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Colonization of Solidago altissima by the Specialist Aphid Uroleucon nigrotuberculatum: Effects of Genetic Identity and Leaf Chemistry

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Abstract

In dominant old-field plant species, genotypic variation in traits important for herbivorous insects may explain variation in insect species abundance. While the importance of plant genetic identity on arthropod abundance has been demonstrated, specific factors that drive genotype choice by insects remain largely unknown. Sixteen genotypes of the widely distributed plant species Solidago altissima were used to investigate the possible role of nutrients and terpene secondary metabolites in shaping the abundance of a common specialist aphid, Uroleucon nigrotuberculatum. Ramets were propagated in a greenhouse and then transferred to a natural field setting. After 76 days, aphid abundance was quantified and leaf tissue assayed for nutrients and terpenes. Aphids/g plant biomass significantly differed among genotypes, with a 30-fold difference observed among plant genotypes. Leaf nitrogen, C:N ratio and water did not vary among genotypes. Of eight terpenes quantified, five were influenced by plant genotype. Aphid abundance increased marginally with the concentration of the monoterpene β-pinene in leaf tissue (P = 0.056). A partial least squares analysis determined that nutritional chemicals did not explain aphid responses, while 49 % of the variation in aphid colonization among genotypes was explained by terpenes. This study is one of the first to demonstrate that variation in allelochemicals may be related to differences in the abundance of a key herbivore among genotypes of a plant species that exhibits large intraspecific genetic variation.

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References

  • Barber NA, Marquis RJ (2011) Leaf quality, predators, and stochastic processes in the assembly of a diverse herbivore community. Ecology 92:699–708

    Article  PubMed  Google Scholar 

  • Bowers WS, Nishino C, Montgomery ME, Nault LR, Nielson MW (1977) Sesquiterpene progenitor, Germacrene A: an alarm pheromone in aphids. Science 196:680–681

    Article  CAS  PubMed  Google Scholar 

  • Burkle LA, Souza L, Genung M, Crutsinger CM (2013) Plant genotype, nutrients, and G X E interactions structure floral visitor communities. Ecosphere 4:1–20

    Article  Google Scholar 

  • Cappuccino N (1988) Spatial patterns of goldenrod aphids and the response of enemies to patch density. Oecologia 76:607–610

    Article  Google Scholar 

  • Couture JJ, Lindroth RL (2012) Atmospheric change alters the performance of an invasive forest insect. Glob Chang Biol 18:3543–3557. doi:10.1111/gcb.1214

    Article  Google Scholar 

  • Couture JJ, Meehan TD, Lindroth RL (2012) Atmospheric change alters foliar quality of host trees and performance of two outbreak insect species. Oecologia 168:863–876. doi:10.1007/s00442-011-2139-1

    Article  PubMed  Google Scholar 

  • Crutsinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC, Sanders NJ (2006) Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313:966–968

    Article  CAS  PubMed  Google Scholar 

  • Crutsinger GM, Reynolds WN, Classen AT, Sanders NJ (2008) Disparate effects of plant genotypic diversity on foliage and litter arthropod communities. Oecologia 158:65–75. doi:10.1007/s00442-008-1130-y

    Article  PubMed  Google Scholar 

  • Dungey HS, Potts BM, Whitham TG, Li HF (2000) Plant genetics affects arthropod community richness and composition: evidence from a synthetic eucalypt hybrid population. Evolution 54:1938–1946

    Article  CAS  PubMed  Google Scholar 

  • Genung MA, Lessard J-P, Brown CB, Bunn WA, Cregger MA, Reynolds WM, Felker-Quinn E, Stevenson ML, Hartley AS, Crutsinger GM, Schweitzer JA, Bailey JK (2010) Non-additive effects of genotypic diversity increases floral abundance and abundance of floral visitors. PLoS One 5:e8711. doi:10.1371/journal.pone.0008711

    Article  PubMed Central  PubMed  Google Scholar 

  • Genung MA, Crutsinger GM, Bailey JK, Schweitzer JA, Sanders NJ (2012) Aphid and ladybird abundance depend on the interaction of spatial effects and genotypic diversity. Oecologia 168:167–174. doi:10.1007/s00442-011-2080-3

    Article  PubMed  Google Scholar 

  • Gutiérrez C, Fereres A, Reina M, Cabrera R, González-Coloma A (1997) Behavioral and sublethal effects of structurally related lower terpenes on Myzus persciae. J Chem Ecol 23:1641–1650

    Article  Google Scholar 

  • Haddad NM, Haarstad J, Tilman D (2000) The effects of long-term nitrogen loading on grassland insect communities. Oecologia 124:73–84

    Article  Google Scholar 

  • Hair JF, Anderson RE, Tatham RL, Black WC (1984) Multivariate analysis: with readings, 3rd edn. MacMillan Publishing Company, New York

    Google Scholar 

  • Hakes AS, Cronin JT (2011) Resistance and tolerance to herbivory in Solidago altissima (Asteraceae): genetic variability, costs, and selection for multiple traits. Am J Bot 98:1446–1455. doi:10.3732/ajb.1000485

    Article  PubMed  Google Scholar 

  • Hersch-Green EI, Turley NE, Johnson MT (2011) Community genetics: what we have accomplished and where should we be going? Phil Trans R Soc B 366:1453–1460. doi:10.1098/rstb.2010.0331

    Article  PubMed Central  PubMed  Google Scholar 

  • Horner JD, Abrahamson WG (1992) Influence of plant genotype and environment on oviposition preference and offspring survival in a gallmaking herbivore. Oecologia 90:323–332

    Article  Google Scholar 

  • Hughes AR, Inouye BD, Johnson MT, Underwood N, Vellend M (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623. doi:10.1111/j.1461-0248.2008.011179x

    Article  PubMed  Google Scholar 

  • Hull-Sanders HM, Clare R, Johnson RH, Meyer GA (2007) Evaluation of the evolution of increased competitive ability (EICA) hypothesis: loss of defense against generalist but not specialist herbivores. J Chem Ecol 33:781–799. doi:10.1007/s10886-007-9252-y

    Article  CAS  PubMed  Google Scholar 

  • Hull-Sanders HM, Johnson RH, Owen HA, Meyer GA (2009) Effects of polyploidy on secondary chemistry, physiology, and performance of native and invasive genotypes of Solidago gigantea (Asteraceae). Am J Bot 96:762–770. doi:10.3732/ajb.0800200

    Article  PubMed  Google Scholar 

  • Johnson MJ (2008) Bottom-up effects of plant genotype on aphids, ants, and predators. Ecology 89:145–154

    Article  PubMed  Google Scholar 

  • Johnson MJ, Agrawal AA (2005) Plant genotype and environment interact to shape a diverse arthropod community on evening primrose (Oenothera biennis). Ecology 86:874–885

    Article  Google Scholar 

  • Johnson MJ, Lajeunesse MJ, Agrawal AA (2006) Additive and interactive effects of plant genotypic diversity on arthropod communities and plant fitness. Ecol Lett 9:24–34. doi:10.1111/j.1461-0248.2005.00833.x

    PubMed  Google Scholar 

  • Johnson RH, Hull-Sander HM, Meyer GA (2007) Comparison of foliar terpenes between native and invasive Solidago giganteana. Biochem Syst Ecol 35:821–830. doi:10.1016/j.bse.2007.06.005

    Article  CAS  Google Scholar 

  • Johnson RH, Halitschke R, Kessler A (2010) Simultaneous analysis of tissue- and genotype-specific variation in Solidago altissima (Asteraceae) rhizome terpenoids, and the polyacetylene dehydromatricaria ester. Chemoecology 20:255–264. doi:10.1007/s00049-010-0055-

    Article  CAS  Google Scholar 

  • Kalemba D, Marschall H, Bradesi P (2001) Constituents of the essential oil of Solidago gigantea Ait. (giant goldenrod). Flavor Frag J 16:19–26

    Article  CAS  Google Scholar 

  • Keinänen M, Julkunen-Titto R, Mutikainen P, Walls M, Ovaska J, Vapaavuori E (1999) Trade-offs in phenolic metabolism of silver birth: effects of fertilization, defoliation and genotype. Ecology 80:1970–1986

    Article  Google Scholar 

  • Langenheim JH (1994) Higher plant terpenoids: a phytocentric overview of their ecological roles. J Chem Ecol 20:1223–1280

    Article  CAS  PubMed  Google Scholar 

  • Maddox GD, Cappuccino N (1986) Genetic determination of plant susceptibility to an herbivorous insect depends on environmental context. Evolution 40:863–866

    Article  Google Scholar 

  • Maddox GD, Cook RE, Wimberger PH, Gardescu S (1989) Clone structure in four Solidago altissima (Asteraceae) populations: rhizome connections within genotypes. Am J Bot 76:318–326

    Article  Google Scholar 

  • Madritch MD, Hunter MD (2005) Phenotypic variation in oak litter influences short- and long-term nutrient cycling through litter chemistry. Soil Biol Biochem 37:319–327. doi:10.1016/j.soilbio.2004.08.002

    Article  CAS  Google Scholar 

  • Maffei ME (2010) Sites of synthesis, biochemistry and functional role of plant volatiles. S Afr J Bot 76:612–631

    Article  CAS  Google Scholar 

  • Müller M, Buchbauer G (2010) Essential oil components as pheromones: a review. Flavor Frag J. doi:10.1002/ffj.2055

    Google Scholar 

  • Ohgushi T, Ando Y, Utsami S, Craig TP (2011) Indirect interaction webs on tall goldenrod: community consequences for herbivore-induced phenotypes and genetic variation in plants. J Plant Interact 6:147–150. doi:10.1080/17429145.2010.544768

    Article  Google Scholar 

  • Schädler M, Brandl R, Kempel A (2010) Host-plant genotype determines bottom-up effects in an aphid-parasitoid-predator system. Entomol Exp Appl 135:162–169. doi:10.1111/j.1570-7458.2010.00976.x

    Article  Google Scholar 

  • Semiz G, Heijari J, Isik K, Holopainen JK (2007) Variation in needle terpenoids among Pinus sylvestris L. (Pinaceae) provenances from Turkey. Biochem Syst Ecol 35:652–661. doi:10.1016/j.bse.2007.05.013

    Article  CAS  Google Scholar 

  • Tobias RD (1995) An introduction to partial least squares regression. SAS Institute, Cary, pp 1–8

    Google Scholar 

  • Utsumi S, Ando Y, Craig TP, Ohgushi T (2011) Plant genotypic diversity increases population size of a herbivorous insect. Proc R Soc B 278:3108–3115. doi:10.1098/rspb.2011.0239

    Article  PubMed Central  PubMed  Google Scholar 

  • Whitham TG, Young WP, Martinsen GD, Gehring CA, Schweitzer JA, Shuster SM, Wimp GM, Fischer DG, Bailey JK, Lindroth RL, Woolbright S, Kuske CR (2003) Community and ecosystem genetics: a consequence of the extended phenotype. Ecology 84:559–573

    Article  Google Scholar 

  • Whitham TG, Gehring CA, Lamit LJ, Wojtowicz T, Evans LM, Keith AR, Smith DS (2012) Community specificity: life and afterlife effects of genes. Trends Plant Sci 17:271–281. doi:10.1016/j.tplants.2012.01.005

    Article  CAS  PubMed  Google Scholar 

  • Wimp GM, Young WP, Woolbright SA, Martinsen GD, Kein P, Whitham TG (2004) Conserving plant genetic diversity for dependent animal communities. Ecol Lett 7:776–780. doi:10.1111/j.1461-0248.2004.00635.x

    Article  Google Scholar 

  • Wimp GM, Martinsen GD, Floate KD, Bangert RK, Whitham TG (2005) Plant genetic determinants of arthropod community structure and diversity. Evolution 59:61–69

    Article  PubMed  Google Scholar 

  • Wimp GM, Wooley S, Bangert RK, Young WP, Martinsen GD, Kein P, Rehill B, Lindroth RL, Whitham TG (2007) Plant genetics predicts intra-annual variation in phytochemistry and arthropod community structure. Mol Ecol 16:5057–5069. doi:10.1111/j.1365-294X.2007.03544.x

    Article  CAS  PubMed  Google Scholar 

  • Wold S (1984) The collinearity problem problem in linear regression. The partial least squares (pls) approach to generalized inverses. SIAM J Sci Stat Comput 5:735–743

    Article  Google Scholar 

  • Wold S, Sjöström M, Erikson L (2001) PLS-regression: a basic tool of chemometrics. Chemometr Intell Lab Syst 58:109–130

    Article  CAS  Google Scholar 

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Acknowledgments

We thank the field crew at the Gilley Research Station, including Jessica, Eli, and Sophie Howells, Jeff Williams, Bryan Taylor, Peter Blum, and Mathew Swain. Special thanks to Drs. Jennifer Schweitzer and Joseph Bailey at the University of Tennessee-Knoxville for supplying the plants. We also acknowledge the contribution of colleagues and anonymous reviewers, which increased the quality of the manuscript. Support for work with gas chromatography came from Dr. Barkley Sive and David Farrar in the Department of Chemistry at Appalachian State University (ASU). The Cratis Williams Graduate School and Office of Student Research at ASU provided financial support.

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  1. Megan A. Avakian

    Present address: MDB, Inc., 2525 Meridian Parkway, Durham, NC, 27713, USA

Authors and Affiliations

  1. Department of Biology, Appalachian State University, P. O. Box 32027, Boone, NC, 28608-2027, USA

    Ray S. Williams & Megan A. Avakian

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  1. Ray S. Williams
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Correspondence to Ray S. Williams.

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Williams, R.S., Avakian, M.A. Colonization of Solidago altissima by the Specialist Aphid Uroleucon nigrotuberculatum: Effects of Genetic Identity and Leaf Chemistry. J Chem Ecol 41, 129–138 (2015). https://doi.org/10.1007/s10886-015-0546-1

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  • DOI: https://doi.org/10.1007/s10886-015-0546-1

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