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Responses of leaf beetle larvae to elevated [CO2] and temperature depend on Eucalyptus species

  • Global change ecology - Original research
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Abstract

It is essential to understand the combined effects of elevated [CO2] and temperature on insect herbivores when attempting to forecast climate change responses of diverse ecosystems. Plant species differ in foliar chemistry, and this may result in idiosyncratic plant-mediated responses of insect herbivores at elevated [CO2] and temperature. We measured the response of the eucalypt leaf beetle Paropsis atomaria (Coleoptera: Chrysomelidae) feeding on Eucalyptus tereticornis and Eucalyptus robusta. Seedlings were grown at ambient (400 µmol mol−1) or elevated (640 µmol mol−1) [CO2] and ambient (26/18 °C day/night) or elevated (ambient + 4 °C) temperature in a greenhouse for 7 months. Larvae fed on flush leaves from egg hatch to pupation while being directly exposed to these conditions. Elevated [CO2] reduced foliar [N] and [P], while it increased total nonstructural carbohydrates and the C:N ratio. Elevated temperature increased foliar [N] in E. robusta but not E. tereticornis. Plant-mediated effects of elevated [CO2] reduced female pupal weight and increased developmental time and leaf consumption. Larval survival at elevated [CO2] was impacted differently by the two host plant species; survival increased on E. robusta while it decreased on E. tereticornis. Elevated temperature accelerated larval development but did not impact other insect parameters. We did not detect a CO2 × temperature interaction, suggesting that elevated temperature as a combined direct and plant-mediated effect may not be able to ameliorate the negative plant-mediated effects of elevated [CO2] on insect herbivores. Our study highlighted host-plant-specific responses of insect herbivores to climate change factors that resulted in host-plant-specific survival.

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References

  • Addo-Bediako A, Chown SL, Gaston KJ (2002) Metabolic cold adaptation in insects: a large-scale perspective. Funct Ecol 16:332–338

    Article  Google Scholar 

  • Agrell J, McDonald EP, Lindroth RL (2000) Effects of CO2 and light on tree phytochemistry and insect performance. Oikos 88:259–272

    Article  CAS  Google Scholar 

  • Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ 30:258–270

    Article  CAS  PubMed  Google Scholar 

  • Ainsworth EA et al (2002) A meta-analysis of elevated [CO2] effects on soybean (glycine max) physiology, growth and yield. Glob Change Biol 8:695–709

  • Andrew NR et al (2013) Assessing insect responses to climate change: what are we testing for? Where should we be heading? Peer J 1:e11. doi:10.7717/peerj.11

    Article  PubMed Central  PubMed  Google Scholar 

  • Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844

    Article  CAS  PubMed  Google Scholar 

  • Ayub G, Smith RA, Tissue DT, Atkin OK (2011) Impacts of drought on leaf respiration in darkness and light in Eucalyptus saligna exposed to industrial-age atmospheric CO2 and growth temperature. New Phytol 190:1003–1018

    Article  PubMed  Google Scholar 

  • Bale JS et al (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Glob Change Biol 8:1–16

    Article  Google Scholar 

  • Ballhorn DJ, Schmitt I, Fankhauser JD, Katagiri F, Pfanz H (2011) CO2-mediated changes of plant traits and their effects on herbivores are determined by leaf age. Ecol Entomol 36:1–13

    Article  Google Scholar 

  • Bezemer TM, Jones TH (1998) Plant-insect herbivore interactions in elevated atmospheric CO2: quantitative analyses and guild effects. Oikos 82:212–222

    Article  Google Scholar 

  • Boland DJ et al (2006) Forest trees of Australia. CSIRO, Collingwood

  • CAB International (2005) Forestry compendium. CAB International, Wallingford

  • Carne P (1966) Ecological characteristics of the eucalypt-defoliating chrysomelid Paropsis atomaria Ol. Aust J Zool 14:647–672

    Article  Google Scholar 

  • Coley PD (1998) Possible effects of climate change on plant/herbivore interactions in moist tropical forests. Clim Change 39:455–472

    Article  Google Scholar 

  • Coley P, Massa M, Lovelock C, Winter K (2002) Effects of elevated CO2 on foliar chemistry of saplings of nine species of tropical tree. Oecologia 133:62–69

    Article  CAS  PubMed  Google Scholar 

  • Coley PD, Bateman ML, Kursar TA (2006) The effects of plant quality on caterpillar growth and defense against natural enemies. Oikos 115:219–228

    Article  Google Scholar 

  • CSIRO, Australian Bureau of Meteorology (2012) State of the climate 2012. CSIRO/Australian Bureau of Meteorology, Collingwood/Melbourne

  • Davis AJ, Jenkinson LS, Lawton JH, Shorrocks B, Wood S (1998) Making mistakes when predicting shifts in species range in response to global warming. Nature 391:783–786

    Article  CAS  PubMed  Google Scholar 

  • Dury SJ, Good JEG, Perrins CM, Buse A, Kaye T (1998) The effects of increasing CO2 and temperature on oak leaf palatability and the implications for herbivorous insects. Glob Change Biol 4:55–61

    Article  Google Scholar 

  • Ebell LF (1969) Variation in total soluble sugars of conifer tissues with method of analysis. Phytochemistry 8:227–233

    Article  CAS  Google Scholar 

  • Ehnes RB, Rall BC, Brose U (2011) Phylogenetic grouping, curvature and metabolic scaling in terrestrial invertebrates. Ecol Lett 14:993–1000

    Article  PubMed  Google Scholar 

  • Fox LR, Macauley B (1977) Insect grazing on Eucalyptus in response to variation in leaf tannins and nitrogen. Oecologia 29:145–162

    Article  Google Scholar 

  • Friedenberg NA, Sarkar S, Kouchoukos N, Billings RF, Ayres MP (2008) Temperature extremes, density dependence, and southern pine beetle (Coleoptera: curculionidae) population dynamics in east Texas. Environ Entomol 37:650–659

    Article  PubMed  Google Scholar 

  • Ghannoum O et al (2010) Exposure to preindustrial, current and future atmospheric CO2 and temperature differentially affects growth and photosynthesis in Eucalyptus. Glob Change Biol 16:303–319

    Article  Google Scholar 

  • Golizadeh ALI, Kamali K, Fathipour Y, Abbasipour H (2007) Temperature-dependent development of diamondback moth, Plutella xylostella (Lepidoptera: plutellidae) on two brassicaceous host plants. Insect Sci 14:309–316

    Article  Google Scholar 

  • Henery ML, Wallis IR, Stone C, Foley WJ (2008) Methyl jasmonate does not induce changes in Eucalyptus grandis leaves that alter the effect of constitutive defences on larvae of a specialist herbivore. Oecologia 156:847–859

    Article  CAS  PubMed  Google Scholar 

  • Holton MK, Lindroth RL, Nordheim EV (2003) Foliar quality influences tree-herbivore-parasitoid interactions: effects of elevated CO2, O3, and plant genotype. Oecologia 137:233–244

    Article  PubMed  Google Scholar 

  • Hovenden MJ, Williams AL (2010) The impacts of rising CO2 concentrations on Australian terrestrial species and ecosystems. Aust Ecol 35:665–684

    Article  Google Scholar 

  • IPCC, Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds ) (2013) Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge

  • Ji LZ, An LL, Wang XW (2011) Growth responses of gypsy moth larvae to elevated CO2: the influence of methods of insect rearing. Insect Sci 18:409–418

    Article  Google Scholar 

  • Johns CV, Hughes L (2002) Interactive effects of elevated CO2 and temperature on the leaf-miner Dialectica scalariella Zeller (Lepidoptera: Gracillariidae) in Paterson’s Curse, Echium plantagineum (Boraginaceae). Glob Change Biol 8:142–152

    Article  Google Scholar 

  • Jones CG, Hartley SE (1999) A protein competition model of phenolic allocation. Oikos 86:27–44

    Article  CAS  Google Scholar 

  • Kinney KK, Lindroth RL, Jung SM, Nordheim EV (1997) Effects of CO2 and NO3-availability on deciduous trees: phytochemistry and insect performance. Ecology 78:215–230

    Google Scholar 

  • Lawler IR, Foley WJ, Woodrow IE, Cork SJ (1997) The effects of elevated CO2 atmospheres on the nutritional quality of Eucalyptus foliage and its interaction with soil nutrient and light availability. Oecologia 109:59–68

    Article  Google Scholar 

  • Levesque KR, Fortin M, Mauffette Y (2002) Temperature and food quality effects on growth, consumption and post-ingestive utilization effciencies of the forest tent caterpillar Malacosoma disstria (Lepidoptera: Lasiocampidae). Bull Entomol Res 92:127–136

    Article  CAS  PubMed  Google Scholar 

  • Lincoln DE, Sionit N, Strain BR (1984) Growth and feeding response of Pseudoplusia includens (Lepidoptera: Noctuidae) to host plants grown in controlled carbon dioxide atmospheres. Environ Entomol 13:1527–1530

    Article  CAS  Google Scholar 

  • Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants face the future. Annu Rev Plant Biol 55:591–628

    Article  CAS  PubMed  Google Scholar 

  • Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161

    Article  Google Scholar 

  • McKiernan AB, O’Reilly-Wapstra JM, Price C, Davies NW, Potts BM, Hovenden MJ (2012) Stability of plant defensive traits among populations in two Eucalyptus species under elevated carbon dioxide. J Chem Ecol 38:204–212

    Article  CAS  PubMed  Google Scholar 

  • Moore BD, Wallis IR, Wood JT, Foley WJ (2004) Foliar nutrition, site quality, and temperature influence foliar chemistry of tallowwood (Eucalyptus microcorys). Ecol Monogr 74:553–568

    Article  Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  • Murray TJ, Ellsworth DS, Tissue DT, Riegler M (2013a) Interactive direct and plant-mediated effects of elevated atmospheric [CO2] and temperature on a eucalypt-feeding insect herbivore. Glob Change Biol 19:1407–1416

    Article  CAS  Google Scholar 

  • Murray TJ, Tissue DT, Ellsworth DS, Riegler M (2013b) Interactive effects of pre-industrial, current and future [CO2] and temperature on an insect herbivore of Eucalyptus. Oecologia 171:1025–1035

    Article  CAS  PubMed  Google Scholar 

  • Nahrung HF (2006) Paropsine beetles (Coleoptera: Chrysomelidae) in south-eastern Queensland hardwood plantations: identifying potential pest species. Aust For 69:270–274

    Article  Google Scholar 

  • Nahrung HF, Dunstan PK, Allen GR (2001) Larval gregariousness and neonate establishment of the eucalypt-feeding beetle Chrysophtharta agricola (Coleoptera: Chrysomelidae: Paropsini). Oikos 94:358–364

  • Niziolek OK, Berenbaum MR, DeLucia EH (2013) Impact of elevated CO2 and increased temperature on Japanese beetle herbivory. Insect Sci 20:513–523

    Article  PubMed  Google Scholar 

  • Ohmart C (1991) Role of food quality in the population dynamics of chrysomelid beetles feeding on Eucalyptus. For Ecol Manag 39:35–46

    Article  Google Scholar 

  • Ohmart C, Stewart L, Thomas J (1985) Effects of food quality, particularly nitrogen concentrations, of Eucalyptus blakelyi foliage on the growth of Paropsis atomaria larvae (Coleoptera: Chrysomelidae). Oecologia 65:543–549

  • Pelini SL, Keppel JA, Kelley AE, Hellmann JJ (2010) Adaptation to host plants may prevent rapid insect responses to climate change. Glob Change Biol 16:2923–2929

    Google Scholar 

  • Peltonen PA, Vapaavuori E, Heinonen J, Julkunen-Tiitto R, Holopainen JK (2010) Do elevated atmospheric CO2 and O3 affect food quality and performance of folivorous insects on silver birch? Glob Change Biol 16:918–935

    Article  Google Scholar 

  • Quirk J, McDowell NG, Leake JR, Hudson PJ, Beerling DJ (2013) Increased susceptibility to drought-induced mortality in Sequoia sempervirens (Cupressaceae) trees under Cenozoic atmospheric carbon dioxide starvation. Am J Bot 100:582–591

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Rapley LP, Allen GR, Potts BM, Davies NW (2007) Constitutive or induced defences—how does Eucalyptus globulus defend itself from larval feeding? Chemoecology 17:235–243

  • Raubenheimer D, Simpson SJ, Mayntz D (2009) Nutrition, ecology and nutritional ecology: toward an integrated framework. Funct Ecol 23:4–16

    Article  Google Scholar 

  • Reid CAM, Ohmart CP (1989) Determination of the sex of pupae of Paropsis atomaria Olivier, and related Paropsina (Coleoptera: Chrysomelidae). Aust J Entomol 28:29–30

  • Robinson EA, Ryan GD, Newman JA (2012) A meta-analytical review of the effects of elevated CO2 on plant–arthropod interactions highlights the importance of interacting environmental and biological variables. New Phytol 194:321–336

    Article  CAS  PubMed  Google Scholar 

  • Rouault G, Candau J, Lieutier F, Nageleisen L, Martin J, Warzée N (2006) Effects of drought and heat on forest insect populations in relation to the 2003 drought in Western Europe. Ann For Sci 63:613–624

    Article  Google Scholar 

  • Ryalls JMW, Riegler M, Moore BD, Lopaticki G, Johnson SN (2013) Effects of elevated temperature and CO2 on aboveground-belowground systems: a case study with plants, their mutualistic bacteria and root/shoot herbivores. Front Plant Sci 4:445

    Article  PubMed Central  PubMed  Google Scholar 

  • Ryan GD, Rasmussen S, Newman JA (2010) Global atmospheric change and trophic interactions: are there any general responses? In: Baluska F, Ninkovic V (eds) Plant communication from an ecological perspective. Springer, Berlin, pp 179–214

  • Salminen JP, Karonen M (2011) Chemical ecology of tannins and other phenolics: we need a change in approach. Funct Ecol 25:325–338

    Article  Google Scholar 

  • Schutze MK, Mather PB, Clarke AR (2006) Species status and population structure of the Australian Eucalyptus pest Paropsis atomaria Olivier (Coleoptera: Chrysomelidae). Agric For Entomol 8:323–332

  • Seneweera S, Makino A, Hirotsu N, Norton R, Suzuki Y (2011) New insight into photosynthetic acclimation to elevated CO2: the role of leaf nitrogen and ribulose-1,5-bisphosphate carboxylase/oxygenase content in rice leaves. Environ Exp Bot 71:128–136

  • Sherwin GL, George L, Kannangara K, Tissue DT, Ghannoum O (2013) Impact of industrial-age climate change on the relationship between water uptake and tissue nitrogen in eucalypt seedlings. Funct Plant Biol 40:201–212

    Article  Google Scholar 

  • Steinbauer MJ (2001) Specific leaf weight as an indicator of juvenile leaf toughness in Tasmanian bluegum (Eucalyptus globulus ssp. globulus): implications for insect defoliation. Aust For 64:32–37

    Article  Google Scholar 

  • Stiling P, Cornelissen T (2007) How does elevated carbon dioxide (CO2) affect plant–herbivore interactions? A field experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance. Glob Change Biol 13:1823–1842

    Article  Google Scholar 

  • Stiling P et al (2003) Elevated CO2 lowers relative and absolute herbivore density across all species of a scrub-oak forest. Oecologia 134:82–87

    Article  PubMed  Google Scholar 

  • Terblanche JS, Clusella-Trullas S, Chown SL (2010) Phenotypic plasticity of gas exchange pattern and water loss in Scarabaeus spretus (Coleoptera: Scarabaeidae): deconstructing the basis for metabolic rate variation. J Exp Biol 213:2940–2949

    Article  PubMed  Google Scholar 

  • Unsicker SB, Mody K (2005) Influence of tree species and compass bearing on insect folivory of nine common tree species in the West African savanna. J Trop Ecol 21:227–231

    Article  Google Scholar 

  • Vigue LM, Lindroth RL (2010) Effects of genotype, elevated CO2 and elevated O3 on aspen phytochemistry and aspen leaf beetle Chrysomela crotchi performance. Agric For Entomol 12:267–276

    Google Scholar 

  • Way DA, Oren R (2010) Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data. Tree Physiol 30:669–688

    Article  PubMed  Google Scholar 

  • White TCR (1993) The inadequate environment: nitrogen and the abundance of animals. Springer, Berlin

    Book  Google Scholar 

  • White TCR (2014) Senescence-feeders: a new trophic sub-guild of insect herbivores. J Appl Entomol. doi:10.1111/jen.12147

    Google Scholar 

  • Williams RS, Norby RJ, Lincoln DE (2000) Effects of elevated CO2 and temperature-grown red and sugar maple on gypsy moth performance. Glob Change Biol 6:685–695

    Article  Google Scholar 

  • Williams RS, Lincoln DE, Norby RJ (2003) Development of gypsy moth larvae feeding on red maple saplings at elevated CO2 and temperature. Oecologia 137:114–122

    Article  PubMed  Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Winkler IS, Mitter C, Scheffer SJ (2009) Repeated climate-linked host shifts have promoted diversification in a temperate clade of leaf-mining flies. Proc Natl Acad Sci USA 106:18103–18108

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zvereva EL, Kozlov MV (2006) Consequences of simultaneous elevation of carbon dioxide and temperature for plant–herbivore interactions: a metaanalysis. Glob Change Biol 12:27–41

    Article  Google Scholar 

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Acknowledgments

This research was supported by an Australian Postgraduate Award to AG and DP1095972 of the Australian Research Council to MR. We thank Goran Lopaticki and Aidan Hall for technical assistance and Kaushal Tewari and Pushpinder Matta for CHN analysis.

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Authors and Affiliations

  1. Hawkesbury Institute for the Environment, University of Western Sydney, Locked Bag 1797, Penrith, NSW, 2751, Australia

    Andrew N. Gherlenda, Ben D. Moore, Scott N. Johnson & Markus Riegler

  2. School of Science and Health, University of Western Sydney, Locked Bag 1797, Penrith, NSW, 2751, Australia

    Anthony M. Haigh

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  1. Andrew N. Gherlenda
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  2. Anthony M. Haigh
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Correspondence to Andrew N. Gherlenda or Markus Riegler.

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Communicated by Evan H. DeLucia.

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Gherlenda, A.N., Haigh, A.M., Moore, B.D. et al. Responses of leaf beetle larvae to elevated [CO2] and temperature depend on Eucalyptus species. Oecologia 177, 607–617 (2015). https://doi.org/10.1007/s00442-014-3182-5

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