovec J. Effect of Habitat Conditions and Plant Traits on Leaf Damage in the Carduoideae Subfamily. PLOS ONE. 2013;8: e64639 10.1371/journal.pone.0064639 PubMed DOI PMC
Koricheva J, Nykänen H, Gianoli E, Pfister AECA. Meta‐analysis of Trade‐offs among Plant Antiherbivore Defenses: Are Plants Jacks‐of‐All‐Trades, Masters of All? Am Nat. 2004;163: E64–E75. 10.1086/382601 PubMed DOI
Ballhorn DJ, Kautz S, Lion U, Heil M. Trade-offs between direct and indirect defences of lima bean (Phaseolus lunatus). J Ecol. 2008;96: 971–980.
Franco M, Silvertown J. A Comparative Demography of Plants Based upon Elasticities of Vital Rates. Ecology. 2004;85: 531–538.
Dostálek T, Münzbergová Z. Comparative Population Biology of Critically Endangered Dracocephalum austriacum (Lamiaceae) in Two Distant Regions. Folia Geobot. 2013;48: 75–93. 10.1007/s12224-012-9132-2 DOI
Černá L, Münzbergová Z. Comparative Population Dynamics of Two Closely Related Species Differing in Ploidy Level. PLoS ONE. 2013;8: e75563 10.1371/journal.pone.0075563 PubMed DOI PMC
Rees M, Ellner SP. Integral projection models for populations in temporally varying environments. Ecol Monogr. 2009;79: 575–594. 10.1890/08-1474.1 DOI
Bucharová A, Brabec J, Münzbergová Z. Effect of land use and climate change on the future fate of populations of an endemic species in central Europe. Biol Conserv. 2012;145: 39–47. 10.1016/j.biocon.2011.09.016 DOI
Johnson CA, Coutinho RM, Berlin E, Dolphin KE, Heyer J, Kim B, et al. Effects of temperature and resource variation on insect population dynamics: the bordered plant bug as a case study. Funct Ecol. 2016;30: 1122–1131. 10.1111/1365-2435.12583 PubMed DOI PMC
Heinken-Šmídová A, Münzbergová Z. Population Dynamics of the Endangered, Long-Lived Perennial Species, Ligularia sibirica. Folia Geobot. 2012;47: 193–214. 10.1007/s12224-011-9116-7 DOI
Koop AL, Horvitz CC. Projection Matrix Analysis of the Demography of an Invasive, Nonnative Shrub (Ardisia elliptica). Ecology. 2005;86: 2661–2672.
Jongejans E, De Kroon H. Space versus time variation in the population dynamics of three co-occurring perennial herbs. J Ecol. 2005;93: 681–692. 10.1111/j.1365-2745.2005.01003.x DOI