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Plant and Soil

, Volume 293, Issue 1–2, pp 153–176 | Cite as

The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions

  • Robert S. Boyd
regular Article

Abstract

Elemental hyperaccumulation may have several functions, including plant defense against natural enemies. A total of 34 studies, including 72 experimental tests, have been conducted to date. At least some tests have demonstrated defense by hyperaccumulated As, Cd, Ni, Se and Zn, but relatively few plant taxa and natural enemies have been investigated. Defense by hyperaccumulated Ni has been shown for most leaf/root chewing herbivores and pathogens tested (20 of 26 tests) but not for herbivores of other feeding modes (1 of 8 tests). Most tests (5 of 6) using Ni concentrations below accumulator levels found no defensive effect, and the single test using plants in the accumulator range also found no effect. For Zn, mixed results have been reported for both hyperaccumulator (3 of 6 tests showed defense) and accumulator levels (3 of 4 tests showed defense). These tests have focused exclusively on leaf chewing/scraping herbivores: no herbivores of other feeding modes, or pathogens, have been tested. Both hyperaccumulator and accumulator concentrations of Se generally have shown defensive effects (12 of 14 tests). Most (75%) of these positive results used plants with accumulator Se concentrations. The three tests of Cd showed defensive effects in two cases, one for hyperaccumulator and one for sub-accumulator Cd concentrations. Arsenic has been tested only once, and was found effective against a leaf-chewing herbivore at a concentration much less than the hyperaccumulator level. Defense studies have used a variety of experimental approaches, including choice and no-choice experiments as well as experiments that use artificial diet or growth media. Investigations of hyperaccumulation as a defense against natural enemies have led to two emerging questions. First, what is the minimum concentration of an element sufficient for defense? Evidence suggests that plants other than hyperaccumulators (such as accumulators) may be defended by elements against some natural enemies. Second, do the effects of an element combine with the effects of organic defensive compounds in plants to produce enhanced joint defensive effects? Recent investigation of this “joint effects hypothesis,” using Ni and secondary plant compounds in artificial insect diet, has demonstrated joint effects. Initial answers to both these questions suggest that defensive effects of elements in plants are more widespread than previously believed. These results also suggest an evolutionary pathway by which elemental hyperaccumulation may have evolved from accumulation. In this “defensive enhancement” scenario, defensive benefits of elevated levels of elements may have led to stepwise increases in element concentrations that further magnified these benefits. This series of steps could have led to increased accumulation, and ultimately hyperaccumulation, of elements by plants.

Keywords

Elemental plant defense Heavy metal Herbivory Hyperaccumulation Plant pathogen 

Notes

Acknowledgments

The author thanks Micky Eubanks and two anonymous reviewers for helpful suggestions on an earlier version of the manuscript.

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© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Department of Biological SciencesAuburn UniversityAuburnUSA

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