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Elemental defense of nickel hyperaccumulator seeds against a generalist insect granivore

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  • Ultramafic Ecosystems: Proceedings of the 9th International Conference on Serpentine Ecology
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Ecological Research

Abstract

Hyperaccumulation has been proposed as an elemental defense against herbivores; however, few studies have examined seed defense. This study included two annual Streptanthus species (Brassicaceae) from California serpentine soils: a non-hyperaccumulator (S. insignis) and three populations (representing Y, P, and U morphs) of a Ni hyperaccumulator (S. polygaloides). Adults of the generalist seed herbivore Tribolium confusum (Coleoptera: Tenebrionidae) were fed either whole or cut seeds, survival was recorded for 7 weeks, and Ni concentrations of both beetles and seeds were determined using ICP-OES. Survival analysis showed significantly more rapid mortality for beetles consuming S. polygaloides seeds compared to those consuming S. insignis. Mortality of beetles fed whole S. polygaloides seeds was more rapid than those fed cut S. polygaloides seeds. Seeds of the S. polygaloides populations contained approximately 300 µg Ni g−1 whereas S. insignis contained approximately 5 µg Ni g−1. Beetles fed whole S. polygaloides seeds contained more than 2.5-fold greater Ni concentrations than those fed cut seeds (approximately 60 and 25 µg Ni g−1, respectively), whereas beetles fed either cut or whole S. insignis seeds contained < 0.3 µg Ni g−1. An artificial diet study, using Ni-amended cornmeal, confirmed that diet Ni concentrations greater than 240 µg Ni g−1 were toxic to T. confusum. We conclude that Ni in S. polygaloides seeds can act as an elemental defense against seed herbivores even at 300 µg Ni g−1, a level below the 1000 µg Ni g−1 hyperaccumulation threshold concentration.

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References

  • Alonso-Amelot ME, Avila JL, Otero LD, Mora F, Wolff B (1994) A new bioassay for testing plant extracts and pure compounds using red flour beetle Tribolium castaneum Herbst. J Chem Ecol 20:1161–1177

    Article  PubMed  CAS  Google Scholar 

  • Baker AJM, McGrath SP, Reeves RD, Smith JAC (2000) Metal hyperaccumulator plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal polluted soils. In: Terry N, Banuelos GS (eds) Phytoremediation of contaminated soil and water. CRC Press, Boca Raton, pp 85–107

    Google Scholar 

  • Baldwin BG, Goldman DH, Keil DJ, Patterson R, Rosatti TJ, Wilken DH (2012) The Jepson manual: vascular plants of California, 2nd edn. University of California Press, Berkeley (CA)

    Google Scholar 

  • Barillas JRV, Quinn CF, Freeman JL, Lindblom SD, Fakra SC, Marcus MA, Gilligan TM, Alford ER, Wangeline AL, Pilon-Smits EAH (2012) Selenium distribution and speciation in the hyperaccumulator Astragalus bisulcatus and associated ecological partners. Plant Physiol 159:1834–1844

    Article  CAS  Google Scholar 

  • Bhatia NP, Orlic I, Siegele R, Ashwath N, Baker AJM, Walsh KB (2003) Elemental mapping using PIXE shows the main pathway of nickel movement is principally symplastic within the fruit of the hyperaccumulator Stackhousia tryonii. New Phytol 160:479–488

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

    Article  PubMed  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 Science Publishers, Hauppauge, pp 227–241

    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, GB-Andover, pp 279–289

    Google Scholar 

  • Boyd RS, Martens SN (1994) Nickel hyperaccumulated by Thlaspi montanum var. montanum is acutely toxic to an insect herbivore. Oikos 70:21–25

    Article  CAS  Google Scholar 

  • Boyd RS, Martens SN (1998) The significance of metal hyperaccumulation for biotic interactions. Chemoecology 8:1–7

    Article  CAS  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  PubMed  Google Scholar 

  • Boyd RS, Davis MA, Wall MA, Balkwill K (2002) Nickel defends the South African hyperaccumulator Senecio coronatus (Asteraceae) against Helix aspersa (Mollusca: Pulmonidae). Chemoecology 12:91–97

    Article  CAS  Google Scholar 

  • Boyd RS, Wall MA, Santos SR, Davis MA (2009) Variation of morphology and elemental concentrations in the California nickel hyperaccumulator Streptanthus polygaloides (Brassicaceae). Northeast Nat 16:21–38

    Article  Google Scholar 

  • Cacho NI, Burrell AM, Pepper AE, Strauss SY (2013) Novel nuclear markers inform the systematics and the evolution of serpentine use in Streptanthus and allies (Thelypodieae, Brassicaceae). Mol Phylogenet Evol 72:71–81

    Article  CAS  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  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899

    Article  PubMed  CAS  Google Scholar 

  • Freeman JL, Marcus MA, Fakra SC, Devonshire J, McGrath SP, Quinn CF, Pilon-Smits EAH (2012) Selenium hyperaccumulator plants Stanleya pinnata and Astragalus bisulcatus are colonized by Se-resistant, Se-excluding wasp and beetle seed herbivores. PLoS ONE 7:e50516

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fürstenberg-Hägg J, Zagrobelny M, BakInt S (2013) Plant defense against insect herbivores. J Mol Sci 14:10242–10297

    Article  CAS  Google Scholar 

  • Gavloski JE, Lamb RJ (2000) Specific impacts of herbivores: comparing diverse insect species on young plants. Environ Entomol 29:1–7

    Article  Google Scholar 

  • Goncalves MT, Goncalves SC, Portuga A, Silva S, Sousa JP, Freitas H (2007) Effects of nickel hyperaccumulation in Alyssum pintodasilvae on model arthropods representatives of two trophic levels. Plant Soil 293:177–188

    Article  CAS  Google Scholar 

  • Gowda JH (1996) Spines of Acacia tortilis: what do they defend and how? Oikos 77:279–284

    Article  Google Scholar 

  • Hanley ME, Lamont BB (2001) Herbivory, serotiny and seedling defence in Western Australian Proteaceae species. Oecologia 126:409–417

    Article  PubMed  Google Scholar 

  • Hanley ME, Lamont BB, Fairbanks MM, Rafferty CM (2007) Plant structural traits and their role in anti-herbivore defence. Perspect Plant Ecol Evol Syst 8:157–178

    Article  Google Scholar 

  • Hanson B, Garifullina GF, Lindblom SD, Wangeline A, Ackley A, Kramer K, Norton AP, Lawrence CB, Pilon-Smits EAH (2003) Selenium accumulation protects Brassica juncea from invertebrate herbivory and fungal infection. New Phytol 159:461–469

    Article  CAS  Google Scholar 

  • Haouas D, Cioni PL, Halima-Kamel MB, Flamini G, Hamouda MHB (2012) Chemical composition and bioactivities of three Chrysanthemum essential oils against Tribolium confusum (du Val) (Coleoptera: Tenebrionidae). J Pest Sci 85:367–379

    Article  Google Scholar 

  • Hashemi SM, Safavi SA (2012) Chemical constituents and toxicity of essential oils of oriental arborvitae, Platycladus orientalis (L.) Franco, against three stored-product beetles. Chil J Agr Res 72:188–194

    Article  Google Scholar 

  • Hulme PE, Benkman CW (2002) Granivory. In: Herrera CM, Pellmyr O (eds) Plant-animal interactions: an evolutionary approach. Blackwell Science, Padstow, pp 132–154

    Google Scholar 

  • Janzen DH (1971) Seed predation by animals. Annu Rev Ecol Syst 2:465–492

    Article  Google Scholar 

  • Jhee EM, Boyd RS, Eubanks MD, Davis MA (2006) Nickel hyperaccumulation by Streptanthus polygaloides protects against the folivore Plutella xylostella (Lepidoptera: Plutellidae). Plant Ecol 183:91–104

    Article  Google Scholar 

  • Jiang RF, Ma DY, Zhao FJ, McGrath SP (2005) Cadmium hyperaccumulation protects Thlaspi caerulescens from leaf feeding damage by thrips (Frankliniella occidentalis). New Phytol 167:805–814

    Article  PubMed  CAS  Google Scholar 

  • Kachenko AG, Bhatia NP, Siegele R, Walsh KB, Singh B (2009) Nickel, Zn and Cd localization in seeds of metal hyperaccumulators using µ-PIXE spectroscopy. Nucl Instr Meth Phys Res B 267:2176–2180

    Article  CAS  Google Scholar 

  • Kant MR, Jonckheere W, Knegt B, Lemos F, Liu J, Schimmel BCJ, Villarroel CA, Ataide LMS, Dermauw W, Glas JJ, Egas M, Janssen A, Van Leeuwen T, Schuurink RC, Sabelis MW, Alba JM (2015) Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities. Ann Bot 115:1015–1051

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Latorre L, Larrinaga AR, Santamaria L (2013) Combined impact of multiple exotic herbivores on different life stages of an endangered plant endemism, Medicago citrina. J Ecol 101:107–117

    Article  Google Scholar 

  • Maron JL, Crone E (2006) Herbivory: effects of plant abundance, distribution and population growth. Proc R Soc Lond [Biol] 273:2575–2584

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Massey FP, Hartley SE (2009) Physical defences wear you down: progressive and irreversible impacts of silica on insect herbivores. J Anim Ecol 78:281–291

    Article  PubMed  Google Scholar 

  • Mortensen B (2013) Plant resistance against herbivory. Nature Edu Knowl 4:5

    Google Scholar 

  • Pollard AJ, Baker AJM (1997) Deterrence of herbivory by zinc hyperaccumulation in Thlaspi caerulescens. New Phytol 135:655–658

    Article  CAS  Google Scholar 

  • Pope N, Fong M, Boyd RS, Rajakaruna N (2013) The role of elevation and soil chemistry in the distribution and ion accumulation of floral morphs of Streptanthus polygaloides Gray (Brassicaceae), a Californian nickel hyperaccumulator. Plant Ecol Divers 3:421–432

    Google Scholar 

  • Price PW, Bouton CE, Gross P, McPheron 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 

  • Psaras GK, Manetas Y (2001) Nickel localization in seeds of the metal hyperaccumulator Thlaspi pindicum Hausskn. Ann Bot 88:513–516

    Article  CAS  Google Scholar 

  • R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Reeves RD, Brooks RR, Macfarlane RM (1981) Nickel uptake by Californian Streptanthus and Caulanthus with particular reference to the hyperaccumulator S. polygaloides A. Gray (Brassicaceae). Am J Bot 68:708–712

    Article  CAS  Google Scholar 

  • Saltz D, Ward D (2000) Responding to a three-pronged attack: desert lilies subject to herbivory by dorcas gazelles. Plant Ecol 148:127–138

    Article  Google Scholar 

  • Strauss SY (1991) Direct, indirect, and cumulative effects of three native herbivores on a shared host plant. Ecology 72:543–558

    Article  Google Scholar 

  • Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185

    Article  PubMed  CAS  Google Scholar 

  • Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17:278–285

    Article  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  CAS  Google Scholar 

  • Van der Ent A, Erskine PD, Sumail S (2015a) Ecology of nickel hyperaccumulator plants from ultramafic soils in Sabah (Malaysia). Chemoecology 25:243–259

    Article  CAS  Google Scholar 

  • Van der Ent A, Rajakaruna N, Boyd R, Echevarria G, Repin R, Williams D (2015b) Global research on ultramafic (serpentine) ecosystems (8th International Conference on Serpentine Ecology in Sabah, Malaysia): a summary and synthesis. Aust J Bot 63:1–16

    Google Scholar 

  • Vanderwall SB, Forget P, Lambert JE, Hulme PE (2005) Seed fate pathways: filling the gap between parent and offspring. In: Lambert JE, Hulme PE, Vanderwall SB (eds) Seed fate: predation, dispersal, and seedling establishment. CABI Publishing, Wallingford, pp 1–8

    Google Scholar 

  • Vesk PA, Reichman SM (2009) Hyperaccumulators and herbivores-a Bayesian meta-analysis of feeding choice trials. J Chem Ecol 35:289–296

    Article  PubMed  CAS  Google Scholar 

  • Wall MA, Boyd RS (2006) Melanotrichus boydi (Hemiptera: Miridae) is a specialist on the nickel hyperaccumulator Streptanthus polygaloides (Brassicaceae). Southwest Nat 51:481–489

    Article  Google Scholar 

  • Walter VE (1990) Stored product pests. In: Story K, Moreland D (eds) Handbook of Pest Control Franzak & Foster Co. Cleveland, OH, pp 526–529

    Google Scholar 

  • War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320

    Article  PubMed  PubMed Central  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 

  • Wu Y, Zhang W, Wang P, Yang K, Huang D, Wei J, Tian Z, Bai J, Du S (2015) Contact toxicity and repellency of the essential oil of Liriope muscari (DECN.) Bailey against three insect tobacco storage pests. Molecules 20:1676–1685

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by the USDA National Institute of Food and Agriculture, Hatch Project 1007072.

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Correspondence to Katherine Anne Mincey.

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Mincey, K.A., Boyd, R.S. Elemental defense of nickel hyperaccumulator seeds against a generalist insect granivore. Ecol Res 33, 561–570 (2018). https://doi.org/10.1007/s11284-018-1583-3

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