Nickel hyperaccumulation as an elemental defense of Streptanthus polygaloides (Brassicaceae): influence of herbivore feeding mode

Abstract

Summary• No study of a single nickel (Ni) hyperaccumulator species has investigated the impact of hyperaccumulation on herbivores representing a variety of feeding modes.• Streptanthus polygaloides plants were grown on high-or low-Ni soils and a series of no-choice and choice feeding experiments was conducted using eight arthropod herbivores. Herbivores used were two leaf-chewing folivores (the grasshopper Melanoplus femurrubrum and the lepidopteran Evergestis rimosalis ), a dipteran rhizovore (the cabbage maggot Delia radicum ), a xylem-feeder (the spittlebug Philaenus spumarius ), two phloem-feeders (the aphid, Lipaphis erysimi and the spidermite Trialeurodes vaporariorum ) and two cell-disruptors (the bug Lygus lineolaris and the whitefly Tetranychus urticae ).• Hyperaccumulated Ni significantly decreased survival of the leaf-chewers and rhizovore, and significantly reduced population growth of the whitefly cell-disruptor. However, vascular tissue-feeding insects were unaffected by hyperaccumulated Ni, as was the bug cell-disruptor.• We conclude that Ni can defend against tissue-chewing herbivores but is ineffective against vascular tissue-feeding herbivores. The effects of Ni on cell-disruptors varies, as a result of either variation of insect Ni sensitivity or the location of Ni in S. polygaloides cells and tissues.

A Ni hyperaccumulator and a congeneric non-accumulator reveal equally effective defenses against herbivory

“…1A-C). Results from the A. pintodasilvae trials provide circumstantial support to the hypothesis that Ni defends this hyperaccumulator species from herbivory in agreement with previous studies on Ni hyperaccumulation Boyd and Jhee, 2005;Boyd and Moar, 1999;Gonçalves et al, 2007;Jhee et al, 2005Jhee et al, , 2006aMartens and Boyd, 1994). However, A. simplex also induced a significant inhibition of food intake and deterred feeding in T. castaneum despite the low concentration of Ni in its leaves (65 ± 26 μg g −1 dry weight).…”

Complexation and Toxicity of Copper in Higher Plants. I. Characterization of Copper Accumulation, Speciation, and Toxicity inCrassula helmsiias a New Copper Accumulator

“…These plants, which accumulate up to several percent of heavy metals in the dry mass of their aboveground parts, are called "hyperaccumulators" (Brooks et al, 1977). In their natural habitats, metal-rich soils in many parts of the world, this type of heavy metal accumulation serves as a defense against pathogens and herbivores Martens and Boyd, 1994;Boyd et al, 2002;Hanson et al, 2003;Jhee et al, 2005). They can now be used for the decontamination ("phytoremediation") of anthropogenically heavy metal-contaminated soils and in some cases also for the commercial extraction ("phytomining") of high-value metals (mainly Ni) from metal-rich soils (Baker et al, 1994;McGrath and Zhao, 2003;Chaney et al, 2005).…”

Nickel in the Environment and Its Role in the Metabolism of Plants and Cyanobacteria

“…Many studies have shown that metal hyperaccumulation serves as a defense mechanism against herbivores and pathogens [159][160][161][162][163]. Herbivores that were given the choice between Senecio coronatus plants grown on different nickel levels chose those plants which accumulated the lowest amount of metal [161].…”

“…The Ni hyperaccumulator Streptanthus polygaloides was more susceptible to turnip mosaic virus than the related nonaccumulator S. insignis, in particular when Ni-fertilized plants were compared [168]. A very recent study [163] testing the effect of nickel hyperaccumulation in Streptanthus polygaloides on different types of herbivores has shown that hyperaccumulation is an efficient protection against tissue-chewing herbivores, but much less effi cient against herbivores feeding on vascular tissue. This is logical in view of the preferentially epidermal sequestration of the metal in most hyperaccumulators (see Section 4.2).…”