kological Studies

olumes published since 1998 are listed at the end of this book.

James R. Ehleringer Thure E. Cerling M. Denise Dearing Editors

A Historv of Atmospheric CO, and Its Effects on Plants, Animals, and Ecosystems

With 15 1 Illustrations

Springer -

21. Herbivory in a World of Elevated CO,

Richard L. Lindroth and M. Denise Dearing

21.1 Introduction

All carbon fixed into plant biomass via photosynthesis is eventually consumed, either by herbivores (living tissues) or by saprophytes and detritivores (litter). Thus, the processes of herbivory and decomposition play pivotal roles in the cycling and storage of carbon in the biosphere (Fig. 21.1).

For several reasons, herbivory is uniquely important among ecological pro- cesses. First, it governs the flow of energy and nutrients to all higher trophic levels, thus strongly influencing the organization and dynamics of biological communities. Second, an extraordinary number of taxa are involved in the pro- cess; approximately half of known species consist of plants and their associated herbivores (Strong et al. 1984). Third, herbivory has contributed markedly as an agent of natural selection to the evolutionary radiation and diversification of both plants and animals (Spencer 1988; Sues 2000; Herrera and Pellmyr 2002). Interactions between herbivores and plants have been studied from a multitude of perspectives, ranging from the molecular basis of interactions to ecosystem level consequences and from evolutionary theory to agricultural application. A synthesis of these studies is beyond the scope of this chapter. Readers desiring additional information are encouraged to see recent reviews (Simrnonds 1998; Barrett and Willis 2001; Herrera and Pellmyr 2002; Strauss et al. 2002).

Atmospheric CO, influences herbivory via a complex array of direct, indirect, and interactive processes (Fig. 21.2). For example, changing levels of atmo-

Net Prlmary production: Quality (C:N)

Nutrient avallablllty

Figure 21.1. Processes affecting carbon cycling and storage in terrestrial ecosystems. Herbivory directly and indirectly influences the amounts and the rate of production of plant biomass.

spheric CO, are likely to alter plant chemical composition, which may alter host selection and population dynamics of herbivores. These changes, in turn, may effect shifts in nutrient cycling and community composition, thereby feeding back to influence concentrations of atmospheric CO,.

Concentrations of atmospheric CO, have exhibited striking variation over the history of life on Earth (Chapters 1, 2, 4, and 5). In this chapter, we describe how such variation has likely served as a driver of, and constraint on, the evo- lution of plants, herbivores, and their interactions. We focus on the direct effects of CO, rather than effects mediated by climate change. Bale et al. (2002) re- cently reviewed the effects of climate change on plant-insect interactions.

21.2 Determinants of Herbivore Food Selection

A host of factors determines which plants are, and are not, selected as food by herbivores. These can be broadly categorized as factors affecting either the qual- iv or quantity (e.g., availability) of food. While ultimately the diet of herbivores is determined by the interplay of both quality and quantity, for simplicity we initially discuss these factors independently.

21.2.1 Plant Quality

The three primary determinants of plant quality are nutrients, chemical defenses, and physical defenses (Schultz 1988; Lindroth 1989; Augner 1995). Herbivores derive all their nutrient requirements directly.from plant tissues, or from sym-

population dynamics evolutr I/ Atmospheric CO, I

Figure 21.2. A complex of interacting factors determines herbivore responses to atmo- spheric C02 concentrations, with feed-forward and feedback effects culminating in changes in ecosystem structure and function (adapted from Lindroth 1996a).

biotic gut microflora (e.g., rumen microbes) that digest plant tissues. Thus, plant chemical composition with respect to essential nutrients, such as protein, car- bohydrates, lipids, vitamins, and minerals, can determine a plant's suitability as food for herbivores. Of the various nutrients, protein (measured as total nitrogen) is generally regarded as the most limiting to herbivore growth and reproductive performance (Mattson 1980). Indeed, exceptionally low nutritive quality in some plant tissues has been postulated to evolve as a form of defense against herbi- vores (Augner 1995).

Plant chemical defenses encompass a vast number of secondary metabolites, including carbon-based compounds, such as phenolics and terpenoids, and nitrogen-based compounds, such as alkaloids and nonprotein amino acids. Gen- erally recognized examples of secondary compounds include condensed tannins, which are phenolics present in beverages produced from red grapes and cran-

21.2.2 Plant Availability

The absolute availability of plant material is largely a function of plant produc- tivity, which is governed by levels of soil nutrients, light, water, temperature,

7 berries, and caffeine, which is an alkaloid present in coffee and chocolate. Al- though nearly all plant species produce multiple forms of secondary metabolites, individual plant taxa are often characterized by particular secondary metabolites (the basis for the discipline of chemotaxonomy). These compounds protect plants by causing toxicosis or disrupting digestive processes in herbivores.

Finally, a variety of physical defenses influence the quality of plant tissues as foods for herbivores. The "barbed wire syndrome" refers to the possession of various bristles, spines, thorns, and trichomes, which ostensibly evolved as de- fense against herbivores (Levin 1973; Grant 1984). Internal constituents can also provide a form of physical defense. The best known of these is silica, which accelerates tooth wear and reduces the digestibility of plant tissues (McNaughton et al. 1985). Fiber is another physical defense that is ubiquitous in photosynthetic tissues and can be present in high concentrations (up to 50% dry weight). Most animals lack the enzymes required to digest fiber constituents, such as cellulose. However, many vertebrate herbivores have circumvented this problem through symbiotic relationships with bacteria and protists capable of digesting fiber. Mi- crobially aided digestion (fermentation) generates byproducts that herbivores use and rely on as a significant energy source (Robbins 1993).

These determinants of plant quality vary both among and within species, and over time. Variation in nutrient concentrations, chemical defenses, and physical defenses can be attributed to a number of factors, including inter- and intraspe- cific genetic variation; availability of critical resources (e.g., light, mineral nu- trients); prior exposure to herbivory (e.g., induced defenses); and developmental stage (Denno and McClure 1983; Karban and Baldwin 1997). Genetic variation, the magnitude of which differs among different habitats (gene by environment interactions), provides the basis for differential selection and evolution of these 1 plant traits.

Of course, herbivores have evolved an array of counter-adaptations such that no plant is completely resistant to all potential consumers. Herbivores have de- toxification systems consisting of scores of enzymes capable of transforming secondary compounds from plants into inactive compounds that are then ex- creted from the animal's body (Scheline 1978; Lindroth 1991). In addition, many herbivores produce specialized salivary proteins that bind to dietary tannins and reduce the potential toxicity of these compounds (Hagerman and Robbins 1993; Dearing 1997a). Some herbivores behaviorally manipulate levels of secondary compounds by storing plants until toxins decay, or mix and match plant foods to minimize the dose of any one toxin (Dearing 1997b; Dearing and Cork 1999). These examples represent a few of the sundry strategies employed by herbivores to deal with plant secondary compounds.

and CO, (Bloom, Chapin, and Mooney 1985). Although plant species differ with respect to optimal levels of resources required for growth, in general productivity is greatest when none of these factors is limiting or in excess.

Plant availability can exhibit tremendous temporal variation in strongly sea- sonal environments and thus can have consequences for herbivores in such hab- itats. For example, the Great Plains in North America have abundant vegetation in the spring and summer, but far less plant material is available during the winter. Herbivores that use such ephemeral resources have a number of strategies for coping with temporal reductions in plant availability. Examples include bison that migrate to other habitats, voles that remain but feed on lower quality veg- etation, and insects that overwinter in a dormant state.

Plant availability coupled with plant quality ultimately shape the diets and diet breadth of herbivores. When a choice is available, herbivores typically select plants of the highest quality: that is, low in secondary compounds and fiber and high in nutrients. Not surprisingly, high-quality forage is rare in nature (Dem- ment and Van Soest 1985). The limited quantity of high-quality forage constrains specialists on this resource to small body sizes. Most herbivores larger than a kilogram are forced to feed on a variety of plant species that vary in quality and quantity (Dernrnent and Van Soest 1985).

21.3 Effects of Elevated CO, on Plant Quality

Over the past several decades, the factors responsible for the evolution and diversification of plant chemical defenses have been the subject of considerable conjecture and debate (Bryant, Chapin, and Klein 1983; Coley, Bryant, and Chapin 1985; Hems and Mattson 1992; Hamilton et al. 2001). Central to many theories of plant defense is the notion that resource availability, particularly the balance of carbon to nutrient (e.g., nitrogen) availability, plays a major role in defining the types and amounts of chemical defenses accumulated by plants. Bryant, Chapin, and JClein (1983) introduced the "carbon-nutrient balance" hy- pothesis to explain intraspecific chemical variation on the basis of physiological responses of plants to shifts in the relative availability of carbon and nutrients. Coley, Bryant, and c h p i n (1985) incorporated resource availability into expla- nations of interspecific variation in plant defense over evolutionary timescales in the "resource availability" hypothesis.

According to these resource-based theories of plant defense, the amount and type of chemical defense expressed by plants is typically determined by two variables interacting over evolutionary time: inherent plant growth rate and re- source availability, both in absolute and in relative terms. Thus, when nutrient resources are limited, in absolute or relative amounts, plants with inherently slow growth rates will be favored over those with fast growth rates. In turn, slow

'

growth rates favor production of carbon-based defenses; although many of these compounds (e.g., tannins) have high costs of initial investment, they are rela- tively stable (low turnover rates). Production of nitrogen-based defenses (e.g.,

alkaloids) would be cost-prohibitive, due to limited nitrogen availability or higher turnover rates, or both, for such compounds. Current examples of these types of plants would include many gymnosperms (e.g., spruce and fir trees), which tend to be slow growing, adapted to nutrient-deplete environments, and defended by large concentrations of such carbon-based secondary metabolites as tannins and terpenoids. Alternatively, when nutrient resources are abundant, plants with rapid growth rates will be favored. The relative cost of nitrogen- based defenses is reduced, so plants expressing these forms of defense are more common. Current examples include the brassicas (containing glucosinolates) and solanaceous plants (containing alkaloids).

2 1.3.1 Geologic History

We propose that fluctuating levels of atmospheric CO, mediated the evolution and diversification of plant chemical defenses during the history of life on Earth. CO, concentrations were extraordinarily high during most of the Paleozoic and Cenozoic Eras, as much as four times higher than present levels. Plant defense theory suggests that during periods of high CO, concentrations, plant growth rates may have been restricted primarily by nutrient (principally nitrogen) de- ficiencies (e.g., Oren et al. 2001). Allocation of nitrogen resources to N-based secondary metabolites would have exacted an exceptionally high cost in terms of plant growth or reproduction. Thus, the evolution of N-based defense systems would have been constrained to a greater extent than that of C-based systems.

I

During the late Cretaceous period, however, coincident with the diversification I

of angiosperms, atmospheric CO, levels declined precipitously over a period of approximately 55 million years. At the beginning of the Tertiary, atmospheric CO, levels were only 35% to 40% of those of the previous 100 million years (Chapters 2, 4, and 5). CO, levels continued to decline during the Quaternary, but to a lesser extent and at a much more gradual rate. Thus at the onset of the Tertiary, the availability of nitrogen relative to that of carbon likely increased. We suggest that this shift may have facilitated the evolution and extraordinary diversification of nitrogen-based defenses in angiosperms (Table 21.1).

The evolution of nitrogen-based compounds vis-2-vis changes in atmospheric CO, levels is presented as a simple graphical model in Fig. 21.3. Under high levels of atmospheric CO,, as occurred prior to the Cretaceous, the construction cost of C-based compounds would have been reduced relative to the cost under current conditions. As atmospheric CO, levels declined during the Cretaceous, the cost of C-based compounds would have increased. We suggest that this decline reduced the differential in cost between C-based and N-based defenses, such that N-based secondary metabolites increased in abundance, frequency, and

i diversity in rapidly growing plant species. We extend this idea to the extremely low levels of atmospheric CO, that occurred during the glacial periods of the Quaternary. During those times, atmospheric CO, concentrations were so low (<200 ppm) that plant growth rates were constrained by CO, availability (Chap- ter 11). These conditions would have accentuated the cost of C-based defenses,

Table 21.1. Evolution appearance of classes of defensive chemicals in plants, adapted from Swain (1978)

- - -

Psilotum Horsetails Ferns Gymnosperms Angiosperms Class of Compound (400)* (370) (320) (200) (70)

Phenolics: Simple + + + + + Tannins - (+) ++ ++ ++ Terpenoids: Mono- - - - ++ ++ Sequi- and Di- - - + ++ ++ Tri- - + ++ ++ - N-Containing : Nonprotein amino acids - - + (+> + Alkaloids - - - (+> ++ Cyanogenic glycosides - - (+> (+> + Glucosinolates - - - - +

Age of dominance (million years ago)

Atmospheric CO, concentration

Glacials

Figure 21.3. A model of how variation in concentrations of atmospheric CO, over ge- ologic timescales likely influenced the evolution of chemical defense traits in plants. The relative costs of defense for compounds based on carbon (C) and nitrogen (N) are pre- sented at varying atmospheric CO, concentrations. As carbon becomes less abundant during the Cretaceous, the cost of C-based compounds relative to N-based compounds increases such that plants should invest in N-based compounds. As carbon becomes even less abundant during the interglacials of the Quaternary, plants should increasingly invest in N-based compounds.

such that N-based defenses would become more prevalent during periods of low CO, concentrations. Thus, over geologic time scales, even recent geologic time such as the last 150 ky, optimal plant defense traits may have been strongly influenced by CO, concentrations.

The primary goal of this simplistic model is to illustrate that the relative cost of C-based defenses correlates negatively with CO, levels, whereas the relative costs of N-based defenses remain constant over variable CO, levels. A limitation of this model is that it does not take into account other factors that also influence allocations to plant defense. For example, life history traits such as leaf lifetime may interact with CO, levels to ultimately determine the cost of a particular defense. Furthermore, the model presents only the cost side of the equation. "Expensive" defensives may be selected for if the benefits in terms of future reproduction outweigh the costs. Thus is it feasible for individual plants to pro- duce both C-based and N-based compounds when these other factors are incor- porated.

Current

21.3.2 Current and Future Trends

Prior to Cretaceous

The concentrations of atmospheric CO, predicted to occur in the next one hun- dred years are relatively low compared to levels prior to the Cenozoic. However, the rates of change in concentrations documented over recent decades and pre- dicted for the near future are much greater than experienced previously on Earth. Thus, biochemical and physiological adjustments of plants to high CO, condi- tions will occur without the benefit of significant periods of time for evolutionary adaptation. This consequence is especially relevant for long-lived species, such as most trees.

A growing body of literature describes the effects of enriched CO, on foliar chemistry. In general, levels of nitrogen and minerals decline, whereas those of C-based storage and defensive compounds (e.g., starch and tannins, respectively) increase (Lincoln, Fajer, and Johnson 1993; Le Thiec et al. 1995; McGuire, Miller, and Joyce 1995; Watt et al. 1995; Lindroth 1996b; Peiiuelas et al. 1996; Poorter et al. 1997; Bezemer and Jones 1998). Overall, changes in chemical composition are consistent with carbon-nutrient balance theory (Koricheva et al. 1998), although many exceptions (especially for terpenoid compounds) exist. Considerable variability in response occurs, however, among species, among genotypes within species, and in relation to the availability of other plant re- sources such as nutrients and water (Lindroth, Kinney, and Platz 1993; Roth, McDonald, and Lindroth 1997; Koricheva et al. 1998; Lindroth, Roth, and Nord- heim 2001).

A study by Lindroth, Roth, and Nordheim (2001) illustrates that a variety of interacting genetic and environmental factors determines the impact of high CO, concentrations on plant quality. Six aspen genotypes were grown under ambient and elevated (700 ppm) concentrations of CO,, in low- or high-nutrient soil. Foliar nitrogen levels declined by an average of 16% under high CO,, and the magnitude of decline did not vary among genotypes or in relation to nutrient

meta-analysis of the results of elevated CO, studies on C, and C, grasses in the Poaceae. Total biomass of C, species increased by 33% whereas total biomass of C, species increased by 44%. The CO, response in C, species was due to an increase in tiller biomass whereas C, species increased leaf area. In a long-term study of species in tallgrass prairie, C, species showed no change in percent abundance after 8 years of elevated CO, whereas C, species declined signifi- cantly (Owensby et al. 1999). However, this response appears to be highly de- pendent on the ecosystem. Morgan et al. (2001) found no change in the relative abundance of C,- C, species in the shortgrass prairie with increasing CO,.

21.5 Responses of Herbivores to C0,-Mediated Changes in Vegetation

As expressed by Thompson (1999): ". . . interactions between species are as evolutionarily malleable as the species themselves and have played a central role in the diversification and organization of life." Such is certainly true for herbi- vory as a means for the acquisition of essential nutrients by animals. Herbivory evolved frequently and independently in numerous phylogenetic lineages over the past 300 million years of life on Earth (Weis and Berenbaum 1989; Sues 2000). Indeed, the advent and proliferation of herbivory as a dominant feeding form was fundamentally important in the evolution of life, contributing to ex- plosive speciation (driven by coevolutionary interactions) as well as to the es- tablishment of expansive, grazing-dominated ecosystems. We suggest that atmospheric CO,, through its effects on plant quality and availability, acted as an abiotic driver of interactions between plants and herbivores, with consequent effects on the emergence, composition, and dynamics of entire ecosystems.

21.5.1 Geologic History

The fossil record provides little in the way of evidence of trophic interactions between plants and animals, so inferences about such interactions must be drawn from data such as biochemistry (Swain 1978), morphology (Sues 2000), and parallel cladograms (Fan-ell, Mitter, and Futuyma 1992). The ideas we present here are thus speculative but nonetheless suggest a key role for atmospheric CO, in mediating the evolution of plant-herbivore associations.

Shifting concentrations of atmospheric CO, over geologic timescales likely impacted herbivorous animals via changes in plant chemical composition. In- deed, Swain (1978) postulated that the extinction of dinosaurs may have been caused by the appearance and proliferation of alkaloids as flowering plants be- came dominant on Earth! Given, however, that various lineages of dinosaurs exhibited divergent and specialized morphological and digestive adaptations for accommodating plant diets, we find it difficult to believe that the reptiles were incapable of evolving effective metabolic adaptations for dealing with alkaloids

'I in their diets. For example, extant herbivorous reptiles discern between foods with and without alkaloids (Schall 1990).

Did dinosaurs and angiosperms coevolve, and were changes mediated to any extent by CO,? Recent work suggests that major groups of herbivorous dinosaurs were affected little by the initial radiation of angiosperms; how they responded to shifts in the distribution of flowering plants by the late Cretaceous remains speculative (Weishampel and Jianu 2000). However, during approx 25 million years of the Cretaceous, a distinct increase in diversity occurred in dinosaurs with feeding morphologies apparently suited to high fiber diets (Weishampel and Jianu 2000). The increase was in part due to the appearance of the ceratop- sians with novel parrotlike bills, as exemplified by Triceratops. The emergence of these unique feeding morphologies is suggestive of an increase in abundance of fiber-rich plants. It is possible that declining CO, levels during the Cretaceous resulted in more fibrous foliage as fiber content is inversely correlated with CO, levels (Runion et al. 1999).

A stronger argument can be made for the role of atmospheric CO, as a forcing factor in the coevolution of plant-insect associations. The explosive radiation of flowering plants and herbivorous insects is attributed, at least in part, to the reciprocal nature of their coevolutionary relationships (Ehrlich and Raven 1964; Farrell, Mitter, and Futuyma 1992). Indeed, evolutionary interactions between plants and insects are considered responsible, directly or indirectly, for much of the diversity of terrestrial life on Earth (Farrell, Mitter, and Futuyma 1992). We suggest that low atmospheric concentrations of CO, in the Cretaceous afforded plants with an entirely new form of armament against herbivorous insects: N- based allelochemicals. Concomitant with a reduction in the relative "cost" of N- based defenses, entirely new biosynthetic pathways evolved for the production of novel alkaloids, glucosinolates, cyanogenic glycosides, and so forth. The pro- liferation of various forms of these defenses was likely driven, at least in part, by coevolutionary interactions between plants and specialist insect feeders.

Changes in atmospheric CO, concentrations over geologic timescales also likely influenced herbivorous animals through changes in plant availability. One of the best-documented changes in plant availability occurred during the Mio- cene, when C, grasses expanded on a global scale (Cerling et al. 1997). The forcing factor behind the C, grass expansion is thought to be the interplay of low CO, and increased temperature (Ehleringer, Cerling, and Helliker 1997; Pagini, Freeman, and Arthur 1999). Major changes in the vertebrate herbivore fauna occurred concomitant to the grassland expansion. In general, species di- versity of woodland herbivores declined while herbivores suited for savannas increased (Cerling et al. 1997). A guild of grazing vertebrates appeared for the first time in hstory (MacFadden 2000). The evolution of grazers during the Miocene is exemplified by the radiation of the Bovidae (cow family), a group defined by its specializations for grassland feeding (Van Soest 1994).

Changes in overall plant productivity during the Miocene may also have af- fected communities of mammalian herbivores. CO, concentrations during the

will be mediated through climate change, particularly warming (see Fig. 21.2). Warmer temperatures affect the physiology, growth, development, phenology, and spatial distribution of herbivores (especially so for heterothems) as well as those of the plants on which they feed. Such indirect effects of CO, are beyond the scope of this chapter and have been covered in other recent reviews (Hughes 2000; Bale et al. 2002).

21.6 Summary

Atmospheric CO, has likely served as a significant driver of, and constraint on, the evolution of plants, herbivores, and their interactions. We propose that CO, has had a major impact on the nutritional quality and quantity of plants over evolutionary time. Low levels of CO, may have provided opportunity for evo- lution of novel N-based plant compounds, which in turn provided the raw ma- terial for an explosive diversification of interacting plant and animal species. In addition, changes in plant abundance and community structure mediated by al- terations in atmospheric CO, likely had significant impacts on herbivore com- munities. Although levels of CO, predicted to occur in the next century are lower than concentrations witnessed in the past, the rate of change may preclude concomitant evolution of some plant-herbivore assemblages.

Acknowledgments. We thank P. Coley for invaluable comments on plant defense theory and N. Lindroth for preparation of the figures. The National Science Foundation (Ecology Program) and USDA (National Research Initiatives Com- petitive Grants Program) supported the research of R.R. Lindroth described in this chapter. The National Science Foundation (IBN '007-9865) and the Packard Foundation supported the research of M.D. Dearing.

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