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Keywords:

  • elemental defense;
  • heavy metal;
  • hyperaccumulator;
  • selenium

There are innumerable studies that report on how plants defend themselves against insect herbivores. Most focus on chemical traits (Harborne, 1993), morphological adaptations (Schoonhoven et al., 2005), compensatory strategies (Trumble et al., 1993), or genetic variations that allow escape in time or space (Denno & McClure, 1983). In 1992, a new strategy was proposed and named the elemental defense hypothesis (Boyd & Martens, 1992). This novel strategy suggested that some plants (termed hyperaccumulators) sequester exceptionally high concentrations of metals as a defense against herbivores. This hypothesis was extended by Coleman et al., in 2005, to include plants that accumulated more modest amounts of trace elements. While there have been an excellent series of studies conducted in the laboratory that generally support this hypothesis (Boyd, 2007 and references therein), and many plant species have been discovered that can accumulate these elements (Reeves & Baker, 2000), field-based studies investigating herbivore responses to metal sequestration have been lacking. The limited field research to date has primarily focused on systems with a single plant and insect (but see Boyd, 2007 for studies with nickel). The paper by Galeas et al., in this issue of New Phytologist (pp. 715–724), is the first to use a field survey approach to test the elemental defense hypothesis across a range of insect species feeding on plants containing elevated concentrations of selenium (Se).

‘... there are now many anthropogenic sources of Se contamination where new relationships may evolve.’

The importance of selenium in the environment

  1. Top of page
  2. The importance of selenium in the environment
  3. Selenium and ecosystem function
  4. Evolution of plant accumulation of metals and metalloids
  5. Testing for elemental defense against herbivores
  6. Looking forward
  7. References

Although the periodic table contains 87 elements that are considered to be metals or metalloids (elements that act like metals, but lack luster), fewer than 15 of these are commonly found at elevated concentrations in plants. These key elements, which include arsenic (As), aluminium (Al), lead (Pb), cobalt (Co), chromium (Cr), copper (Cu), cadmium (Cd), mercury (Hg), manganese (Mn), nickel (Ni), Se and zinc (Zn), have all been demonstrated to be toxic to arthropods (Heliovaara & Vaisanen, 1993 and references therein). Of these, Se is a particularly important problem. Although Se is an essential trace nutrient important to most animals as an antioxidant (Mayland, 1994), this widespread metalloid displays a narrow margin between concentrations that are beneficial and those that are toxic. No continent on earth is free of soils with significant concentrations of Se (McNeal & Balistrieri, 1989), but some specific regions do have Se-poor soils. The many Se-contaminated sites in North America have been reviewed by Mayland et al. (1989). In California, the San Joaquin Valley alone has over 213 000 ha of soil with elevated amounts of Se, resulting primarily from agricultural activities (http://tin.er.usgs.gov/geochem/doc/averages/se/usa.html). In fact, virtually all countries that burn coal as an energy source, or that mine metals such as copper, have significant point source contamination with Se (McNeal & Balistrieri, 1989). Thus, while the primary evolution of plants and insects with adaptations to elevated concentrations of Se has almost certainly occured at geologically stable sites with rainfall leaching selenate from naturally seleniferous soils, there are now many anthropogenic sources of Se contamination where new relationships may evolve.

Selenium and ecosystem function

  1. Top of page
  2. The importance of selenium in the environment
  3. Selenium and ecosystem function
  4. Evolution of plant accumulation of metals and metalloids
  5. Testing for elemental defense against herbivores
  6. Looking forward
  7. References

Terrestrial herbivores, particularly arthropods, are critical to the effective functioning of ecosystems. Because these organisms are active at the base of the food web, changes in population densities of arthropods can have profound effects on higher-level organisms that depend on them as primary food sources. Many arthropods are beneficial, serving to keep pest populations under control, thereby preventing damaging outbreaks. Other arthropods pollinate plants, disseminate seeds and produce structures used by countless other animals. Disruption of any of these activities can have substantial (and usually deleterious) effects on an ecosystem. Thus, arthropods are often used as bio-indicators when ecosystems become polluted. While many studies have examined insect diversity at sites with anthropogenic metal contamination, it is somewhat surprising that relatively little information is available from sites with seleniferous soils where elevated concentrations of Se occur naturally. Nonetheless, there is unambiguous information that Se has significant fitness effects on arthropods.

Terrestrial insect herbivores have to acquire their nutrients, minerals and trace elements from food, and toxic ions can readily cross an arthropod's midgut epithelium and enter the hemolymph. The early ecotoxicology literature suggested that intake of metals and metalloids by arthropods was dependent primarily on the concentrations in the food (Dallinger & Rainbow, 1993). A subsequent review by Jensen & Trumble (2003) cites numerous cases across several insect orders where a dose-dependent concentration effect has been documented for a variety of elements. However, the soil concentrations of Se are not always indicative of the concentrations of Se in plants because of the rapid transport and uptake (Mayland et al., 1989). Typically, sodium selenate is leached from rocks or soil by rainwater or agricultural irrigation water, and then transformed within plants to other forms of Se. Plants can acquire Se as either sodium selenate or sodium selenite, or in organic forms such as selenomethionine or selenocysteine, but the most common soluble form of Se in water is sodium selenate. When acquired as sodium selenate, plants generally convert it to sodium selenite. The Se in sodium selenite is then substituted for sulfur in certain amino acids, commonly producing selenomethionine, selenocysteine or selenocystine. Selenomethionine is the most common form of Se found in plants (Daniels, 1996). This form, which was found to be highly toxic to insects in laboratory feeding studies (Jensen et al., 2006), is not detected by some insects, allowing rapid ingestion of toxic doses (Trumble et al., 1998). The various forms of Se are known to be transferred between plants and herbivores, with a tendency for biomagnification (Vickerman & Trumble, 2003).

Comparatively few studies have examined the relative toxicological responses of higher trophic levels to metals accumulated in prey. Boyd & Wall (2001) fed four different predator species (two insects and two arachnid species) with prey containing high concentrations of nickel. They found that while three of the species were not affected, one of the spider genera had a significant decrease in survival. Vickerman & Trumble (2003) found that hemipteran predators exposed to Se in their prey (a caterpillar) had significantly higher mortality and weighed less than control predators fed prey with low Se concentrations. Detrimental effects were observed for predators despite the prey containing more Se than the predators. Thus, a trace element in the food chain can have detrimental effects, even in the absence of biomagnification. In a contrasting study, Merrington et al. (2001) tracked Cd and Zn from fertilizer applications through wheat plants to aphids, and then to their lacewing predators. They found that the aphids accumulated concentrations of Cd and Zn some 24 and 140 times greater, respectively, than the concentrations in the fertilized soil on which the wheat plants were grown. However, the predatory lacewings fed high-Cd/Zn prey did not accumulate Cd or Zn any differently from the controls. The authors speculated that this was because of the piercing and sucking method of feeding by the predator and the location of contaminants in the body of the prey. Therefore, higher trophic level predators or parasites may be differentially affected by trace elements based on variable feeding strategies or detoxification mechanisms. This variability provides an opportunity for the evolution of plants, herbivores and higher tropic level organisms in areas with elevated metal or metalloid contents in soil.

Evolution of plant accumulation of metals and metalloids

  1. Top of page
  2. The importance of selenium in the environment
  3. Selenium and ecosystem function
  4. Evolution of plant accumulation of metals and metalloids
  5. Testing for elemental defense against herbivores
  6. Looking forward
  7. References

As early as 1957, a possible evolutionary role for plants accumulating metalloids was suggested when Tadros (1957) reported that plants adapted to high Se environments were attacked more readily by pathogens if they were grown in soils containing low concentrations of Se. Subsequently, Boyd & Martens (1992) listed five hypotheses that have attempted to explain the evolution of plants that accumulate high concentrations of metals. These hypotheses predict that the ability to accumulate metals and metalloids evolved to provide (1) tolerance to, or disposal of, the elements from the plant, (2) a drought-resistance strategy, (3) a means of avoiding competition from plants less tolerant to the elements, (4) inadvertent uptake of elements and (5) defense against herbivores or pathogens. All of these hypotheses have been tested to varying degrees (Boyd, 2004), and there is some indication that each has merit. Of these, the best studied is the elemental defense hypothesis, for which considerable support has been found. However, not surprisingly, the available literature shows that this hypothesis is not universally applicable, as some herbivores, pathogens and parasitic plants can successfully attack hyperaccumulator species (Boyd, 2007). Interestingly, the literature treats all five proposed hypotheses as independent, and even mutually exclusive, evolutionary processes. We believe that these hypotheses are compatible and can act jointly to reinforce each other in driving the evolution of plant accumulation of elements.

The importance of the study of Galeas et al. is that their research provides a comprehensive field survey of a naturally seleniferous site, including a combination of herbivore and predator occurrence data, in conjunction with Se concentrations in the plants, insects and predators. These data permit a detailed analysis of associations that has not been previously possible. This is a necessary step in unraveling why some plants have evolved the ability to accummulate substantial amounts of Se, and how some insects appear to be compensating. In addition, the assessment they provide of the prevalence of insect adaptation or tolerance to Se across feeding guilds is particularly intriguing. The plant–insect associations presented in the paper by Galeas et al. may even find application in the developing fields of phytoremediation and phytomining (Reeves & Baker, 2000; Vickerman et al., 2004).

Testing for elemental defense against herbivores

  1. Top of page
  2. The importance of selenium in the environment
  3. Selenium and ecosystem function
  4. Evolution of plant accumulation of metals and metalloids
  5. Testing for elemental defense against herbivores
  6. Looking forward
  7. References

Using the reasoning employed by Berdegue et al. (1996) to examine the theory of enemy-free space, we suggest that three falsifiable null hypotheses can be constructed to test the theory of elemental defense for Se-containing plants. The first hypothesis is that the fitness of a plant without Se and without herbivores is equal to the fitness of a plant without Se and in the presence of herbivores. Disproving the first null hypothesis demonstrates that herbivores have fitness effects for this plant. While it can be argued that herbivores are known to harm plants, and therefore experimental testing is unnecessary, herbivory may not be limiting plant fitness in a particular system at a particular time (see Trumble et al., 1993).

The second hypothesis states that the fitness of a plant with Se and in the presence of herbivores is equal to the fitness of a plant without Se and in the presence of herbivores. Disproving the second null hypothesis demonstrates that the presence of Se has fitness consequences for herbivores. The second hypothesis has been tested in the laboratory and to a lesser extent in the field (Freeman et al., 2007; see also Galeas et al.), providing evidence that insect herbivory is in fact reduced by the presence of Se. The limitation of these studies is that they do not directly measure plant fitness, but rather focus on the amount of leaf eaten, or the survival or development of the insect herbivore.

The third hypothesis predicts that the fitness of a plant with Se but without herbivores is equal to the fitness of a plant without Se and without herbivores. This final hypothesis looks for a cost or a benefit of Se accumulation in the absence of herbivores. If Se is costly, there is support for the elemental defense hypothesis. However, if Se is beneficial in the absence of herbivores, then defense against herbivores is probably not the primary advantage of Se accumulation. Note that failing to disprove this last hypothesis does not disprove the elemental defense hypothesis, but merely suggests that alternative hypotheses explaining Se hyperaccumulation should also be considered.

Looking forward

  1. Top of page
  2. The importance of selenium in the environment
  3. Selenium and ecosystem function
  4. Evolution of plant accumulation of metals and metalloids
  5. Testing for elemental defense against herbivores
  6. Looking forward
  7. References

The opportunities for compelling research on these fascinating metal-accumulating systems are nearly endless, particularly as they relate to current physiological and ecological theories. Although some recent research has suggested physiological mechanisms by which Se may be detoxified in insects (see Jensen, 2006), substantially more information is needed before we can begin to understand fully the physiological ecology of the independent and joint effects of metals and metalloids. Minimal information is available on the effects of Se on fitness and population dynamics of parasitoids in either natural or agricultural systems. No studies have addressed the relative importance of top-down (natural enemies) vs bottom-up (plant nutrition) processes at contaminated sites. In addition, the possible role that Se may play in mediating competitive interactions among herbivores, or among natural enemies, is completely unknown. No reports are available on the effects of Se on pollination ecology or on the possible interactions of Se accumulation with the increasing temperatures predicted as a result of global warming. How these various ecological processes will be altered by the presence of metals, such as Se, should provide exciting research opportunities for the foreseeable future.

References

  1. Top of page
  2. The importance of selenium in the environment
  3. Selenium and ecosystem function
  4. Evolution of plant accumulation of metals and metalloids
  5. Testing for elemental defense against herbivores
  6. Looking forward
  7. References
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  • Boyd RS. 2004. Ecology of metal hyperaccumulation. New Phytologist 162: 563567.
  • Boyd RS. 2007. The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant and Soil 293: 153176.
  • Boyd RS, Martens SN. 1992. The raison d’etre of metal hyperaccumulation by plants. In: BakerAJM, ProctorJ, ReevesRD, eds. The vegetation of ultramafic (serpentine) soils. Andover, UK: Intercept, 279289.
  • Boyd RS, Wall MA. 2001. Responses of generalist predators fed high-Ni Melanotrichus boydi (Heteroptera: Miridae): elemental defense against the third trophic level. American Midland Naturalist 146: 186198.
  • Coleman CM, Boyd RS, Eubanks MD. 2005. Extending the elemental defense hypothesis: dietary metal concentrations below hyperaccumulator levels could harm herbivores. Journal of Chemical Ecology 31: 16691681.
  • Dallinger R, Rainbow P. 1993. Ecotoxicology of metals in invertebrates. Boca Raton, FL, USA: Lewis Publishers, CRC Press.
  • Daniels LA. 1996. Selenium metabolism and bioavailability. Biological Trace Element Research 51: 185199.
  • Denno RF, McClure MS. 1983. Variable plants and herbivores in natural and managed systems. New York, NY, US: Academic Press.
  • Freeman JL, Lindblom SD, Quinn CF, Fakra S, Marcus MA, Pilon-Smits EAH. 2007. Selenium accumulation protects plants from herbivory by orthoptera due to toxicity and deterrence. New Phytologist 175: 490500.
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  • 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 (Diptera: Phoridae). Archives of Environmental Contamination and Toxicology 50: 523530.
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  • McNeal JM, Balistrieri LS. 1989. Geochemistry and occurrence of selenium: an overview. In: JacobsLW, ed. Selenium in agriculture and the environment. Madison, WI, USA: Soil Science Society of America Special Publication 23: 114.
  • Merrington G, Miller D, McKaughlin MJ, Keller MA. 2001. Trophic barriers to fertilizer Cd bioaccumulation through the food chain: a case study using a plant–insect predator pathway Archives of Environmental Contamination and Toxicology 41: 151156.
  • Reeves RD, Baker AJM. 2000. Metal accumulating plants. In: RaskinI, EnsleyBD, eds. Phytoremediation of toxic metals: using plants to clean up the environment. New York, NY, USA: John Wiley and Sons, 193229.
  • Schoonhoven LM, Van Loon JJ, Dicke M. 2005. Insect-plant biology, 2nd edn. Oxford, UK: Oxford University Press.
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  • Trumble JT, Kolodny-Hirsch DM, Ting IP. 1993. Plant compensation for arthropod herbivory. Annual Review of Entomology 38: 93119.
  • Trumble JT, Kund GS, White KK. 1998. Influence of form and quantity of selenium on the development and survival of an insect herbivore. Environmental Pollution 101: 175198.
  • Vickerman DB, Trumble JT. 2003. Biotransfer of selenium: effects on an insect predator, Podisus maculiventris. Ecotoxicology 12: 497504.
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