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Keywords:

  • elevated CO2;
  • global climate change;
  • insect herbivory;
  • ozone;
  • plant chemical defenses;
  • plant-insect interactions;
  • plant secondary metabolites;
  • temperature;
  • tri-trophic interactions;
  • UV light

Abstract

  1. Top of page
  2. Abstract
  3. Elevated CO2 Effects
  4. Elevated O3 Effects
  5. Enhanced UV Light Effects
  6. Global Warming Effects
  7. Conclusions and Future Research Directions
  8. Acknowledgements
  9. References

This review focuses on individual effects of major global change factors, such as elevated CO2, O3, UV light and temperature, on plant secondary chemistry. These secondary metabolites are well-known for their role in plant defense against insect herbivory. Global change effects on secondary chemicals appear to be plant species-specific and dependent on the chemical type. Even though plant chemical responses induced by these factors are highly variable, there seems to be some specificity in the response to different environmental stressors. For example, even though the production of phenolic compounds is enhanced by both elevated CO2 and UV light levels, the latter appears to primarily increase the concentrations of flavonoids. Likewise, specific phenolic metabolites seem to be induced by O3 but not by other factors, and an increase in volatile organic compounds has been particularly detected under elevated temperature. More information is needed regarding how global change factors influence inducibility of plant chemical defenses as well as how their indirect and direct effects impact insect performance and behavior, herbivory rates and pathogen attack. This knowledge is crucial to better understand how plants and their associated natural enemies will be affected in future changing environments.

Climate change has been defined as “any change in climate over time, whether due to natural variability or as a result of human activity” (Intergovernmental Panel on Climate Change, IPCC 2007). However, this term is usually used in the context of global changes resulting from anthropogenic actions. Regardless of subtle differences in the usage of this term, there is a general consensus that current changes in climatic factors are primarily due to human-driven practices such as burning of fossil fuels and deforestation. These activities release significant amounts carbon into the atmosphere, which have caused a dramatic increase in carbon dioxide (CO2) concentrations during the past 60 years. The IPCC has repeatedly reported that augmented emissions of greenhouse gases into the atmosphere (mainly elevated CO2 followed by methane and ozone) are the major cause of climatic changes observed today. These changes include global warming, precipitation fluctuations, rising sea levels and other “extreme climatic events”. Despite the amount of information that exists on global climate change, little is known regarding how these changes may affect natural ecosystems, particularly interactions among living organisms.

Interactions of plants and insects are of major importance in most natural ecosystems since these two groups of organisms are extremely diverse and comprise almost 50% of all identified species on earth (Price 1997). The phytochemical coevolution theory suggests that secondary metabolites are likely the most important mediators of plant-insect interactions (Ehrlich and Raven 1964; Berenbaum 1983, 1995; Cornell and Hawkins 2003). According to this theory, both plants and insect herbivores generate selective forces that lead to the evolution of plant defense (i.e., plant secondary metabolites) and herbivore offense (i.e., detoxification ability) in a so-called coevolutionary arms race. These chemicals, although not required for primary plant metabolic processes such as respiration or growth, have been extensively recognized for their role in plant defense against herbivore and pathogen attack (Kliebenstein 2004). Therefore, the evaluation of global change effects on plant secondary metabolites is essential to predict future reciprocal evolutionary changes between plants and insect herbivores.

Plant defense responses to herbivory are dependent on the plants' evolutionary history (e.g., past exposure to herbivory) as well as the physical environment affecting plant-insect associations (Tollrian and Harvell 1999). Human-induced changes in abiotic environmental factors such as atmospheric CO2 and ozone (O3) levels, ultraviolet (UV) light, changes in precipitation patterns or temperature may directly affect the concentration of secondary chemicals in plants, which in turn may influence rates of herbivory or pathogen attack. In addition, little emphasis has been placed on how the environment affects the inducibility of plant chemical defenses. To our knowledge, Bidart-Bouzat et al. (2005) were the first to report that herbivore induction of plant secondary chemicals (glucosinolates) can be affected by changes in climatic factors like atmospheric CO2 concentrations. This result has been corroborated in a subsequent study by Himanen et al. (2008) showing that inducibility of secondary metabolites can be altered not only by elevated CO2 but also by changes in O3 levels. These studies are important because variation in plant chemical induction can have significant ecological and evolutionary implications for plants and their interactions with insect herbivores.

In this review paper, we will focus on the individual effect of four major abiotic factors affecting global climate change, their impact on plant secondary chemistry, and how these effects may influence plant-insect interactions. These factors include elevated CO2 and O3, which are greenhouse gases significantly contributing to global climate change, as well as UV light and temperature, which in turn are directly affected by these greenhouse gases. While global warming has been mainly attributed to increases in greenhouse gases such as CO2, augmented UV light has been linked to ozone depletion caused by chlorofluorocarbons, hydrofluorocarbons and other harmful chemicals released by the industry, which break down stratospheric O3 molecules (IPCC 2007). Our goal is to identify future directions for research on global change and plant chemical defenses, including ecological implications mostly for insect herbivores but also for tritrophic interactions (plants/herbivores/predators) and plant disease in both natural and agricultural systems.

Elevated CO2 Effects

  1. Top of page
  2. Abstract
  3. Elevated CO2 Effects
  4. Elevated O3 Effects
  5. Enhanced UV Light Effects
  6. Global Warming Effects
  7. Conclusions and Future Research Directions
  8. Acknowledgements
  9. References

As previously mentioned, levels of atmospheric CO2 have been constantly increasing since the industrial revolution due to anthropogenic activities, including burning of fossil fuels and deforestation. There is a general prediction that elevated CO2 levels enhance plant photosynthetic rates and growth (Bazzaz et al. 1990; Bazzaz and Miao 1993; Ceulemans and Mousseau 1994; Curtis 1996). However, it has been shown that potential benefits of CO2 enrichment on plant growth or reproduction may be offset by other environmental factors interacting with elevated CO2 (Bidart-Bouzat et al. 2005). For example, the inclusion of insect herbivory in a growth chamber experiment altered the lifetime fitness response of Arabidopsis thaliana to elevated CO2 (Bidart-Bouzat et al. 2005); in other words, herbivory was found to either suppressed or decreased plant fitness enhancements induced by elevated CO2per se. Other studies have also demonstrated that plant responses to elevated CO2 can be influenced by plant-plant competition, temperature, light, water stress, and nutrients (Bazzaz and Miao 1993; Bazzaz et al. 1995; Zhang and Lechowicz 1995; Kellomaki and Vaisanen 1997; Curtis and Wang 1998; Andalo et al. 2001; Kubiske et al. 2002; Wullschleger et al. 2002).

Prior research has revealed that elevated CO2 may affect a variety of plant traits including plant secondary chemistry. Table 1 summarizes studies showing the effect of elevated CO2 on secondary metabolites, which are known to influence plant-insect interactions (see references therein). CO2-induced changes in plant secondary chemicals have been frequently explained on the basis of the carbon-nutrient balance hypothesis (CNBH) (Karowe et al. 1997; Gebauer et al. 1998). Under high CO2 conditions, this hypothesis predicts an increase in carbon allocation to secondary metabolism due to augmented production of carbohydrates (Bryant et al. 1983, 1987). Even though the concentration of plant secondary compounds can be directly influenced by resource availability, several studies have shown that these responses to elevated CO2 are also dependent on the specific chemical type and plant species (or genotypes) under consideration (Table 1). Table 1 provides several examples of elevated CO2 inducing either an increase, decrease or no change in the concentrations of secondary chemicals commonly found in plants (e.g., glucosinolates, phenolics, tannins, and terpenoids). Given the ambiguity of plant chemical responses to increased CO2, care should be taken not to consider them as a simple cause-effect relationship between environmental characteristics (e.g., availability of resources) and production of secondary metabolites. As a matter of fact, it should not be overlooked that interactions of plants with herbivores are a major factor determining variability in plant chemical defenses (Ehrlich and Raven 1964; Berenbaum 1983).

Table 1.  Effects of elevated CO2, O3, UV light and temperature on constitutive levels of plant secondary chemicals
Plant species or communitySecondary chemicalsEnvironmentally-induced changes in levels of secondary chemicalsaReferences
  1. a(+) increase, (−) decrease or (0) no change in levels of plant secondary chemicals; b marginally significant response.

Elevated CO2
Arabidopsis thalianaGlucosinolates+/− or 0Bidart-Bouzat et al. 2005
Artemisia tridentataCoumarins0Johnson and Lincoln 1990
Flavonoids0Johnson and Lincoln 1990
Monoterpenes0Johnson and Lincoln 1990
Sesquiterpenes0Johnson and Lincoln 1990
Betula pendulaCondensed tannins+Kuokkanen et al. 2001
Flavonol glycosides+Kuokkanen et al. 2001, Lavola and Julkunen-Tiito 1994
Terpenoids+Kuokkanen et al. 2001
Brassica junceaGlucosinolatesKarowe et al. 1997
Brassica rapaGlucosinolates0Karowe et al. 1997
Raphanus sativusGlucosinolates0Karowe et al. 1997
Brassica napusIndolyl glucosinolatesHimanen et al. 2008
Brassica oleraceaGlucosinolates+/− or 0Reddy et al. 2004, Schonhof et al. 2007
Monoterpenesb or 0Vuorinen et al. 2004a
Phenolics− or 0Reddy et al. 2004
Bromus erectusPhenolics (Gallic acid)+ or 0Castells et al. 2002
Dactylis glomerataPhenolics (Gallic acid)+Castells et al. 2002
Forest community (12 tree species)Phenolics+ or 0Knepp et al. 2005
Glycine maxPhytoalexins+ or 0Braga et al. 2006
Gossypium hirsutumCondensed tannins+ or 0Coviella et al. 2002
Terpenoid aldehydes0Coviella et al. 2002, Agrell et al. 2004
Lotus corniculatusCondensed tannins+bGoverde et al. 2004
Polyphenols+bGoverde et al. 2004
Medicago sativaFlavonoids+/− or 0Agrell et al. 2004
Triterpenes (Saponins)+/− or 0Agrell et al. 2004
Nicotiana tabaccumPhenolics+Matros et al. 2006
Lignins+Matros et al. 2006
Pinus sylvestrisCondensed tannins0Heyworth et al. 1998
Monoterpenes+Heyworth et al. 1998
Pinus taedaPhenolics+Gebauer et al. 1998
Plantago maritimaPolyphenols (p-Coumaric acid)+ or 0Davey et al. 2004
Phenolics (Caffeic acid)+ or 0Davey et al. 2004
Phenolics (Ferulic acid)0Davey et al. 2004
Monoterpenes0Davey et al. 2004
Populus tremuloidesCondensed tannins+ or 0Roth et al. 1998, McDonald et al. 1999, Agrell et al. 2000, Holton et al. 2003
Phenolic glycosides+ or 0McDonald et al. 1999, Agrell et al. 2000, Holton et al. 2003, Lindroth et al. 1993
Quercus myrtifoliaTannins+bRossi et al. 2004
Tropical tree community (nine tree species)Phenolics+ or 0Coley et al. 2002
Vaccinium myrtillusLignins0Asshoff and Hattenschwiller 2005
Vaccinium uliginosumLignins0Asshoff and Hattenschwiller 2005
Elevated O3
Acer saccharumFlavonoids+Sager et al. 2005
Brassica napusAromatic glucosinolates+Himanen et al. 2008
Indolyl glucosinolatesHimanen et al. 2008
Brassica oleraceaTerpenesPinto et al. 2007a,b
Glycine maxIsoflavonoids+Keen and Taylor 1975
Phytoalexins+Keen and Taylor 1975
Gossypiuum hirsutumFlavonoids+bBooker 2000
Lycopersicon esculentumJasmonic acid+ or 0Zandra et al. 2006
Petroselinium crispumFlavone glycosides+Hahlbrock and Scheel 1989
Furanocoumarins+Hahlbrock and Scheel 1989
Phytoalexins+Hahlbrock and Scheel 1989
Phaseolus lunatusTerpenes+Vuorinen et al. 2004b
Phaseolus vulgarisPhenolics (Hydroxycinamic acid)Kanoun et al. 2001
Isoflavonoids+ or 0Kanoun et al. 2001
Picea abiesLignins+Sandermann Jr. 1996
Monoterpenes0Sandermann Jr. 1996
Pinus ponderosaPhytoalexins+Sandermann Jr. 1996
Pinus strobesPhenolics− or 0Shadkami et al. 2007
Diterpenoids0Shadkami et al. 2007
Pinus sylvestrisPhenolics0Kainulainen et al. 1998
Monoterpenes0Kainulainen et al. 1998
Polyphenols (Catechin)Bonello et al. 1993
Phenolics (Stilbenes)+Bonello et al. 1993
Populus tremuloidesCondensed tannins0Lindroth et al. 2001
Phenolic glycosidesKopper and Lindroth 2003
Elevated UV light
Ascophyllum nodosumPhenolics (Phlorotannins)+Pavia et al. 1997
Betula pendulaFlavonoids+Lavola 1998, Lavola et al. 2000
Phenolic acids+Lavola 1998, Lavola et al. 2000
Cannabis sativaCanabinoid alkaloids+Lydon et al. 1987
Catharanthus roseusTerpenoid indole alkaloids+Ouwerkerk et al. 1999
Cistus creticusFlavonoids+Stephanou and Manetas 1997
Festuca rubraAlkaloids0McLeod et al. 2001
Festuca arundinaceaAlkaloids0McLeod et al. 2001
Festuca pratensisAlkaloids0McLeod et al. 2001
Glycine maxTerpenoidsSingh 1996
Phenolics+Mazza et al. 2000, Mirecki and Teramura 1984, Zavala et al. 2001
LigninsZavala et al. 2001
Lolium perenneAlkaloids0McLeod et al. 2001
Nicotiana attenuataPhenolics+Izaguirre et al. 2007
Nicotiana longifloraPhenolics+Izaguirre et al. 2007
Nothofagus pumiloPhenolics (Gallic acid)Rousseaux et al. 2004
Flavonoid aglycones+Rousseaux et al. 2004
Nothofagus antarcticaPhenolics (Gallic acid)Rousseaux et al. 2004
Flavonoid aglycones+Rousseaux et al. 2004
Hydrolysable tanninsRousseaux et al. 2004
Oriza sativaTerpenoidsAmbasht and Agrawal 1997
Quercus ilexTerpenoids+Filella and Penuelas 1999
Quercus roburLigninsNewsham et al. 1999
Pastinaca sativaCoumarins+Zangerl and Berenbaum 1987
Populus tremuloidesPhenolic glycosides+McDonald et al. 1999
Salix myrsinifoliaTannins0Veteli et al. 2006
Flavonoids0Veteli et al. 2006
Salicylates0Veteli et al. 2006
Salix phylicifoliaTannins0Veteli et al. 2006
Flavonoids0Veteli et al. 2006
Salicylates0Veteli et al. 2006
Trifolium repensFlavonol glycosides+Hofmann et al. 2003
Elevated temperature
Acer rubrumPhenolics0Williams et al. 2003
Brassica oleraceaGlucosinolates+/−Velasco et al. 2007, Matusheski et al. 2004, Pereira at al. 2002
Indoly glucosinolatePereira at al. 2002
Betula pendulaTotal phenolicsKuokkanen et al. 2001
Flavonol glycosidesKuokkanen et al. 2001
Phenolics (Cinnamoylquinic acid)Kuokkanen et al. 2001
Polyphenols (Catechin)Kuokkanen et al. 2001
Flavone aglycones+Kuokkanen et al. 2001
Cassiope tetragonaCondensed tannins+ or 0Hansen et al. 2006
Phenolics− or 0Hansen et al. 2006
Phragmites australisVolatile organic compounds+Loreto et al. 2006
Picea abiesTerpenes+Sallas et al. 2003
Phenolics0Sallas et al. 2003
Pinus ponderosaMonoterpenes+Constable et al. 1999
Pinus sylvestrisTerpenes+Sallas et al. 2003
Phenolics0Sallas et al. 2003
Pseudotsuga menziesiiMonoterpenes+/−Constable et al. 1999, Snow et al. 2003
Sesbania herbaceaCondensed tannins0Hansen et al. 2006
Phenolics− or 0Hansen et al. 2006
Salix myrsinifoliaPhenolicsVeteli et al. 2006
Quercus roburCondensed tanninsDury et al. 1998
Vaccinum vitis-idaeaCondensed tannins+ or 0Hansen et al. 2006

There is also evidence that elevated CO2 may influence inducibility of plant chemical defenses. In a growth chamber study, Bidart-Bouzat et al. (2005) found that herbivory by the diamondback moth (Plutella xylostella) induced a significant increase in the levels of total as well as some individual glucosinolates in Arabidopsis thaliana although only under elevated CO2 conditions (Figure 1). In addition, they found that elevated CO2 modified plant-insect relationships, that is, the type and degree of association between insect performance (i.e., adult insect weight) and glucosinolate levels. Himanen et al. (2008) has subsequently reported that herbivore-induced glucosinolates responses in Brassica napus were affected by environmental variation (i.e., elevated CO2 and O3). Other studies, however, have either failed to find significant CO2× herbivory interaction effects on plant secondary chemicals (Lindroth and Kinney 1998; Roth et al. 1998; Bazin et al. 2002) or detected only a marginally significant result (Agrell et al. 2004). More studies assessing how elevated CO2 may alter herbivore-induced plant secondary metabolites are definitely needed since these results can have direct implications for the evolution of inducible defenses and thus, coevolutionary relationships of plants and insects in future enriched CO2 environments.

image

Figure 1. Elevated CO2 effects on insect herbivore induction of total glucosinolates in Arabidopsis thaliana. *P < 0.05, **P < 0.001. Control (bsl00077); herbivory (▪).

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Rising atmospheric CO2 levels are also expected to influence insect herbivore performance (Lindroth 1996; Bezemer and Jones 1998; Whittaker 1999) through changes in plant quality, such as variation in the levels of nutritional components and/or secondary metabolites. Decreased insect performance has been commonly reported and associated with elevated CO2-induced decreases in plant nitrogen concentrations or increased C/N ratios (“nitrogen dilution” effect) (Fajer 1989; Traw et al. 1996; Hattenschwiler and Schafellner 1999; Goverde et al. 2004; Reddy et al. 2004; Asshoff and Hattenschwiler 2005), particularly in C3 plants (Barbehenn et al. 2004). Although higher leaf consumption has been observed (apparently to compensate for the decrease in plant nitrogen levels), several studies have revealed that herbivore densities and damage were lower under elevated CO2 conditions (Stiling et al. 1999, 2003; Rossi et al. 2004; Knepp et al. 2005). In addition, when given a choice, lepidopteran larvae have been reported to prefer feeding on leaf tissue grown under ambient CO2 conditions (Goverde and Erhardt 2003; Agrell et al. 2005, 2006; Knepp et al. 2007; but see Johnson and Lincoln 1990; Traw et al. 1996; and Diaz et al. 1998 documenting an opposite trend).

Elevated CO2-induced changes in plant defenses and their potential effects on insect performance have been frequently predicted (Lincoln et al. 1993; Penuelas and Estiarte 1998; Zvereva and Kozlov 2006; Valkama et al. 2007); however, they have been rarely quantified (but see McDonald et al. 1999; Holton et al. 2003; Bidart-Bouzat et al. 2005). McDonald et al. (1999) found that enhanced levels of plant phenolic glycosides under elevated CO2 conditions negatively affected relative consumption rates and efficiency for conversion of ingested food of the gypsy moth Lymantria dispar. Conversely, elevated CO2-induced increases in glucosinolate levels (i.e., indolyl, propenyl and total glucosinolates) in Arabidopsis thaliana were positively correlated with diamondback moth adult weights (Bidart-Bouzat et al. 2005). This last result could have been due to phagostimulatory properties of glucosinolates in specialist insects such as the diamondback moth, which are adapted to feed on these chemicals. It is worth noting this previous study also reported that insect-glucosinolate associations were dependent on the specific glucosinolate and insect gender. This finding highlights the importance of assessing the entire chemical profile rather than only total concentrations (as commonly reported) to better understand interactions between insect performance and plant secondary metabolism in future changing environments.

Elevated CO2-induced changes in plant secondary chemistry are also likely to influence tritrophic interactions and plant disease, although little is known about these research topics. Secondary metabolites can act as plant indirect defenses by attracting natural enemies (e.g., predators and parasitoids) of insect herbivores (van Poecke and Dicke 2004). For example, van Poecke et al. (2001) found that Cotesia rubecula, a common parasitic wasp of the white cabbage butterfly Pieris rapae was attracted to Arabidopsis thaliana's volatiles emitted by P. rapae-infested plants. It has been shown that elevated CO2 can either increase, decrease, or induce no change in the concentration of monoterpenes, which are known to attract predators or parasitoids of insect herbivores (Penuelas and Llusia 1997; Constable et al. 1999; Loreto et al. 2001; Staudt et al. 2001; Vuorinen et al. 2004a,b). There is also some evidence that CO2 enrichment can affect the searching efficiency of insect parasitoids probably as a result of changes in the plant chemical cues used by parasitoids to locate their insect herbivore hosts (Gates et al. 1995; Vuorinen et al. 2004b). For example, Vuorinen et al. (2004b) detected CO2 effects on parasitoid preference for herbivore-damaged plants growing under ambient compared with elevated CO2 conditions. A possible explanation for this result was that the emission of certain volatiles (e.g., 3-hexenyl acetate) declined when plants were grown in enriched CO2 environments. CO2-mediated changes in secondary chemicals may also influence insect parasitoid fitness, although the only study we found on this topic failed to find a significant effect of elevated CO2 on parasitoid performance (Holton et al. 2003). On the other hand, parasitoid abundance and incidence of attack appear to be influenced by CO2 levels. Parasitism rates were found to be higher in insect herbivores feeding on a native scrub-oak community when exposed to elevated CO2 (Stiling et al. 1999); however, information is lacking as to whether this outcome could be attributed to potential CO2-induced changes in plant volatile emissions or simply to differences in insect herbivore abundance between CO2 treatments.

As previously mentioned, little information exists on elevated CO2-mediated changes in plant quality and how these in turn impact plant disease. Pathogenic fungi can be either nitrogen- or carbon-limited; consequently, changes in C/N ratios and plant growth induced by elevated CO2 may affect pathogens' growth as well as disease spread in the hosts (Strengbom and Reich 2006). Likewise, elevated CO2-induced changes in plant carbon or nitrogen may, at least, partly influence the production of plant secondary chemicals (Braga et al. 2006), which in turn may affect pathogen performance (although evidence for the latter is lacking). Furthermore, elevated CO2 appears to affect inducibility of secondary chemicals by pathogens. For example, induction levels of the phytoalexin glyceollins by the fungus Phythophthora sojae in a soybean cultivar have increased under elevated CO2 conditions, although these results were cultivar- and phytoalexin-specific (Braga et al. 2006). Future research should focus more on evaluating indirect as well as potential direct effects of elevated CO2 on plant disease, since this information is essential for both natural and agricultural systems.

Elevated O3 Effects

  1. Top of page
  2. Abstract
  3. Elevated CO2 Effects
  4. Elevated O3 Effects
  5. Enhanced UV Light Effects
  6. Global Warming Effects
  7. Conclusions and Future Research Directions
  8. Acknowledgements
  9. References

Ozone is a naturally occurring atmospheric gas. Most of this gas is present in the stratosphere (about 90% of the total) forming a layer that protects living organisms from high energy UV radiation (http://www.ozonelayer.noaa.gov). Ozone is also a natural constituent of the troposphere, although in much lower concentrations. However, O3 levels in the lower atmosphere have considerably increased as a result of human activities, and this “greenhouse gas” is now significantly contributing to global climate change (IPCC 2007). Tropospheric O3 pollution mainly results from the combustion of fossil fuels, which produce nitrogen oxide gases and volatile organic compounds that react with oxygen and generate O3. Unlike CO2, which overall enhances plant growth, O3 causes oxidative stress in plant cells resulting in decreased plant photosynthesis, respiration, and plant growth as well as inducing changes in nutrient allocation and senescence (Sager et al. 2005). Although much less is known regarding elevated O3 compared with CO2 enrichment effects on plants and higher trophic levels, several studies have shown that changes in O3 concentrations can alter the production of secondary chemicals in plants (Sandermann Jr. 1996 and references therein; Kopper and Lindroth 2003; Vuorinen et al. 2004a). Plant physiological stress imposed by augmented O3 levels may stimulate the induction of metabolic pathways (e.g., salicylic acid and jasmonic acid pathways) involved in the production of secondary compounds (Holopainen 2002). Since these metabolic pathways are also activated by insect herbivores feeding on plants (Traw and Bergelson 2003), herbivore-induction of secondary metabolites is likely to be enhanced by O3 levels.

Previous studies suggest that plant species differ in their susceptibility to elevated O3 levels (reviewed in Valkama et al. 2007), and show variable responses in terms of the type and amount of metabolite induced by this global change factor (Table 1). While angiosperms appear to be more affected by elevated O3 than gymnosperms, the latter have shown a diverse array of defense responses to this type of stress (Sandermann Jr. 1996; Valkama et al. 2007). For example, elevated O3 has been shown to induce the lignin biosynthetic pathway in Picea abies, increase the production of phytoalexins in Pinus ponderosa as well as that of the polyphenolic antioxidant catechin in Pinus sylvestris and Picea abies. In addition, ethylene production has been enhanced by this environmental factor in several other conifer species (Sandermann Jr. 1996). Other studies have shown that elevated O3 can decrease levels of plant secondary chemicals (Kanoun et al. 2001; Holton et al. 2003; Kopper and Lindroth 2003; Pinto et al. 2007a,b; Himanen et al. 2008) or have no effect on these metabolites (Booker 2000; Kopper et al. 2001; Lindroth et al. 2001), even after several years of continuous high O3 exposure (Kainulainen et al. 1998). The phytochemical variation observed in these previous studies may reflect differences in the plant metabolic response to “acute stress” versus “chronic stress” (Kanoun et al. 2001). Kanoun et al. (2001) have detected a temporal variation in the content and composition of phenolic compounds in bean leaves (Phaseolus vulgaris) exposed to moderately enhanced O3 levels. For example, an initial decrease in a phenolic derivative (i.e., hydroxycinnamic acid) followed by de novo synthesis of other phenolic compounds (isoflavonoids) was specifically induced by O3 enrichment. In another study, three quercetin glycosides (i.e., quercitrin, isoquercitrin and avicularin) were specifically induced by increased O3 levels, while levels of other phenolic compounds remained unchanged. These “ozone-induced phenolics” have been recognized as potential bioindicators of O3 pollution in natural ecosystems (Kanoun et al. 2001; Sager et al. 2005).

Elevated O3-induced changes in plant secondary chemicals may affect not only insect herbivores but also their associated predators or parasitoids (Kopper and Lindroth 2003). Performance of the forest tent larva (Malacosoma distria) increased under O3 enrichment probably as a result of decreased concentrations of plant phenolic glycosides and augmented nitrogen (early in the season) under enhanced O3 levels (Holton et al. 2003; Kopper and Lindroth 2003). Conversely, parasitoid survivorship decreased under elevated O3 (Holton et al. 2003), although it is not known whether this outcome could be attributed to O3-induced changes in the parasitoid's food quality (i.e., lepidopteran larvae feeding on elevated O3-grown plants). Enhanced O3 levels may also affect the “orientation behavior” of parasitoid wasps, since this toxic gas may degrade certain plant volatiles (e.g., terpenes) used by wasps as chemical cues for finding their hosts in the field. Pinto et al. (2007a,b) reported that O3-induced degradation of certain terpenes did not affect the overall orientation behavior of wasps probably because not all of the compounds used by wasps as host finding cues were affected by ozone. Thus, wasps could have alternatively used chemicals that were unaffected by elevated O3. However, given the choice, wasps apparently preferred herbivore-induced plants growing under ambient O3 concentrations. In addition, we found two studies showing evidence that elevated O3 could influence herbivore induction of secondary metabolites including glucosinolates and terpenes (Vuorinen et al. 2004a,b; Himanen et al. 2008). These results may have important implications for plant-insect herbivore interactions as well as for interactions with the third trophic level (predators and parasitoids), which may also be indirectly affected by elevated O3-induced changes in plant quality.

Regarding elevated O3 effects on plant disease, little information exists on whether these are mediated by changes in secondary chemicals. Ozone appears to induce the salicylic acid pathway, which is involved in plant responses to stress as well as in resistance to pathogen attack (Ogawa et al. 2005). Exposure to O3 has also led to pathogen-mediated increased induction of secondary metabolites such as the phenolic compounds stilbenes in the roots of Pinus sylvestris; however, other chemicals were negatively or not affected by this environmental factor (Bonello et al. 1993). Even though these previous studies suggest that O3 exposure may induce defense-related responses in plants against pathogens, the significance of these responses for pathogen resistance is still ambiguous. As a matter of fact, despite the apparent positive effect of O3 on the pathogen-mediated chemical induction in P. sylvestris, O3-exposed tree seedlings were more susceptible to disease than untreated ones (Bonello et al. 1993). Conversely, pre-exposure to O3 increased salicylic acid levels in Nicotiana tabacum, which in turn increased resistance to the tobacco mosaic virus (Yalpani et al. 1994). More information is definitely needed to elucidate the potential link between plant secondary metabolism and disease resistance under elevated O3, especially since increased predisposition to disease has been observed in O3-polluted forests of USA and Europe (Sandermann Jr. 1996; Paoletti et al. 2007).

Enhanced UV Light Effects

  1. Top of page
  2. Abstract
  3. Elevated CO2 Effects
  4. Elevated O3 Effects
  5. Enhanced UV Light Effects
  6. Global Warming Effects
  7. Conclusions and Future Research Directions
  8. Acknowledgements
  9. References

During the past 30–40 years, there has been an increased concern regarding potential effects of stratospheric O3 depletion and thus, enhanced UV radiation on terrestrial ecosystems (Stratmann 2003). Although tropospheric O3 has increased as a result of air pollution, stratospheric O3 has been considerably reduced due to the emission of chlorofluorocarbons (and related chemicals) into the atmosphere. These chemicals break down stratospheric O3 and thus, deplete the O3 layer, of which the main role is the absorption of high energy UV radiation (Wilson et al. 2007).

Even though UV light is necessary for numerous chemical reactions and biological processes, high levels of this type of solar radiation may be harmful for living organisms, particularly for plants (Roberts and Paul 2006). Ultraviolet radiation can cause molecular and cellular damage; for example, it can damage proteins, DNA and other biopolymers (Stratmann 2003). Furthermore, this type of radiation can affect plant growth and development and result in changes in vegetative or reproductive biomass, height, leaf characteristics, and flowering time (Bornman and Teramura 1993). However, several studies have failed to find significant effects of UV radiation on plant growth-related traits or photosynthetic processes (Searles et al. 2001; Tegelberg et al. 2004). Ultraviolet radiation can also alter the production of secondary chemicals with photoprotective qualities, which include many phenolic compounds such as flavonoids, coumarins and stilbenes. Although these secondary metabolites are induced by enhanced UV radiation, likely as a plant response to this stress, high constitutive levels of these chemicals may represent an adaptation to UV light damage in plants naturally exposed to higher UV levels (Dixon et al. 2001).

UV light effects on plant secondary metabolism have usually been associated with changes in phenolic compounds synthesized via the shikimic acid or phenylpropanoid pathway (Bassman 2004). Although there are some exceptions, most studies have detected an increase in phenolic compounds under higher levels of UV light, particularly UV-B solar radiation (McCloud and Berenbaum 1994; Lavola 1998; McDonald et al. 1999; Lavola et al. 2000; Mazza et al. 2000; Hofmann et al. 2003; Rousseaux et al. 2004; Tegelberg et al. 2004). This increase has been predominantly documented for phenolic compounds such as flavonoids including anthocyanins, isoflavonoids, flavonol glycosides and flavoproteins, phenolic acids and coumarins (Zangerl and Berenbaum 1987; Bornman and Teramura 1993; Lavola 1998; Lavola et al. 2000; Hofmann et al. 2003; Tegelberg et al. 2004). On the other hand, information on other important chemical classes such as terpenoids and alkaloids is less extensive or consistent. While some studies have detected a UV-induced increase in terpenoids (Filella and Penuelas 1999; Zavala and Ravetta 2002), others have found a decrease (Singh 1996; Ambasht and Agrawal 1997) or no change (Bassman 2004) in the levels of these chemicals. UV light effects on alkaloids are the least well-known. A few studies on this topic have showed an increase in terpenoid indole alkaloids and cyanogenic glucosides as well as an increase or decrease in the levels of cannabinoid alkaloids (reviewed in Bassman 2004). Information on UV light-induced changes in secondary metabolites has been summarized in Table 1.

The induction of UV-absorbing plant chemicals apparently overlaps with plant responses to other stresses, such as herbivore or pathogen attack. This overlapping in induction may act either synergistically or antagonistically on the levels of phytochemical production. For example, levels of proteinase inhibitors significantly accumulated in the tomato plant Lycopersicon esculentum when plants were exposed to both UV-B radiation and mechanical damage, but not when exposed to each of these factors separately (Stratmann et al. 2000). As a matter of fact, Izaguirre et al. (2003) found that about 20% of the genes associated with the response of Nicotiana attenuata plants to insect herbivory were also induced by UV-B radiation. On the other hand, there is evidence that induction of the flavonoid biosynthetic pathway by UV light can be inhibited by pathogen-induced defense responses in parsley (Logemann and Hahlbrock 2002). Other studies have also demonstrated that genes regulating the phenylpropanoid pathway leading to the synthesis of phenolic compounds (e.g., flavonoids) are regulated by both UV light levels and herbivory (reviewed in Stratmann 2003). Overall, despite the observed convergence in the responses of plants to UV radiation and herbivory, these previous studies still reflect some specificity in the responses triggered by these different environmental stresses (Stratmann 2003).

The effect of UV radiation (particularly UV-B radiation) on plant-insect interactions has been well studied and summarized in numerous reviews (Bornman and Teramura 1993; Searles et al. 2001; Caldwell et al. 2003; Bassman 2004; Raviv and Antignus 2004; Kunz et al. 2006; Roberts and Paul 2006; Caldwell et al. 2007). Therefore, here, we will focus on the major trends that have been reported as well as topics that need further investigation. As previously noted, UV light is not only essential for plant growth but also for some biochemical processes associated with plant defense responses to insect herbivory (Roberts and Paul 2006). In general, previous studies have shown UV-B mediated effects on plant secondary chemicals, which in turn influenced plant-insect interactions (e.g., decreased herbivory under higher UV-B light levels) (Ballare et al. 1996; Rousseaux et al. 1998; Mazza et al. 1999; Izaguirre et al. 2003; Rousseaux et al. 2004; Caputo et al. 2006; Izaguirre et al. 2007). Decreases in insect herbivory under enhanced UV-B conditions have been related to changes in plant secondary chemistry (Zavala et al. 2001; Izaguirre et al. 2003, 2007) or nutritional quality (Roberts and Paul 2006) as well as resulting from direct UV-B effects on insect herbivore behavior (Mazza et al. 1999; Caputo et al. 2006). These effects of higher UV-B levels have led to decreased insect oviposition rates (Caputo et al. 2006), insect abundance (Mazza et al. 1999), insect consumption (Rousseaux et al. 2004), insect performance (McDonald et al 1999; Lindroth et al. 2000), as well as lowered plant damage (Ballare et al. 1996; Mazza et al. 1999; Rousseaux et al. 2004; Izaguirre et al. 2007). For example, UV-B-induced reductions in herbivore attack have been associated with increases in phenolics in soybean (Zavala et al. 2001) and flavonoid aglycone levels in the southern beech tree Nothofagus Antarctica (Rousseaux et al. 2004). Yet, decreased damage in the perennial herb Gunnera magellanica was detected under higher UV-B light levels despite the lack of response of soluble phenolics to changes in this environmental agent (i.e., solar versus reduced UV-B radiation) (Rousseaux et al. 1998). Likewise, Veteli et al. (2003) found no effect of enhanced UV-B light on flavonoids, tannins and salicylates, but an opposing trend to that previously discussed in terms of insect abundance and herbivory. That is, insect abundance was higher under elevated UV-B than under UV-A or shade; however, insect damage levels did not differ between enhanced UV-B and control treatments. Even though the literature provides ample evidence of decreases in herbivory under higher UV-B levels (either solar versus filtered or elevated versus ambient UV-B radiation), some specificity in the responses to UV-B radiation found in a few studies deserve further investigation. By the same token, most previous studies have focused on UV-B induced effects on the interaction between plant phenolics and insect herbivory. Conversely, the effect of this environmental factor on plant-herbivore associations mediated by other important phytochemical classes, such as alkaloids and terpenoids, are virtually lacking.

In contrast to UV light effects on plant-insect interactions, the impact of enhanced UV light on plant disease is not well understood. Some studies suggest that plant resistance to pathogens may be enhanced by exposure to UV radiation and that this type of radiation might even be required for the induction of plant defense responses (Fujibe et al. 2000; Kunz et al. 2006; Roberts and Paul 2006). For example, UV-C light has specifically induced the salicylic acid pathway and thus, the production of salicylic acid (elicitor of plant defenses) as well as pathogenesis-related proteins in Nicotiana tabacum, which are likely to enhance pathogen resistance (Yalpani et al. 1994; Fujibe et al. 2000).

Likewise, induction of flavonoids by pathogens has been observed under plant exposure to light (Raviv and Antignus 2004). However, some pathogens may inhibit the flavonoid biosynthetic pathway under light exposure and elicit the accumulation of other phytochemicals (Lo and Nicholson 1998; Logemann and Hahlbrock 2002), which may be more specifically associated to the plant response to pathogen attack. An example of “crosstalk” between responses to fungal attack and light has been provided by Lo and Nicholson (1998), who detected the induction of photoprotective anthocyanins in Sorghum bicolor exposed to light. However, synthesis of these flavonoids was overridden by upregulation of the genes activating the production of phytoalexins, which are involved in plant defense against fungal infections. UV light may also directly affect fungal pathogens by suppressing the production of spores and their ability to infect a host plant. More information is needed on these potential direct effects (but see Roberts and Paul 2006 for a brief discussion on this topic), which in addition to indirect effects may drive responses of plant pathogens to enhanced UV radiation.

Global Warming Effects

  1. Top of page
  2. Abstract
  3. Elevated CO2 Effects
  4. Elevated O3 Effects
  5. Enhanced UV Light Effects
  6. Global Warming Effects
  7. Conclusions and Future Research Directions
  8. Acknowledgements
  9. References

Global warming relates to the increase in mean temperature that has been observed since the mid-twentieth century resulting from anthropogenic emissions of greenhouse gases into the atmosphere (IPCC 2007). Since plant and insect physiological processes are directly dependent on temperature, both increased levels and fluctuations in this factor can have pronounced consequences for the interaction between these two diverse groups of organisms. For example, global changes in temperature can lead to ontogenetic mismatches between plants and insects. Dewar and Watt (1992) have demonstrated that an increase in mean winter temperature causes a phenological mismatch between the winter moth and its hostplant, the Sitka spruce, since this global change factor differentially affects the timing of the moth's larval emergence and that of the spruce's budburst. These phenological shifts can have dramatic consequences for coevolved plant-insect associations (Harrington et al. 1999).

In contrast to the previously reviewed global change factors, the individual effects of temperature on plant secondary chemistry and how these may impact plant-insect interactions are poorly known. Even though no generalizations can be made from the few studies that have assessed the effect of elevated temperature on plant secondary chemistry (summarized in Table 1), the outcome appears to be dependent on the plant species and the chemical type, as it has been previously observed for other environmental factors. For example, variable responses have been found in terms of plant phenolic compounds (Kuokkanen et al. 2001; Veteli et al. 2002; Williams et al. 2003; Hansen et al. 2006), glucosinolates (Pereira et al. 2002; Matusheski et al. 2004; Velasco et al. 2007), and volatile organic compounds (VOCs) such as terpenes and hexenal (Constable et al. 1999; Sallas et al. 2003; Snow et al. 2003; Loreto et al. 2006). Though, emission of VOCs seems to increase under elevated temperature, which could add to tropospheric ozone pollution (Loreto et al. 2006). In terms of glucosinolates, temperature has been shown to influence the production of glucosinolates in several cruciferous plants such as broccoli (Brassica oleracea var. italica), turnip rape (Brassica campestris) and Arabidopsis thaliana (Kirk and Macdonald 1974; Matusheski et al. 2004). Heating apparently causes an increase in the concentration of certain glucosinolate hydrolysis products such as isothiocyanates but a decrease in other derived-products like nitriles. These changes may impact the dynamic of natural communities, since glucosinolate hydrolysis products are known to mediate plant-insect herbivore interactions as well as tritrophic interactions between plants, herbivores and their associated parasitoids and predators (van Poecke and Dicke 2004).

As previously noted, little information exists regarding potential elevated temperature-induced changes in plant secondary chemicals and their potential effects on insect performance. Even though higher temperatures have usually been considered to have a favorable effect on insect growth and reproduction (Zvereva and Kozlov 2006), it has been hypothesized that increased production of secondary metabolites under these conditions may adversely affect insect performance (Dury et al. 1998). For example, Dury et al. (1998) found increased condensed tannin concentrations in Quercus robur exposed to elevated temperature, which might negatively influence the larval development and fecundity of phytophagous insects associated with this tree species. Other studies have indeed detected a decrease in female fecundity, and pupal weight (Buse et al. 1998), shorter developmental times (Johns and Hughes 2002; Johns et al. 2003; Williams et al. 2003; Chong et al. 2004), and increased survival (Chong et al. 2004) of insects reared on plants at elevated temperature. In addition, a lack of insect responses under elevated temperature regimes (e.g., unaffected insect growth or consumption) has been reported (Williams et al. 2000; Veteli et al. 2002). It should not be overlooked that insect responses reflect not only indirect effects of temperature through changes in plant quality but also direct impacts of this factor on insect herbivores. In contrast to the limited knowledge on direct CO2, O3 or UV light effects on herbivores, temperature is well-known for its pronounced direct effects on insect physiological processes. Temperature has a direct influence on the phenology, life cycle, growth and developmental rates as well as the distribution of insects among plants and geographic locations (Bale et al. 2002). Therefore, evaluating the interaction of this factor with other global change factors is fundamental for predicting the potential effect of global climate change on insect herbivores and their associated insect parasitoids and predators.

Conclusions and Future Research Directions

  1. Top of page
  2. Abstract
  3. Elevated CO2 Effects
  4. Elevated O3 Effects
  5. Enhanced UV Light Effects
  6. Global Warming Effects
  7. Conclusions and Future Research Directions
  8. Acknowledgements
  9. References

This review has focused on individual effects of major global change factors on plant secondary chemistry and its implications mostly for insect herbivores. Overall, the effect of global change factors on plant secondary chemistry appears to be plant species-specific (and genotype-specific) as well as dependent on the chemical type. However, some trends seem to be related to the type of environmental stressor as well. For example, phenolic compounds are usually positively enhanced by elevated CO2 and UV light (references included in Table 1). In particular, flavonoids tend to increase in response to UV light stress (Lavola et al. 2000; Veteli et al. 2006). Responses to O3 have been found more ambiguous, although it is worth emphasizing the specificity in the response of phenolic metabolites to this environmental factor. While some of these compounds are induced by both herbivory and elevated O3, others are specifically induced by O3per se. These “ozone-induced phenolics” have been considered potential bio-indicators of O3 pollution in natural ecosystems (Kanoun et al. 2001; Sager et al. 2005). Finally, responses of secondary chemicals to increased temperature are less well understood, although an increase in volatile organic compounds has been generally detected (Loreto et al. 2006).

The effect of global change factors on insect performance has been generally attributed to environmentally-induced changes in plant nutritional composition or secondary chemistry (Zavala et al. 2001; Roberts and Paul 2006). However, some factors such as temperature and UV light have been shown to directly influence insect physiology and behavior (Bale et al. 2002; Caputo et al. 2006). Numerous studies have evaluated the effect of global change factors on plant secondary chemistry and its implications for insect performance. However, few have actually quantified the association between these plant and insect traits (but see McDonald et al. 1999; Holton et al. 2003; Bidart-Bouzat et al. 2005), and to our knowledge, none has simultaneously assessed the significance of both direct and indirect effects in determining insect responses. In addition, more emphasis should be placed on tritrophic interactions and plant disease, which are also mediated by plant secondary chemistry and are not yet well understood under the framework of global change.

Future research should focus more on long-term effects of global change factors as well as their interactive effects on plant secondary chemistry. For example, it has long been predicted that plant growth as well as the production of carbon-based secondary chemicals are favored under elevated CO2 conditions (reviewed in Korner and Bazzaz 1996). However, we know little about the perpetuation of this effect over time, or how elevated CO2 interacts with many other abiotic and biotic factors that influence plant chemistry and performance (Bidart-Bouzat 2004). Even though we have not addressed interactive effects in this review, most of these studies usually include only two environmental factors (Lavola et al. 2000; Johns and Hughes 2002; Newman 2003; Caldwell et al. 2007 and references therein). Since the inclusion of each environmental factor can induce a differential response (in direction and magnitude), it is difficult to predict the outcome of present and future climatic changes based on the evaluation of only one or two factors at a time. Previous studies have suggested that temperature could ameliorate adverse effects of elevated CO2 on insect performance (Zvereva and Kozlov 2006), elevated CO2 could mitigate the effects of enhanced UV radiation or O3 on plant growth (Lavola et al. 2000; Valkama et al. 2007), higher UV levels might allow plants to increase their range of temperature and drought tolerance (Caldwell et al. 2007), and elevated CO2 might modify plant chemical responses to herbivory (Bidart-Bouzat et al. 2005). Yet, information is lacking regarding the combined effect of these abiotic and biotic factors on plant-insect interactions. Future studies should therefore focus on simultaneously testing the effects of multiple environmental factors to gain a more realistic perspective of how global climatic changes may impact the production of secondary chemicals and its potential implications for coevolutionary associations between interacting plant and insect species.

(Handling editor: Scott Alan Heckathorn)

Acknowledgements

  1. Top of page
  2. Abstract
  3. Elevated CO2 Effects
  4. Elevated O3 Effects
  5. Enhanced UV Light Effects
  6. Global Warming Effects
  7. Conclusions and Future Research Directions
  8. Acknowledgements
  9. References

We thank Juan L. Bouzat, Scott Heckathorn and two anonymous reviewers for constructive comments on this manuscript.

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  2. Abstract
  3. Elevated CO2 Effects
  4. Elevated O3 Effects
  5. Enhanced UV Light Effects
  6. Global Warming Effects
  7. Conclusions and Future Research Directions
  8. Acknowledgements
  9. References
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