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Testing the Joint Effects Hypothesis of Elemental Defense using Spodoptera Exigua

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Abstract

Metal hyperaccumulation may be an elemental defense, in which high concentrations of a metal in plant tissues decrease herbivore survival or growth rate. The Joint Effects Hypothesis suggests that a combination of metals, or a combination of a metal with an organic compound, may have an enhanced defensive effect. The enhancement may be additive or synergistic: in either case the concentration of a particular metal necessary to provide a defensive benefit for the plant is lowered. We tested the Joint Effects Hypothesis using Spodoptera exigua (beet armyworm) neonates fed artificial diets. Metal + metal experiments utilized diets amended with metal pairs, using four metals commonly hyperaccumulated by plants (Co, Cu, Ni, and Zn). We also conducted metal + organic compound experiments, pairing each metal with nicotine, mustard seed powder, or tannic acid. We tested for joint effects using both lethal (LC20 levels) and sublethal concentrations (10–25 % reduced larval weight) of the chemicals tested. For all experiments, either additive or synergistic effects were found. Of the metal + metal pairs tested, three (Co + Cu, Cu + Zn, and Ni + Zn) were synergistic in lethal concentration tests and only Co + Cu was synergistic in sublethal tests. For metal + organic combination lethal tests, synergism occurred for all combinations except for Co or Ni + nicotine, Ni + mustard seed powder, and Zn + nicotine. For sublethal tests, Zn + all three organic chemicals, Co + mustard seed powder or tannic acid, and Cu + nicotine, were synergistic. These results support the Joint Effects Hypothesis, suggesting that metals combined with other metals or organic compounds may be more effective against herbivores than individual metals.

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References

  • Abivardi C, Benz G (1984) Tests with the extracts of 21 medicinal plants for antifeedant activity against larvae of Pieris brassicae L. (Lep., Pieridae). Bull Soc Entomol Suisse 57:383–392

    Google Scholar 

  • Ali MI, Luttrell RG (2009) Response estimates for assessing Heliothine susceptibility to Bt toxins. J Econ Entomol 102:1935–1947

    Article  CAS  PubMed  Google Scholar 

  • Anilkumar KJ, Sivasupramaniam S, Head G, Orth R, Van Santen E, Moar WJ (2009) Synergistic interactions between Cry1Ac and natural cotton defenses limit survival of Cry1Ac-resistant Helicoverpa zea (Lepidoptera: Noctuidae) on Bt cotton. J Chem Ecol 35:785–795

    Article  CAS  PubMed  Google Scholar 

  • Bennett RN, Wallsgrove RM (1994) Secondary metabolites in plant defense mechanisms. New Phytol 127:617–633

    Article  CAS  Google Scholar 

  • Boyd RS (2014) Ecology and evolution of metal-hyperaccumulating plants. In: Rajakaruna N, Boyd RS, Harris TB (eds) Plant ecology and evolution in harsh environments. Nova, Happauge, pp 227–241

    Google Scholar 

  • Boyd RS (2012) Plant defense using toxic inorganic ions: conceptual models of the defensive enhancement and joint effects hypotheses. Plant Sci 195:88–95

    Article  CAS  PubMed  Google Scholar 

  • Boyd RS (2007) The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant Soil 293:153–176

    Article  CAS  Google Scholar 

  • Boyd RS, Martens SN (1992) The raison d’etre for metal hyperaccumulation by plants. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept Limited, Andover, pp 279–289

    Google Scholar 

  • Boyd RS, Moar WJ (1999) The defensive function of Ni in plants: response of the polyphagous herbivore Spodoptera exigua (Lepidoptera: Noctuidae) to hyperaccumulator and accumulator species of Streptanthus (Brassicaceae). Oecologia 118:218–224

    Article  Google Scholar 

  • Capinera JL (2006) Beet Armyworm, Spodoptera exigua (Hübner)(Insecta: Lepidoptera: Noctuidae). Entomology and Nematology Department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida

    Google Scholar 

  • Cheruiyot DJ, Boyd RS, Moar WJ (2013) Exploring lower limits of plant elemental defense by cobalt, copper, nickel and zinc. J Chem Ecol 39:666–674

    Article  CAS  PubMed  Google Scholar 

  • Clancy KM, Price PW (1987) Rapid herbivore growth enhances enemy attack: sublethal plant defenses remain a paradox. Ecology 68:733–737

    Article  Google Scholar 

  • Coleman CM, Boyd RS, Eubanks MD (2005) Extending the elemental defense hypothesis: dietary metal concentrations below hyperaccumulator levels could harm herbivores. J Chem Ecol 31:1669–1681

    Article  CAS  PubMed  Google Scholar 

  • Davis MA, Boyd RS (2000) Dynamics of Ni-based defense and organic defenses in the Ni hyperaccumulator, Streptanthus polygaloides (Brassicaceae). New Phytol 146:11–217

    Google Scholar 

  • Davis MA, Pritchard SG, Boyd RS, Prior SA (2001) Developmental and induced responses of nickel-based and organic defenses of nickel-hyperaccumulating shrub, Psychotria douarrei. New Phytol 150:49–58

    Article  CAS  Google Scholar 

  • Dyer LA (2011) New synthesis—Back to the future: new approaches and directions in chemical studies of coevolution. J Chem Ecol 37:669

    Article  CAS  PubMed  Google Scholar 

  • Gershenzon J, Fontana A, Burow M, Wittstock U, Degenhardt J (2012) Mixtures of plant secondary metabolites: metabolic origins and ecological benefits. In: Iason GR, Dicke M, Hartley SE (eds) The ecology of plant secondary metabolites: from genes to global processes. Cambridge University Press, New York, pp 56–77

    Chapter  Google Scholar 

  • Greenberg SM, Sappington TW, Legaspi BC, Liu T-X, Sétamou M (2001) Feeding and life history of Spodoptera exigua (Lepidoptera: Noctuidae) on different host plants. Ann Entomol Soc Am 94:566–575

    Article  Google Scholar 

  • Hodgson E, Das PC, Cho TM, Rose RL (2008) Chapter 10. Phase 1 metabolism of toxicants and metabolic interactions. In: Stuart RC, Hodgson E (eds) Molecular and biochemical toxicology, 4th edn. John Wiley and Sons, Hoboken, pp 173–203

    Chapter  Google Scholar 

  • Hörger AC, Fones HN, Preston GM (2013) The current status of the elemental defense hypothesis in relation to pathogens. Front Plant Sci. doi:10.3389/fpls.2013.00395

    PubMed Central  PubMed  Google Scholar 

  • Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    Article  CAS  PubMed  Google Scholar 

  • Jaffré T, Brooks RR, Lee J, Reeves RD (1976) Sebertia acuminata: a hyperaccumulator of nickel from New Caledonia. Science 193:579–580

    Article  PubMed  Google Scholar 

  • Jensen PD, Johnson LR, Trumble JT (2006) Individual and joint actions of selenate and methylmercury on the development and survival of insect detritivore Megaselia scalaris. Arch Environ Contam Toxicol 50:523–530

    Article  CAS  PubMed  Google Scholar 

  • Jensen PD, Sorensen MA, Walton WE, Trumble JT (2007) Lethal and sublethal responses of an aquatic insect Culex quinquefasciatus (Diptera: Culicidae) challenged with individual and joint exposure to dissolved sodium selenite and methylmercury chloride. Environ Toxicol 22:287–294

    Article  CAS  PubMed  Google Scholar 

  • Jhee EM, Boyd RS, Eubanks MD (2006) Effectiveness of metal-metal and metal-organic compound combinations against Plutella xylostella (Lepidoptera: Plutellidae): implications for plant elemental defense. J Chem Ecol 32:239–259

    Article  CAS  PubMed  Google Scholar 

  • Kazemi-Dinan A, Thomaschky S, Stein RJ, Krämer U, Müller C (2014) Zinc and cadmium hyperaccumulation act as deterrents towards specialist herbivores and impede the performance of a generalist herbivore. New Phytol. doi:10.1111/nph.12663

    PubMed  Google Scholar 

  • Li G, Pang Y, Chen Q, Su Z, Wen X (2002) Studies on the artificial diet for Beet Armyworm, Spodoptera exigua. Chin J Biol Control 18:132–134

    CAS  Google Scholar 

  • Martens SN, Boyd RS (1994) The ecological significance of nickel hyperaccumulation: a plant chemical defense. Oecologia 98:379–384

    Article  Google Scholar 

  • Mazid M, Khan TA, Mohammad F (2011) Role of secondary metabolites in defense mechanisms of plants. Biol Med 3(2):232–249

    CAS  Google Scholar 

  • Mithöfer Z, Boland W (2012) Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63:431–450

    Article  PubMed  Google Scholar 

  • Morrison RS, Brooks RR, Reeves RD, Malaisse F (1979) Copper and cobalt uptake by metallophytes from Zaïre. Plant Soil 53:535–539

    Article  CAS  Google Scholar 

  • Moyes CL, Collin HA, Britton G, Raybould AF (2000) Glucosinolates and differential herbivory in wild populations of Brassica oleracea. J Chem Ecol 26:2625–2641

    Article  CAS  Google Scholar 

  • Nelson AC, Kursar TA (1999) Interactions among plant defense compounds: a method for analysis. Chemoecology 2:81–92

    Article  Google Scholar 

  • Nomura M, Itioka T (2002) Effects of synthesized tannin on the growth and survival of a generalist herbivorous insect, the common cutworm, Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Appl Entomol Zool 37:285–289

    Article  CAS  Google Scholar 

  • Price PW, Bouton CE, Gross P, McPherson BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Evol Syst 11:41–65

    Article  Google Scholar 

  • Rasmann S, Agrawal AA (2009) Plant defense against herbivory: progress in identifying synergism, redundancy, and antagonism between resistance traits. Curr Opin Plant Biol 12:473–478

    Article  CAS  PubMed  Google Scholar 

  • Reeves RD, Baker AJM (2000) Metal-accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. John Wiley and Sons, New York, pp 193–229

    Google Scholar 

  • Reeves RD, Baker AJM (1984) Studies on metal uptake by plants from serpentine and non-serpentine populations of Thlaspi goesingense Halacsy (Cruciferae). New Phytol 98:191–204

    Article  CAS  Google Scholar 

  • Robertson JL, Preisler HK, Russell RM (2007) PoloPlus: Probit and Logit Analysis. LeOra Software, Berkeley

    Google Scholar 

  • Salama HS, Foda MS, Zaki FN, Moawad S (1984) Potency of combinations of Bacillus thuringiensis and chemical insecticides on Spodoptera littoralis (Lepidoptera: Noctuidae). J Econ Entomol 77:885–890

    Article  CAS  Google Scholar 

  • Sambamurty AVSS (2006) A textbook of plant pathology. I.K. International Pvt. Ltd., New Delhi

    Google Scholar 

  • SAS Institute (2005) StatView 5.0. Thomson—Brooks/Cole, Belmont

    Google Scholar 

  • Tang Y-T, Qiu R-L, Zeng X-W, Ying R-R, Yu F-M, Zhou X-Y (2009) Lead, zinc, cadmium hyperaccumulation and growth stimulation in Arabis paniculata Franch. Environ Exp Bot 66:126–134

    Article  CAS  Google Scholar 

  • Thamthiankul S, Moar WJ, Miller ME, Panbangred W (2004) Improving the insecticidal activity of Bacillus thuringiensis subsp. aizawai against Spodoptera exigua by chromosomal expression of a chitinase gene. Appl Microbiol Biotechnol 65:183–192

    Article  CAS  PubMed  Google Scholar 

  • Tolrá RS, Poschenrieder C, Alonso R, Barcélo D, Barcélo J (2001) Influence of zinc hyperaccumulation on glucosinolates in Thlaspi caerulescens. New Phytol 151:621–626

    Article  Google Scholar 

  • Trumble JT, Kund GS, White KK (1998) Influence of form and quantity of selenium on the development and survival of an insect herbivore. Environ Pollut 101:175–182

    Article  CAS  PubMed  Google Scholar 

  • Van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334

    Article  Google Scholar 

  • Wink M (2008) Plant secondary metabolism: diversity, function and its evolution. Nat Prod Commun 3:1205–1216

    CAS  Google Scholar 

  • Wise MJ, Fox RJ, Abrahamson WG (2006) Disarming the paradox of sublethal plant defense against insects: Trirhabda virgata larval development time and leaf tissue loss on Solidago altissima. Entomol Exp Appl 120:77–87

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by Alabama Agricultural Experiment Station Project No. ALA021-1-09008.

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Correspondence to Robert S. Boyd.

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Cheruiyot, D.J., Boyd, R.S. & Moar, W. Testing the Joint Effects Hypothesis of Elemental Defense using Spodoptera Exigua . J Chem Ecol 41, 168–177 (2015). https://doi.org/10.1007/s10886-015-0553-2

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  • DOI: https://doi.org/10.1007/s10886-015-0553-2

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