Skip to main content
SpringerLink
Log in

Ellagitannins from the Onagraceae Decrease the Performance of Generalist and Specialist Herbivores

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Phenolics have a role in defenses against herbivores, but the defensive functions of specific groups of phenolics are still poorly understood. For example, ellagitannins (a type of hydrolyzable tannin) are predicted to decrease insect herbivore performance, but the effect of different types of ellagitannins on generalist and specialist herbivores has rarely been assessed. Here, we test the effects of the dominant oligomeric ellagitannins of Oenothera biennis and other Onagraceae on herbivore performance. We fed artificial diets containing between 1 and 100 mg/g of polyphenol fractions comprised of varying amounts and compositions of dimeric oenothein B, the trimeric oenothein A and larger oligomers, to one generalist (Spodoptera exigua) and one specialist (Schinia florida) insect herbivore species. We compared the effects of these ellagitannin fractions on herbivore performance to the effects of artificial diet containing total phenolic extracts from O. biennis, which contained these ellagitannins as well as many additional phenolic metabolites including flavonoid glycosides and caffeic acid derivatives. Both the ellagitannin fractions and O. biennis phenolic extracts had strong negative effects on S. exigua and S. florida performance, with stronger effects on the generalist herbivore. Differences between the effects of the various ellagitannin fractions were small and depended on insect life stage. The defensive effects of these ellagitannins were large, with lethal concentrations as low as 0.1% of the diet. These results highlight the important defensive function of ellagitannins against specialist and generalist herbivores and the need to characterize the effects of these understudied phenolics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Agrawal AA, Hastings AP, Johnson MTJ, Maron JL, Salminen J-P (2012) Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338:113–116

    Article  CAS  PubMed  Google Scholar 

  • Anstett DN, Ahern JR, Glinos J, Nawar N, Salminen J-P, Johnson MTJ (2015) Can genetically based clines in plant defense explain greater herbivory at higher latitudes? Ecol Lett 18:1376–1386

    Article  PubMed  Google Scholar 

  • Anstett DN, Chen W, Johnson MTJ (2016) Latitudinal gradients in induced and constitutive resistance against herbivores. J Chem Ecol 42:772–781

    Article  CAS  PubMed  Google Scholar 

  • Appel HM (1993) Phenolics in ecological interactions: the importance of oxidation. J Chem Ecol 19:1521–1552

    Article  CAS  PubMed  Google Scholar 

  • Baert N, Karonen M, Salminen J-P (2015) Isolation, characterisation and quantification of the main oligomeric macrocyclic ellagitannins in Epilobium angustifolium by ultra-high performance chromatography with diode array detection and electrospray tandem mass spectrometry. J Chromatogr A 1419:26–36

    Article  CAS  PubMed  Google Scholar 

  • Baert N, Pellikaan WF, Karonen M, Salminen J-P (2016) A study of the structure-activity relationship of oligomeric ellagitannins on ruminal fermentation in vitro. J Dairy Sci 99:8041–8052

    Article  CAS  PubMed  Google Scholar 

  • Baert N, Kim J, Karonen M, Salminen J-P (2017) Inter-population and inter-organ distribution of the main polyphenolic compounds of Epilobium angustifolium. Phytochemistry 132:54–63

    Article  CAS  Google Scholar 

  • Barbehenn RV, Jones CP, Hagerman AE, Karonen M, Salminen J-P (2006) Ellagitannins have greater oxidative activities than condensed tannins and galloyl glucoses at high pH: potential impact on caterpillars. J Chem Ecol 32:2253–2267

    Article  CAS  PubMed  Google Scholar 

  • Barbehenn R, Weir Q, Salminen J-P (2008) Oxidation of ingested phenolics in the tree-feeding caterpillar Orgyia leucostigma depends on foliar chemical composition. J Chem Ecol 34:748–756

    Article  CAS  PubMed  Google Scholar 

  • Barbehenn RV, Jaros A, Lee G, Mozola C, Weir Q, Salminen J-P (2009) Hydrolyzable tannins as “quantitative defenses”: limited impact against Lymantria dispar caterpillars on hybrid poplar. J Insect Physiol 55:297–304

    Article  CAS  PubMed  Google Scholar 

  • Carmona D, Lajeunesse MJ, Johnson MTJ (2011) Plant traits that predict resistance to herbivores. Funct Ecol 25:358–367

    Article  Google Scholar 

  • Denno RF, McClure MS (1983) Variable plants and herbivores in natural and managed systems. Academic Press, New York

    Google Scholar 

  • Feeny P (1976) Plant apparency and chemical defense. In: Wallace JW, Manse RL (eds) Biochemical interaction between plants and insects. Plenum Press, New York, pp 1–40

    Google Scholar 

  • Felton GW, Summers CB (1995) Antioxidant systems in insects. Arch Insect Biochem 29:187–197

  • Fritz RS, Simms EL (1992) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55:481–504

    Article  CAS  PubMed  Google Scholar 

  • Johnson MTJ (2011) Evolutionary ecology of plant defenses against herbivores. Funct Ecol 25:305–311

    Article  Google Scholar 

  • Johnson MTJ, 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 MTJ, Agrawal AA (2007) Covariation and composition of arthropod species across plant genotypes of evening primrose (Oenothera biennis). Oikos 116:941–956

    Google Scholar 

  • Johnson MTJ, Agrawal AA, Maron JL, Salminen J-P (2009) Heritability, covariation and natural selection on 24 traits of common evening primrose (Oenothera biennis) from a field experiment. J Evol Biol 22:1295–1307

    Article  CAS  PubMed  Google Scholar 

  • Johnson MTJ, Ives AR, Ahern J, Salminen J-P (2014) Macroevolution of plant defenses against herbivores in the evening primroses. New Phytol 203:267–279

    Article  CAS  PubMed  Google Scholar 

  • Karonen M, Parker J, Agrawal AA, Salminen J-P (2010) First evidence of hexameric and heptameric ellagitannins in plants detected by liquid chromatography/electrospray ionisation mass spectrometry. Rapid Commun Mass Spectrom 24:3151–3156

    Article  CAS  PubMed  Google Scholar 

  • Karonen M, Oraviita M, Mueller-Harvey I, Salminen J-P, Green RJ (2015) Binding of an oligomeric ellagitannin series to bovine serum albumin (BSA): analysis by isothermal titration calorimetry (ITC). J Agric Food Chem 63:10647–10654

    Article  CAS  PubMed  Google Scholar 

  • Kim J, Pälijärvi M, Karonen M, Salminen J-P (2018) Oxidatively active plant phenolics detected by UHPLC-DAD-MS after enzymatic and alkaline oxidation. J Chem Ecol 44:483–496

    Article  CAS  PubMed  Google Scholar 

  • McArt SH, Halitschke R, Salminen J-P, Thaler JS (2013) Leaf herbivory increases plant fitness via induced resistance to seed predators. Ecology 94:966–975

    Article  Google Scholar 

  • Moilanen J, Salminen J-P (2008) Ecologically neglected tannins and their biologically relevant activity: chemical structures of plant ellagitannins reveal their in vitro oxidative activity at high pH. Chemoecology 18:73–83

    Article  CAS  Google Scholar 

  • Moilanen J, Koskinen P, Salminen J-P (2015) Distribution and content of ellagitannins in Finnish plant species. Phytochemistry 116:188–197

    Article  CAS  PubMed  Google Scholar 

  • Niemetz R, Gross GG (2005) Enzymology of gallotannin and ellagitannin biosynthesis. Phytochemistry 66:2001–2011

    Article  CAS  PubMed  Google Scholar 

  • Normark BB, Johnson NA (2011) Niche explosion. Genetica 139:551–564

    Article  PubMed  Google Scholar 

  • Parker J, Salminen J-P, Agrawal AA (2012) Evolutionary potential of root chemical defense: genetic correlations with shoot chemistry and plant growth. J Chem Ecol 38:992–995

    Article  CAS  PubMed  Google Scholar 

  • Quideau S, Feldman KS (1996) Ellagitannin chemistry. Chem Rev 96:475–504

    Article  CAS  PubMed  Google Scholar 

  • R Core Development Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rosenthal GA, Berenbaum MR (1991) Herbivores: their interactions with secondary plant metabolites. Volume II: Ecological and evolutionary processes. Academic Press, San Diego

    Google Scholar 

  • Roslin T, Salminen J-P (2008) Specialization pays off: contrasting effects of two types of tannins on oak specialist and generalist moth species. Oikos 117:1560–1568

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Salminen J-P, Ossipov V, Haukioja E, Pihlaja K (2001) Seasonal variation in the content of hydrolyzable tannins in leaves of Betula pubescens. Phytochemistry 57:15–22

    Article  CAS  PubMed  Google Scholar 

  • Salminen J-P, Ossipov V, Pihlaja K (2002) Distribution of hydrolyzable tannins in the foliage of Finnish birch species. Z Naturforsch C 57:248–256

    Article  CAS  PubMed  Google Scholar 

  • Salminen J-P, Roslin T, Karonen M, Sinkkonen J, Pihlaja K, Pulkkinen P (2004) Seasonal variation in the content of hydrolyzable tannins, flavonoid glycosides, and proanthocyanidins in oak leaves. J Chem Ecol 30:1693–1711

    Article  CAS  PubMed  Google Scholar 

  • Salminen J-P, Karonen M, Sinkkonen J (2011) Chemical ecology of tannins: recent developments in tannin chemistry reveal new structures and structure-activity patterns. Chemistry 17:2806–2816

    Article  CAS  PubMed  Google Scholar 

  • Sargent TD (1969) Behavioral adaptations of cryptic moths. V. Preliminary studies on an anthophilous species, Schinia florida (Noctuidae). J New York Entomol Soc 77:123–128

    Google Scholar 

  • Wallace J (1976) Biochemical interaction between plants and insects. Plenum, New York

    Book  Google Scholar 

  • Walters D (2011) Plant defense: warding off attack by pathogens, herbivores and parasitic plants. Wiley, Oxford

    Google Scholar 

  • Yarnes CT, Boecklen WJ, Tuominen K, Salminen J-P (2006) Defining phytochemical phenotypes: size and shape analysis of phenolic compounds in oaks (Fagaceae, Quercus) of the Chihuahuan Desert. Can J Bot 84:1233–1248

    Article  Google Scholar 

Download references

Acknowledgements

We thank X. Zhao, J. Anstett, E. Kibkalo, J. Kim and T. Lempiäinen. This project was funded by an NSERC CGS-D Vanier, and a NSERC Banting Fellowship to D. Anstett. The project was further funded by an NSERC Discovery Grant, the Canadian Foundation for Innovation, and Ontario’s Early Researcher Award to M. Johnson. J.-P. Salminen was supported by grant no. 258992 from the Academy of Finland.

Author information

Author notes

  1. Daniel N. Anstett

    Present address: Biodiversity Research Centre and Department of Botany, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

Authors and Affiliations

  1. Department of Biology, University of Toronto Mississauga, Mississauga, ON, L5L 1C6, Canada

    Daniel N. Anstett, Caitlyn D’Souza & Marc T. J. Johnson

  2. Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, M5S 3B2, Canada

    Daniel N. Anstett & Marc T. J. Johnson

  3. AgroSup Dijon, 21000, Dijon, Burgundy, France

    Iris Cheval

  4. Department of Chemistry, University of Turku, FI-20014, Turku, Finland

    Juha-Pekka Salminen

Authors
  1. Daniel N. Anstett
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Iris Cheval
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Caitlyn D’Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Juha-Pekka Salminen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marc T. J. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daniel N. Anstett.

Electronic supplementary material

ESM 1

(DOCX 35 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Anstett, D.N., Cheval, I., D’Souza, C. et al. Ellagitannins from the Onagraceae Decrease the Performance of Generalist and Specialist Herbivores. J Chem Ecol 45, 86–94 (2019). https://doi.org/10.1007/s10886-018-1038-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-018-1038-x

Keywords

Search

Navigation