NATURAL TOXINS 1:I 97-208 (1992)

Ecology of Plant-Herbivore Communities: A Fungal Component? Kyle E. Hammon and Stanley H. Faeth Department of Zoology, Arizona State University, Tempe, Arizona

ABSTRACT We consider how microorganisms may alter conventional theories of the organization of plant-herbivore communities. We focus on endophytic fungi and their role in mediating interactions among herbivores, their host plants, and natural enemies. We propose hypotheses about the role of microbes in plant-herbivore communities and suggest ways to test these hypotheses. An initial approach to the overwhelming complexity of interacting species is to view species as components of functional groups, be they micro- or macroscopic, that potentially affect the ecology and evolution of host plants. 1991 W I I ~ ~ - L I Sinc. S, @

Key Words: Endophytic fungi, Herbivory, Host selection, Host range, Succession, Plant-pathogeninteractions, Plant-insect interactions

INTRODUCTION

natural enemies will potentially affect populations and community structure of plants and their herbivores. Microorganisms that live on surfaces and within tisWhile there are intriguing possibilities for microbes to sues of plants are typically very diverse and abundant influence population dynamics and community structure [e.g., Dickenson and Preece, 1976; Blakeman. I98 1 ; of herbivore-plant communities, ecologists should not Wicklow and Carroll, 1981; Fokkema and van den Hueautomatically assign overwhelming importance to all miVal, 1986; Andrews and Minano, 1991; Bills and Policrobes on plants. Macroscopic herbivores consume or shook, 19911. The group includes viruses, bacteria, mycocontact many microbes with literally every bite or touch plasmas, fungi, and protozoa. Despite their diversity and of the leaf, but most of these likely have little or no effect ubiquity, microorganisms have been generally overon either the plant or macroscopic herbivore. The challooked in studies of the ecology and evolution of herlenge for ecologists is to: 1) elucidate which of the hunbivores and their host plants [Price et al., 1986; Letourdreds or thousands of microbial species that live on or in neau, 1988; Berenbaum, 1988; Marquis and Alexander, tissues of a plant species potentially affect the ecology 1992; but see Krischik et al., 1988; Savopoulou-Soultana and evolution of plant-herbivore interactions; 2) deterand Tzanakakis, 1988; Bowers and Sacchi, 19911. Acmine when and under what environmental conditions cumulating evidence suggests that at least some species of these species exert their effects; and 3) ascertain the role microbes mediate interactions between herbivores and of microbes in the ecology and evolution of plant-herbihost plants, interactions within or among herbivore spevore interactions relative to many other factors exerting cies, and interactions between herbivores and their natuselective pressure on plants, macroscopic herbivores, and ral enemies. For example, Karban et al. [1987] showed their natural enemies. that Verticillum wilt infections decrease colonization and In this paper, we review some conventional hypotheses survival of mites, presumably by induction of phytoalexabout spatial and temporal patterns in herbivore-plant ins, a broad class of low molecular weight antibiotic communities. We suggest that inclusion of microorgancompounds known to affect phytophagous insects [e.g., isms can provide new insights about these patterns and Green and Ryan, 1972; Russell et al., 1978; Sutherland et their causes. We generally focus our attention on the al., 1980; McIntyre et al., 19811. Other low molecular effects of endophytic fungi on communities of phytophaweight compounds produced by pathogenic infections gous insects, their host plants, and their natural enemies. may serve as attractants to the parasitoids of phytophagous insects [Whitman, 19881. In general, we expect that any microorganism that alters the attractiveness or Received June 1, 1992; accepted for publication August 20, 1992. PhYsiological suitability Of plants to herbivores Or those Address reprint requests to Dr. Stanley H. Faeth, Department of zoology, that alter herbivores’ attractiveness or suitability to their Arizona State University, Tempe, Az 85287-1501. Q

1992 WileyLiss, Inc.

198

HAMMON AND FAETH

metabolites from Aureobasidium pullukuns, which grows both endophytically and epiphytically, and other epiphytic species (Geoirichum cundidum, Fusurium uvenuceum, F. sporotrichoides, and Penicillium cyclopium) inRecently, ecologists have focused attention on one terfere with spruce budworm (Choristoneurufumiferunu) group of microbes, endophytic fungi, as potentially powdevelopment and increase larval mortality in mixed erful mediators of herbivore-host plant interactions [Carspruce-fir forests [Miller et al., 1985; Strongman et al., roll, 1988; Clay, 1988; Strong, 19881 for two reasons. 1988, 19901. Some of these fungi are typically viewed as First, endophytic fungi (fungi that produce asymptoFusurium uvenuceum) [Booth plant pathogens (e.g., matic internal infections, sensu strictu [Carroll, 19861) 11, yet produce chemicals toxic to herbivorous insects 197 purportedly interact mutualistically with plants by deter[Claydon and Grove 1984; Grove and Pople, 19801. Churing or inhibiting colonization, reducing growth, or killetophoma quercifoliu is described as a pathogen of oak ing macroscopic herbivores and microscopic pathogens [Cooke, 1878; Chakravorty and Das, 19811. On Emory of their hosts [Carroll, 1988, 1991a,b; Clay, 1988; Strong, 19881. The evolution of mutualistic interactions are gen- oak (Quercus emoryi), however, it grows endophytically erally rare relative to other ecological interactions be- in living tissue and inhibits development of some insects, tween species [Thompson, 19821. That some fungi and and grows saprophytically in dead tissues (Hammon and plants interact mutualistically is further supported by Faeth, unpublished results). The term “endophyte” is studies showing that the cost in terms of plant fitness of spatially descriptive, but is clearly not synonymous with harboring endophytic fungi appears negligible [Carroll, “plant mutualist” or any other ecological relationship. 1988; Clay, 19881, and may even increase plant fitness in We also expect that the direction and strength of interacways unrelated to herbivory. For example, the presence tions between plants and endophytes vary greatly with of endophytes can enhance competitiveness in the ab- the presence of other species (e.g., competitors) and envisence of herbivores [Sutherland and Hoglund, 19901. ronmental settings (e.g., plant age, nutrient availability). On evolutionary grounds, we predict mutualistic endoFisher et al. [I9861 and Carroll [I9881 suggest that endophytic fungi should be rare compared to antagonistic phytic fungi in gorse (Ulex spp.), some of which are normally coprophilous, increase nutrient availability endophytes (plant pathogens), contrary to impressions in during senescence and after fires. We caution here, how- the literature that most fungal endophytes are mutualisever, that the number and extent of studies examining the tic in their interactions with plant hosts. Mutualistic eneffects of endophytic fungi on plant fitness are very lim- dophytes are thought to have evolved from parasitic speited, particularly in non-agricultural systems. Second, the cies [Carroll, 19881, as are most ecological mutualists mode of action by which fungal endophytes affect her- [Thompson, 19821. Attenuation of virulence in such hostbivores is largely chemical via the production of myco- parasite relationships to the point of mutualism is not toxins. We are not aware of reports of mechanical ob- necessarily a probable outcome in evolutionary time struction or other non-chemical antibioses by [Williams and Nesse, 19911, as was once thought [e.g., endophytes. This mechanism of resistance to herbivores Dobzhansky, 19511. The conditions for evolution of mufits well with most ecological and evolutionary theories tualism from host-parasite interactions are very restricof plant defenses against herbivores that traditionally tive [Gill and Mock, 1985; Massad, 1987; Williams and have been based upon plant allelochemistry. Nesse, 199I]. We can predict, however, when endophyteWe should not, however, expect that all fungi that occur host relationships are more likely to be mutualistic based endophytically for all or part of their life stages act mutua- upon the theoretical predictions of Ewald [1987, 1988, listically by increasing plant fitness. Increasing evidence 19911 and Ewald and Schubert [1989] as summarized in suggests that endophytic fungi are highly variable in their Williams and Nesse [1991]. We expect a higher probabilecological effects on herbivores in time and space. For ity of mutualism in fungal species that are transmitted example, Johnson et al. [1982] found that two aphid vertically (i.e., from parent to seed) since increasing host species preferred endophyte-free tall fescue, but the same survival and fecundity directly increases transmission. two species showed no preference for either endophyte- Fungi transmitted by inanimate means such as rainfall or free or endophyte-infected perennial ryegrass. Latch et al. rainsplash should be more virulent than those transmit[1985]showed that aphids avoided tall fescue infected with ted vertically or by animal vectors since transmission the endophyte Acremonium coenophiulum but not Phiulo- relies on production of large numbers of propagules to phoru sp. Likewise, plant resistance to nematodes via overcome dilution and random dispersal effects. Secendophytes varies depending on nematode species, plant ondly, fungi that occur alone within the host plant are species,fungal species, and local edaphic and environmen- more likely to be mutualists than those co-occurring with tal factors [Kimmons et al., 1990; O’Day et al., 19901. other fungal species. Competition among fungal species Alternatively, mutualistic interactions are not re- or even among clones of the same species in a host plant stricted to fungi that grow endophytically. Toxic is predicted to select for increased virulence and hence ENDOPHYTIC FUNGI: MUTUAUSTS, ANTAGONISTS, AND NEUTRALISTS

FUNGI AND HERBIVORE COMMUNITIES

199

increased transmission. Interestingly, these two charac- have centered on plant allelochemistry beginning with teristics are found in the fungal endophytes of grassesEhrlich and Raven’s [I9641 synthetic paper postulating they are vertically transmitted and more than one species that insect and plant diversity are evolutionarily linked are rarely found in an individual plant [Clay, 19881. Be- via secondary chemistry. More recently, however, hycause of their toxic effects on livestock, the endophytes of potheses about the evolution of host plant specificity grasses have attracted the attention of agriculturalists, have moved from a strict allelochemical focus, stimumycologists, botanists, and ecologists. Perhaps this dis- lated by evidence that contradicts ideas of plant-insect proportionate attention has contributed to the impres- coevolution based only on chemistry [Bernays and Grasion that endophytes must be mutualists. As studies of ham, 19881. Other hypotheses now include nutritional non-grass endophytes increase, a more balanced view of and physical barriers [e.g., Southwood, 1973; Scriber and fungal endophytes and their role in plant-herbivore com- Slansky, 198I], generalist predators [Bernays and Gramunities should emerge. ham, 19881, enemy-free space from parasites [Lawton, For convenience, we will use the term “fungal endo- 19861, and temperature-imposed restrictions on larval phyte” in the following discussion of fungal effects on growth and voltinism [Scriber and Lederhouse, 19921. plant-herbivore interactions and communities. However, These hypotheses are not mutually exclusive of the in doing so, we are extending the term to mean any secondary chemistry hypothesis. Rausher [ 19881suggests fungal species that inhabits interior tissues of a plant for that natural enemies may initiate specialization but host at least part of its life cycle. We do not restrict ourselves plant chemistry maintains it. Scriber and Lederhouse’s to only fungi that positively affect the host plant (mutual- [ 19921 voltinism-suitability hypothesis proposes that inists), or to those that remain asymptomatic and internal teractions among host plant quality, length of the growthroughout their entire life cycle. Further, some exam- ing season, and herbivore natural enemies may determine ples of microbe-plant-herbivore interactions and com- patterns of voltinism and host plant specialization. In munities may include nonfungal species. Our intention in their scheme, polyphagy may be favored in geographic including nonfungal species here is to draw attention to regions where the same number of generations can be the diverse nature of microorganism-plant-herbivore in- produced regardless of the host plant species. In these teractions and to encourage the broadest possible view of regions, there is no selective penalty for using hosts with the microbial component in plant and herbivore commu- lower physiological suitability in terms of number of gennities. erations and use of such hosts may reduce attack by natural enemies. The latter is consistent with Lawton’s SPATIAL PAllERNS OF HERBIVORY [ 19861 proposal that escape from parasitoids selects for Host Plant Range host range expansion. We do not intend to review the vast literature on insect A central yet still controversial question in the ecology of insect-plant interactions is what determines patterns of host plant range; there are many excellent reviews to this host plant range among phytophagous insect species end [ e g , Denno and McClure, 1983; Mitter et al., 1991; [e.g., Barbosa, 1988; Bernays and Graham, 1988; Court- Fritz and Simms, 1992; Hunter et al., 1992; Stamp, 19921. ney, 1988; Ehrlich and Murphy, 1988; Fox, 1988; Janzen, Our aim is only to suggest that microbial plant associates 1988; Jermy, 1988; Rausher, 1988; Schultz, 1988; Strong, could be important factors for hypotheses about host 1988; Thompson, 19881. Most phytophagous insects are range of herbivorous insects. more specialized than expected by chance [Futuyma and Gould, 1979; Price, 1983; Bernays and Graham, 19881 The hngal endophyfe explanation Fungi on or in plants often produce mycotoxins, notaand feed on relatively few plant families, although this pattern varies among herbaceous and woody plants bly alkaloids. Herbivory may stimulate fungi to begin or increase production of mycotoxins. The presence of fungi [Futuyma, 19761. and their toxins may deter colonization, inhibit growth ?be conventional explanations of, or kill phytophagous insects [Miller et al., 1985; Explanations for patterns of host plant range of her- Bacon et al., 1986; Calhoun et al., 1992; Carroll, 1988, bivores have focused on three different levels of causality: 1991a,b; Clay, 1988, 1989; Pederson et al., 1988; Strong1) the sensory/behavioral level of host plant acceptance man et al., 1988; West et al., 19881. Thus, infections by or rejection by ovipositing females or feeding stages [e.g., endophytic fungi add to the repertoire of plant constituSzentesi and Jermy, 19901, 2) the physiological and eco- tive and induced “defenses,” nutritional and physical logical levels of growth, development, and survival of barriers, and phenological variability that colonizing and feeding stages [e.g., Courtney and Kibota, 19901, and 3) feeding stages of an insect species must overcome in the evolutionary level of phylogenetic constraints that order to use a plant species as a host. Generally, the alkaloids produced by fungi are unique are superimposed over the first two levels [e.g., Mitter et al., 19911. Historically, explanations at all three levels and are not synthesized by plants except by those plants

200

H M O N AND FAETH

with purportedly transgenic factors from fungi [Jarvis et al., 19911. Thus, the presence of fungi in plants may act to create functionally another chemical “species,” whose phytochemistry may be as different from a non-infected conspecific as a plant from a different family. Further, variation in host plant phenotype may be increased not only by the presence of fungi, but also by genotypic variation within the fungal population [Hill et al., 1990, 19911. Is a “monophagous” species feeding on a plant taxon that hosts a suite of microbial species with their varying chemical compounds more specialized than an herbivore that can feed on an equivalent number of host plant species from disparate plant families? We contend it is not, and that traditional perceptions of monophagy and polyphagy may need to be radically altered if plant microbial associates are included. Inclusion of microbes may also help to explain discrepancies between behavioral acceptance or rejection by insects and their physiological performance. In addition to chemical composition, pathogens can alter plant temperature [Toler, 1981 ; Blazquez, 19901, which we suggest may alter oviposition and feeding choices. Could rejection of plant species in the field by ovipositing females be related to fungal infections not present in laboratory grown plants used in bioassays? Could the failure to find predicted tradeoffs in polyphagy and monophagy [e.g., Bernays and Graham, 1988) be explained either by failure to consider microorganisms that can affect performance and survival of insects, or perhaps because inclusion of fungally infected plants extends or shrinks insect host ranges biologically, but not taxonomically? Phenology of host plants can strongly affect suitability of plants as hosts, and can also be altered by microbial infections. For example, Pegg [I9811 showed that microbial infestation causes premature leaf abscission which has been linked with increased mortality for sedentary herbivores like leaf miners [Faeth et al., 1981; Simberloff and Stiling, 1988; Auerbach and Simberloff, 19891. Alternatively, Carroll [1991a] suggested that endophytic fungi in senescent leaves produced cytokinins and other metabolites that produce “green islands” [Kiraly et al., 1967; Goodman et al., 19861. Some leafminers can survive in these “green islands” even after the leaf has abscised [Engelbrecht et aI., 1969; Faeth 1985a, 19871. In Scriber and Lederhouse’s [ 19921 voltinism-suitability hypothesis, they predict specialization in localities where temperatures permit additional generations, but only on plant species with high quality tissues. The hypothesis also predicts that ovipositing females select high quality hosts to maximize survival of the second generation. Because microbes can functionally lengthen or shorten growing seasons by altering plant phenology, we suggest that they should be considered within the context of this hypothesis.

Microorganisms also can influence attack by natural enemies. In addition to altering plant phenology, microbial infections can modify plant chemistry and morphology that could change feeding behavior, developmental rates, physiological state, and movement patterns of insects. These changes, in turn, can alter vulnerability of insect herbivores to attack by natural enemies [e.g., Schultz, 1983; West, 1985; Faeth, 1985a, 1991a,b; Gross and Price, 1988; but see Fowler and MacGarvin, 1986; Bergelson and Lawton, 19881. We suggest that natural enemies of herbivorous insects might also use fungal metabolic products to locate their hosts. Recent evidence [e.g., Turlings et al., 19901 indicates that parasitoids can locate insect hosts via green leaf volatiles produced after damage to plants by insects. Since some endophytic fungi can be stimulated to become metabolically active by herbivore damage [Carroll, 1986; Sherwood-Pike et al., 19861, any cues produced by actively-growing fungi could serve as attractants to parasitoids of the herbivores. We know of no studies showing that endophytic fungal infections are associated with increased natural enemy attack. However, phytoalexins produced by, or in response to, pathogenic infections attract both insect herbivores [Harborne, 19831 and parasitoids [Whitman, 19881. Although research on endophytic fungal toxins has focused on direct antibiosis, an interesting line of research might also examine the effect mycotoxins and other metabolites have on insect natural enemies. If endophytic fungi strongly affect natural enemies of herbivores, then ecologists will need to incorporate fungi into hypotheses about host plant specialization that include natural enemies, such as the generalist natural enemy hypothesis [Bernays and Graham, 19881 or the voltinism suitability hypothesis [Scriber and Lederhouse, 19921. Levels of Herbivory and Plant Defenses

Types and concentrations of plant compounds with antiherbivore activity vary widely among and within plant species and temporally. Recent hypotheses suggest that resource availability, inherent growth rates, carbon/nutrient balance, and stress influence the types and amounts of carbon-based (e.g., phenolics) or nitrogen-based (e.g., alkaloids) defenses. For example, plant species growing in nutrient-poor environments are expected to evolve higher levels of carbon-based defenses than species in nutrientrich environments [McKey et al., 1978; Bryant et al., 1983; Coley et al., 1985; Chapin et al., 19871. Inherent growth rates of species are also proposed to alter allocation to Cor N-based defenses among plant species, with slower growing species containing more phenolics than co-occurring fast growing species [Coley, 1983, 1988; Denslow et al., 1990; but see Shure and Wilson, 19921. Environmental conditions can also change allocation to carbon-based defenses within a plant species in ecolog-

FUNGI AND HERBIVORE COMMUNITIES

ical time [Bryant et al., 19831. For example, if light levels are high and nutrients low, plants convert more carbon to phenolic compounds than if carbon/nutrient levels are more favorable [Larsson et al., 1986; Chapin et al., 19871. Similarly, abiotic stress to plants, although difficult to quantify or standardize [Larsson, 19891, may also alter carbonlnutrient balance and render plants more or less vulnerable to herbivory [White, 1974, 1984; Rhoades, 1979; Waring and Pitman, 1985; Mattson and Haack, 19871. The presence of endophytic fungi can change growth and photosynthetic rates of plants under differing nutrient or stress levels and thus alter carbon/nutrient balance. Although the effect of varying nutrient or stress levels on growth rates of endophyte-infected woody plants has not yet been tested, several grass-endophyte systems have been examined. Marks and Clay [I9901 found that nutrient (nitrogen) and C 0 2 addition to greenhouse-grown perennial ryegrass (Lolium perenne) resulted in greater growth in infected than uninfected clones at all enrichment levels of COz and nutrient levels, but particularly at high nitrogen levels. However, Cheplick et al. [I9891 found that grasses with endophytic infections had slower growth rates than noninfected plants when nutrients were limiting. Fertilization of Chewings fescue (F. rubra) reduced seed abortion caused by its endophyte, but did not affect distribution of the fungus within plant tissues [Sun et al., 19901. Collectively, these studies suggest that harboring endophytes may be costly to plants in terms of growth rates and plant competition under conditions of low to extreme nutrient stress [Clay, 19901, and may explain why both infected and uninfected plants typically occur in most natural plant populations. On the other hand, endophyte infected grasses appear to be more resistant to moisture stress [Clay, 19901, in terms of successful germination [Pinkerton et al., 19901 and dry matter production by established plants [Arachevaleta et al., 1989; Read and Camp, 1986; West et al., 19881, although resistance depends on plant and fungal genotype [Richardson et al., 19901. Clearly, the production of mycotoxins is not the only pathway by which endophytes affect plant-herbivore communities since they can alter photosynthetic rates and hormonal, water, nutrient, and carbon balance, at least in grasses [Clay, 19901. The extent of these physiological changes, in turn, are influenced by abiotic conditions such as resource availability and stress. If endophytic fungi also alter physiology of non-graminaceous plants, then we expect widespread, endophyte-related shifts in plant-herbivore community structure due to changes in inter- and intraspecific competition for resources and susceptibility to herbivory. In terms of the latter, endophyte-related variation in host quality is superimposed over the enormous temporal and spatial var-

201

iation in nutritional and allelochemical makeups of host plants that confront herbivores. For example, in ecological time, endophyte-induced increases in photosynthetic rates could alter carbon/nutrient balance and hence increase phenolic and carbohydrate levels in the host plant. Marks and Clay [I9901 suggested that such increases in C-based compounds could dilute N-rich alkaloid mycotoxins and their effects on herbivores. In evolutionary time, we might expect plant species with endophytes to be found in nutrient-rich environments with high herbivore pressure, and less often in nutrient-poor environments with low levels of herbivory. These predictions are based on very few studies of the performance of endophyteinfected relative to endophyte-free plants under varying conditions of abiotic factors, presence of herbivores, and plant competition. As more studies accumulate, we should have a clearer picture of how inclusion of endophytes alters our theoretical views of the evolution and ecology of plant defenses. Do Fungi Affect Within-Species and Within-Plant Patterns of Herbivory?

Insect herbivory is highly variable among individuals of a given plant species. This level of variability may be caused by environmental, genetic, and ontogenetic conditions that influence plant dispersion and association with other plant species, allelochemistry, nutrition, morphology, phenology, and interactions with natural enemies of insects [for reviews see Denno and McClure, 1983; Faeth, 1987; Price, 1992; Ohgushi, 19921. The presence of fungal infections, be they pathogenic or mutualistic, can alter virtually any individual factor or combinations of factors. We must therefore consider the presence of fungi as another level of variability that potentially influences among-plant patterns of herbivory. For example, Taper and Case [I9871 found that abundances of cynipid galls among trees were positively related to tannin levels, partly because increased tannins protect larvae from an unidentified gall-inhabiting fungus [Taper et al., 19861. Conventional wisdom would predict the opposite: trees with higher tannin levels should have lower herbivore loads. Microbial interactions with plants and insects can clearly alter our concepts of plant defenses. Similarly, herbivory varies greatly within plants, particularly in architecturally complex plants such as trees, for many of the same reasons as variability among individual plants. In Emory oak, for example, leafmining insects (Cameraria sp. nov. Davis) are concentrated on interior, shaded parts of the canopy [Bultman and Faeth, 1986; Faeth, 1990, 1991al. Leafmining adults select interior leaves that are larger [Faeth, 1991al and less prone to leaf abscission [Bultman and Faeth, 19861. The sedentary and slow-developing larvae survive better and attain greater pupal mass in large and longlived leaves [Bultman and Faeth, 19861. Interior leaves,

202

HAMMON AND FAETH

however, are also prone to higher levels of infection by endophytic fungi, which can increase development time and decrease survival of larval leafminers (Hammon and Faeth, unpublished results). We have hypothesized that ovipositing females may select leaves within interior regions that are less likely to become infected by endophytic fungi. Ovipositing females prefer leaves in shaded regions with higher levels of tannins [Faeth, 19901 which are known to have fungicidal properties [Zucker, 1983; Seaman, 1984; Brownlee et al., 19901. We have tested the effects of tannins purified from Emory oak leaves on the growth of Chaetophoma quercifoliu, an endophyte of Emory oak. While this fungus can tolerate concentrations of tannins lethal to most fungi, its growth is retarded by tannin levels comparable to those found in some interior leaves (Hammon and Faeth, unpublished results). Thus, the variability in fungal infections within plants may account for some within-tree variation in folivory by this leafminer. We are continuing tests of this hypothesis in the oak-endophytic fungi-leafminer system. Could microorganisms be involved in patterns of herbivory at even finer spatial scales within plants? Overdispersed patterns of damage within leaves are hypothesized to result from behavioral adaptations of insects to avoid localized induction of chemical defenses by plants [e.g., Edwards and Wratten, 19831 or the attraction of their natural enemies via visual cues or induced chemicals [e.g., Schultz, 1983; Faeth, 1987, 1988; but see Hawkins, 1988; Faeth, 19921. Many endophytic fungal species remain asymptomatic within plants until stimulated by herbivory to grow and produce mycotoxins [Clay, 1988; Carroll, 19881. Overdispersion of leaf damage may therefore be the result of insects avoiding mycotoxins rather than induced defenses directly produced by the plant. Carroll [1991a,b] and Cheplick and Clay [1988], for example, consider that endophyte infections function as acquired immunity of plants against insect attack. We hypothesize that fungal endophytes are at least partially responsible for patterns of herbivory within plants. A correlative test of this hypothesis would be to determine differences in the dispersion of leaf damage in plants with and without endophyte infections, preferably for a wide array of insect-plant systems, since feeding behavior of some insect species is phylogenetically constrained. Manipulative tests of the hypothesis could be accomplished by controlling endophytic fungal infections in various plant parts and monitoring insect feeding patterns. SEASONAL TRENDS IN HERBIVORY

New foliage on woody plants generally is more susceptible to herbivory. In temperate zones, a large fraction of herbivory on perennial plants occurs in the spring when most new leaves are produced [Feeny, 1970; Faeth,

1985b, 19871. New leaves produced after the spring flush also tend to be more susceptible to herbivory than mature foliage [Fowler and Lawton, 1984; Faeth and Rooney, 1992; but see Du Merle, 19881. In tropical regions, new leaves of woody plants tend to be more susceptible to herbivores whether they are produced synchronously at the beginning [Coley, 19831 or asynchronously later in the wet season [Rockwood, 1974; Lieberman and Lieberman, 1984; Aide, 19881. The Conventional Hypotheses

Feeny [1970, 19751 and Rhoades and Cates [1976] proposed that seasonal changes in intensity of herbivory are driven by phytochemical changes that reduce palatability and digestibility of plant tissues. In Quercus robur, protein levels decrease while tannins and fiber content increase seasonally [Feeny, 19701. Tannins and physical toughness were postulated to have evolved as “quantitative defenses” in long-lived plants that were likely to be discovered in ecological time by their herbivores. More recent studies of herbivory, however, do not corroborate this pattern [e.g., Coley, 1983; Raup and Denno, 1983; Karban and Ricklefs, 1984; Faeth, 1985b; Puttick, 19861, and Zucker [1983] has argued against the evolutionary dichotomy of chemical defenses in long-lived and short-lived plants for biochemical reasons. In addition to seasonal changes in constitutive chemical defenses, induction of chemical defenses is also postulated to influence seasonal patterns of herbivory [Karban and Myers, 1989; Faeth, 1987, 19881. Some phytophagous insect species, particularly sedentary ones, may have evolved to oviposit and feed late in the growing season to avoid short-term phytochemical or phenological changes associated with early season herbivory [West, 19851. The predation hypothesis [Holmes et al., 19791 states that predation by nesting adult birds and their fledglings peaks in mid-summer in temperate zones and selects for early and late season feeding by many phytophagous insect species. Variation in attack by natural enemies may not be independent of hypotheses based on plant chemistry, morphology, or phenology. Constitutive or induced changes in plants may enhance attack on herbivores by vertebrate [Heinrich and Collins, 19831 and invertebrate predators or parasites [e.g. Faeth, 1986; Turlings et al., 19901. Finally, seasonal patterns of herbivory may also be influenced by abiotic factors, particularly temperature and precipitation [Faeth, 1985bl. In temperate zones, increases in summer temperatures can decrease adult fecundity and larval development. The same may be true for tropical zones where the combination of lower humidity and higher temperatures during dry seasons inhibits development of insect herbivores.

NNGl AND HERBIVORE COMMUNITIES

The Fungal Endophyte Hypothesis

Frequency of fungal endophyte infections in woody perennial plants tends to increase with increased tissue age. In Emory oak (Quercus emoryi), for example, infections by the endophytic fungus Chaetophoma quercfolia do not appear in leaves until late-summer rains disperse spores and humidity is high enough for spore germination. Further, twig age is a significant predictor of infection frequency, and this suggests that older twigs are a likely source of spores infecting leaves (Hammon and Faeth, unpublished data). Similarly, the endophyte Rhabdoclineparkeri in Douglas fir does not appear in the youngest age-class of needles until the fall rains begin [Carroll, 199I a]. Carroll [ 199la] suggested that the late appearance of the endophyte preempted ecological interactions with most insect herbivores since they tend to feed early in the season. We propose an additional hypothesis based on an evolutionary perspective: herbivory by least some macroscopic species is concentrated early in the growing season as an evolutionary response to mycotoxins produced by late season endophytic fungi. Evolutionary hypotheses are difficult to test in ecological time. We can, however, make some predictions that are consistent with the fungal endophyte hypothesis. We predict that late-season herbivore species would prefer and perform better on infected tissues than would early season herbivore species on the same host plant, controlling for other chemical or morphological differences between newer and older tissues. We also predict that lateseason feeders should prefer and perform better on endophyte infected leaves when given a choice between infected and uninfected leaves. Just as many oligophagous insects have evolved to use noxious compounds from their host plants as nutritional requirements or defenses against their own natural enemies and pathogens [e.g., see references in Krischik, I991J, one expects adaptation by insect species that have been consistently associated with a host plant and its microbial associates in evolutionary time. For example, adult mycophagous flies “pollinate” the sexual form of an endophytic fungus they feed upon in grasses [Bultman and White, 19881, yet the same fungus is toxic to many generalist herbivores. PLANT COMMUNITY SUCCESSION-A CONNECTION?

FUNGAL

Classical theories of succession in plant communities have focused on the magnitude and direction of interactions among plant species as the major force driving changes in species composition and relative abundances [Horn, 1976; Connell and Slayter, 1977; Connell et al., 19871. The metabolic costs of harboring endophytes appear to be negligible, at least for some fungus-plant associations, and in some cases fungi appear to enhance the competitive ability of infected plants [Carroll, 1991a,b;

203

Clay, 19911. Thus, based upon plant-plant interactions alone, we might expect fungal endophytes to alter the speed and outcome of succession. An observation consistent with this view is that endophyte frequencies tend to increase with population and community age IDiehl, 1950; Bradshaw, 1959; Clay, 1986, 1991; Latch et al., 1987; Lewis and Clements, 19861, suggesting that endophyte-harboring plants may be more competitive and thus persist longer than noninfected individuals or species. We emphasize caution here, however, for several reasons. First, the evidence that endophytes are not costly to the plant has only been examined in a few grass species, and under limited environmental conditions. Second, endophytic interactions with plants generally range from pathogenic to mutualistic, and the direction and magnitude of this interaction may vary in time and space. Third, the increased frequency of endophyte infected plants in more mature populations may simply be a function of time-accumulated infections, or a result of life history traits of plants in older communities. Plants in older communities tend to be longer-lived and more architecturally complex, thus presenting more temporal and spatial opportunities for fungal infection. Therefore, it is premature to suggest that endophyte-infected species are competitively superior under all conditions. More recently, the effects of herbivores and plant pathogens and their interactions with each other have been incorporated into ideas of plant succession [Bowers and Sacchi, 1991; Walker and Chapin, 19871. Bowers and Sacchi [ 199I], for example, showed that mammalian herbivores kept red clover populations below densities where a rust-forming pathogen became epidemic. Thus, herbivores via their interactions with a fungal pathogen positively affected the presence and abundance of red clover. We also could envision endophytic microorganisms mediating herbivore- and plant-plant interactions in succession. For example, if endophytes do confer a competitive advantage either directly in plant-plant competition [Hill et al., 1991; Kelrick et al., 1990; Marks and Clay, 1990; Marks et al., 19911 or indirectly by deterring herbivores, then they could affect the direction of plant succession in many communities. Tests of this hypothesis would require the difficult, but not impossible, task of monitoring succession in plant communities where combinations of endophyte-infected and endophyte-free species interact with their herbivores over time under controlled abiotic conditions. Perhaps simple, few-species systems where succession occurs rapidly, endophytes and nutrient levels can be controlled, and plant fitness can be measured are the best systems for such tests. Seed-borne fungi could also have a role in differential plant dispersal and hence successional change [McCaffrey et al., 1991; Wolock and Clay, 19911. We have conducted pilot studies (with D. Arnott and T. Knoch) to examine the role endophyte infection may have in disper-

204

H W O N AND FAETH

sal and predation of tall fescue (Festuca arundinacea) seeds by desert seed-harvesting ants (Pogonomyrmex rugosus and P. occidentalis). These ants remove noninfected seeds nearly twice as often as infected seeds from feeding stations left at their nests (Knoch, Arnott, and Hammon, Faeth unpublished results). Rissing [19861 has shown that P. rugosus influences dispersion of fescue species (F. octoflora), and that fescue plants are found growing more often in ant refuse piles than randomly chosen plots. If endophyte-infected seeds are less acceptable to ants, they might also be discarded more often in refuse piles. Similarly, avian seed predators can distinguish between infected and noninfected tall fescue seeds. Wolock and Clay [I9911 found that five species of passerines preferred uninfected seeds in choice tests. Endophytes may thus contribute to survival and dispersal of seeds, and hence succession. SUMMARY-MICROS

A N D MACROS: A FUNCTIONAL VIEW

The great diversity, fluctuating abundances, complex life histories, unknown taxonomies, and small size of microorganisms that inhabit plant surfaces and interior tissues have inhibited most ecologists from including them into theory and empirical tests of plant-herbivore community interactions. Considering the plant as the frontispiece of ecological interactions and evolutionary change may help to simplify potentially important interactions involving species from widely disparate taxonomic groups. For example, from the plant perspective, loss of tissue due to herbivory results in the same net effect [sensu Jones, 19911 in terms of fitness, whether the agent is a micro- or macroorganism. Indeed, many plant responses to herbivory are apparently nonspecific, and perhaps result from selective pressures from functionally equivalent micro- (e.g. fungal pathogens) and macroparasites (e.g., insect herbivores). Marquis and Alexander [ 19921 advocate considering plant enemies collectively in order to understand plant responses to damage. This functional approach need not be limited to parasitism. Endophytic fungi that prevent flowering [Clay, 19901 may be functional equivalents to grazing herbivores that remove flowering parts [e.g., Paige and Whitham, 19871, while certain fungi and insects both act as seed predators. We might consider ants that protect plants from herbivory [e.g., Janzen, 19661 functional equivalents of endophytic fungi that deter herbivory. From this standpoint, we would also expect interactions (i.e., interspecific competition) within and among these groups, although they are taxonomically unrelated. Indeed, Hochberg and Lawton [1990] propose that competition among kingdoms, such as insect pathogens and parasitoids, may be prevalent and important in the evolution of species’ traits and life histories. The same is likely true of microscopic and macroscopic parasites,

predators, competitors, and mutualists. A functional approach centered around the resource, the plant, focuses more on the interaction per se and its impact on the ecology and evolution of plant-herbivore communities rather than the impact of any particular taxonomic group. It also begins to answer our primary question whether microorganisms are truly important in the ecology and evolution of plant-herbivore communities. To the chagrin of most ecologists who have ignored this component of communities, we feel the answer is, in most cases, that they do. ACKNOWLEDGMENTS

We thank Liz Bernays, Tom Bultman, George Carroll, Keith Clay, and Michael Kelrick for critical comments. Tall fescue seed was generously provided by Malcolm R. Siegel. This work was supported in part by NSF Dissertation Improvement Grant BSR-9112037 to KEH and BSR-9107296 to SHF. REFERENCES Aide TM (1988): Herbivory as a selective agent on the timing of leaf production in a tropical understory community. Nature 336:574575.

Andrews JH, Minano SS. eds. (1991): “Microbial Ecology of Leaves.” New York: Springer-Verlag. Arachevaleta M. Bacon CW, Hoveland CS. Radcliffe DE (1989): Effect of tall fescue endophyte on plant response to environmental stress. Agron J 81243-90. Auerbach MJ, Simberloff D (1989): Oviposition site preference and larval mortality in a leaf-mining moth. Ecol Entomol 14:131-140. Bacon CW, Lyons PC, Porter JK, Robbins J D (1986): Ergot toxicity from endophyte-infected grasses: A review. Agron J 78: 106- I 16. Barbosa P (1988): Some thoughts on “the evolution of host range.” Ecology 69:912-915. Berenbaum MR (1988): Allelochemicals in insect-microbe-plant interactions: Agents provocateurs in the coevolutionary arms race. In Barbosa P, Letourneau DK (eds): “Novel Aspects of Insect-Plant Interactions.” New York: Wiley, pp 97-124. Bergelson JM, Lawton JH (1988): Does foliar damage influence predation on the insect herbivores of birch? Ecology 69:434-445. Bernays E, Graham M (1988): On the evolution of host specificity in phytophagous arthropods. Ecology 69:886-892. Bills GF, Polishook J D (1991): Microfungi from Curpinus curoliniuna. Can J Bot 69:1477-1482. Blakeman JP, ed. (1981): “Microbial Ecology of the Phylloplane.” London: Academic Press. Blazquez CH (1990): Late blight detection in tomato fields by aerial photography with natural and IR color film. Plant Dis 74589592,

Booth C (1971): The genus Fusurium. Kew, England, Commonwealth Mycological Institute. Bowers MA, Sacchi CF (1991): Fungal mediation of a plant-herbivore interaction in an early successional plant community. Ecology 72: 1032- 1037.

Bradshaw AD (1959): Population differentiation in Agrostis tenius Sibth. 11. The incidence and significance of infection by Epichloe typhinu. New Phytol 58:310-315. Brownlee HE, McEven AR, Hedger J, Scott IM (1990): Anti-fungal effects of cocoa tannin on the witches’ broom pathogen Crinipellis perniciosu. Physiol Mol Plant Pathol 36(1):39-48. Bryant JP, Chapin FS 111, Klein DR (1983): Carbon nutrient balance

FUNGI AND HERBIVORE COMMUNITIES of boreal plants in relation to vertebrate herbivory. Oikos 40:357368. Bultman TL, Faeth SH (1986): Selective oviposition by a leaf-miner in response to temporal variation in abscission. Oecologka 6 9 177120. Bultman TL, White J F (1988): “Pollination” of a fungus by a fly. Oecologia 75:3 17-319. Calhoun LA, Findlay JA, Miller JD, Whitney NJ (1992): Metabolites toxic to spruce budworrn from balsam fir needle endophytes. Mycol Res 96:281-286. Carroll GC (1986): The biology of endophytism in plants with particular reference to woody perennials. In Fokkema NJ, Van den Hueval J (eds): “Microbiology of the Phyllophere. Proceedings of the Fourth International Symposium of the Phylloplane.” New York: Cambridge University Press. Carroll GC (1988): Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology 69:lO-16. Carroll GC (199la): Beyond pest deterrence. Alternate strategies and hidden costs of endophytic mutualisms in vascular plants. In Andrews JH, Minano SS (eds): “Microbial Ecology of Leaves.” New York: Springer-Verlag. Carroll G C (1991b): Fungal associates of woody plants as insect antagonists in leaves and stems. In Barbosa P, Krischik VA, Jones CG (eds): “Microbial Mediation of Plant-Herbivore Interactions.” New York: Wiley, pp 253-271. Chakravorty R, Das BC (1981): Occurrence of sooty mold on oak plants. Current Sci 50:138. Chapin FS 111, Bloom AJ, Field CB, Waring RH (1987): Plant responses to environmental factors. BioScience 37:49-57. Cheplick GP, Clay K (1988): Acquired chemical defenses of grasses: The role of fungal endophytes. Oikos 52:309-318. Cheplick GP, Clay K, Wray S (1989): Interactions betwcen fungal endophyte infection and nutrient limitation in the grasses Lolium perenne and F ~ S ~ U urundinuceu. CCI New Phytol I 1 1:89-97. Clay K (1986): Grass endophytes. In Fokkema NJ, Van den Hueval J (eds): “Microbiology of the Phyllophere. Proceedings of the Fourth International Symposium of the Phylloplane.” New York: Cambridge University Press, pp 188-204. Clay K (1988): Fungal endophytes of grasses: A defensive mutualism between plants and fungi. Ecology 69: 10- 16. Clay K (1989): Clavicipivaceousendophytes of grasses: Their potential as biocontrol agents. Mycol Res 92:l-12. Clay K (1990): Fungal endophytes of grasses. Ann Rev Ecol Syst 21:275-297. Clay K (1991): Fungal endophytes, grasses and herbivores. In Barbosa P, Krischik VA, Jones CG (eds): “Microbial Mediation of PlantHerbivore Interactions.” New York: Wiley, pp 199-226 Claydon N, Grove J F (1984): Fusurium as an insect pathogen. In Moss MO, Smith JK (eds): “British Mycological Society Symposium, vol 7, The Applied Biology of Fusurium. New York: Cambridge University Press. Coley PD (1983): Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol Monogr 53:209-223. Coley PD (1988): Effects of plant growth rate and leaf lifetime on the amount and type of anti-herbivore defense. Oecologia 74531 -536. Coley PD, Bryant JP, Chapin FS Ill (1985): Resource availability and plant anti-herbivore defense. Science 230:895-899. Connell JH, Slayter RO (1977): Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119-1144. Connell JH, Noble, IR,Slayter RO (1987): On the mechanism producing successional change. Oikos 5 0 136-137. Cooke MC (1878): On Chaerophomu. Grevillea 7:24-26. Courtney S (1988): If it’s not coevolution it must be predation? Ecology 69:910-911. Courtney SP. Kibota TT (1990): Mother doesn’t know best: Selection ”

205

of hosts by ovipositing insects. In Bernays EA (ed): “Insect-Plant Interactions.” Boca Raton. Fla.: CRC Press, vol 11. pp 162-188. Denno RF, McClure MS, eds. (1983): “Variable Plants and Herbivores in Natural and Managed Systems.” New York: Academic Press. Denslow JS, Schultz JL. Vitousek PM, Strain BR (1990): Growth responses of tropical shrubs to treefall gap environments. Ecology 71: 165- 176. Dickenson CH, Preece TF, eds. (1976): Microbiology of Aerial Plant Surfaces. London: Academic Press. Diehl WW (1950): Bulansiu and Balansiae in America. Agric Monogr 4, USDA, Washington, D.C. Dobzhansky T (1951): “Genetics and the Origin of Species.” New York: Columbia University Press. Du Merle P (1988): Phenological resistance of oaks to the green leafroller Torfrix viriduno. In Mattson WJ, Levieux J, Bernard-Dagan C (eds): “Mechanisms of Woody Plant Resistance against Insects. Search and Pattern.” New York: Springer Verlag, pp 215-226. Edwards PJ, Wratten SD (1983): Wound induced defenses in plants and their consequences for patterns of insect grazing. Oecologia 59188-93. Ehrlich PR, Raven PH (1964): Butterflies and plants: A study in coevolution. Evolution 18:586-608. Ehrlich PR. Murphy DD (1988): Plant chemistry and host range in insect herbivores. Ecology 69:908-909. Engelbrecht L, Orban U, Heese W (1969): Leaf miner caterpillars and cytokinins in the “green islands” of autumn leaves. Nature 223:319321. Ewald PW (1987): Transition modes and evolution of the parasitismmutualism continuum. Ann NY Acad Sci 503:175-306. Ewald PW (1988): Cultural vectors, virulence, and the emergence of evolutionary epidemiology. Oxford Surv Evol Biol 5:215-245. Ewald PW (1991): Culture, transmission modes, and the evolution of virulence with special reference to cholera. influenza, and AIDS. Hum Nat 2:l-30. Ewald PW, Schubert J (1989): Vertical and vector-borne transmission of insect endocytobionts, and the evolution of benignity. In Schwemmler W, Gassner G (eds): “Insect Endocytobiosis: Morphology, Physiology, Genetics.’’ Boca Raton, Fla.: CRC Press, pp 21-35. Faeth SH (1985a): Host leaf selection by a leaf-mining insect, Srilbosis juvunris: Interactions among three trophic levels. Ecology 66370875. Faeth SH (1985b): Quantitative defense theory and patterns of feeding by oak insects. Oecologia 68:34-40. Faeth SH (1986): Indirect interactions between temporally separated herbivores mediated by the host plant. Ecology 67:479-494. Faeth SH (1987): Community structure and folivorous insect outbreaks: The roles of vertical and horizontal interactions. In Barbosa P, Schultz JC (eds): “Insect Outbreaks.” New York: Academic Press, pp 135-171. Faeth SH (1988): Plant-mediated interactions between seasonal herbivores: enough for evolution or coevolution? In Spencer KC (ed): “Chemical Mediation of Coevolution.” New York: Academic Press, pp 391-414. Faeth SH (1990): Aggregation of a leafminer, Cumerurio sp. nov. (Davis): consequences and causes. J Anim Ecol 59569-586. Faeth SH (1991a): The effect of oak leaf size on abundances, dispersion, and survival of the leafminer, Cumeraria sp nov. (Lepidoptera: Gracillariidae). Environ Entomol 2 0 196-204. Faeth SH (1991b): Inducible responses and interactions among oak folivores. In Raup MJ, Tallamy DW (eds): “Phytochemical Induction by Herbivores.” New York: Academic Press, pp 391-414. Faeth SH (I 992): Interspecific and intraspecific interactions via plant responses to folivory: an experimental test. Ecology 73: 1802- 1813. Faeth SH, Conner EF, Simberloff D (1981): Early leaf abscission: A neglected source of mortality for folivores. Am Nat 117:409-415. Faeth SH, Rooney RF Ill (1992): Variable budbreak and insect foliv-

206

HAMMON AND FAEM

ory of Gambel oak (Quercusgumhelii: Fagaceae). Southwestern Naturalist (in press). Feeny P (1970): Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51: 565-581. Feeny P (1975): Biochemical coevolution between plants and their insect herbivores, Symp Int Congr Syst Evol Biol 1:3-19. Fisher PJ, Anson AE, Petrini 0 (1986): Fungal endophytes in Ulex europueus and Ulex gufii. Trans Br Mycol SOC8 6 153- 156. Fokkema NJ, van den Hueval J, eds (1986): Microbiology of the Phyllophere. Proceedings of the Fourth International Symposium of the Phylloplane. New York: Cambridge University Press. Fowler SV, Lawton JH (1984): Foliage preference of birch herbivores: A field manipulation experiment. Oikos 42:239-248. Fowler SV, MacGarvin M (1986): The effects of leaf damage on the performance of insect herbivores on birch. B e f u hpubescens. J Anim ECOI55:565-573. . Fox L (1988): Diffuse coevolution within complex communities. Ecology 691906-907. Fritz RS, Simms EL. eds. (1992): “Ecology and Evolution of Plant Resistance.” Chicago: University of Chicago Press. Futuyma DJ (1976): Food plant specialization and environmental predictability in Lepidoptera. Am Nat 110285-292. Futuyma DJ. Could F (1979): Associations of plants and insects in a deciduous forest. Ecol Monogr 49:33-50. Gill DE. Mock BA (1985): Ecological and evolutionary dynamics of parasites: The case of Trypunosi~mutliemyciyli in the red spotted newt Ni~tphrhu~mus viridescens. In Rollinson D, Anderson RM (eds): “The Evolution of Host Parasite Interactions.” London: Academic Press. pp. 157-183. Goodman RN. Kiraly 2, Wood KR (1986): The biochemistry and physiology of plant diseases. Columbia, Mo.: University of Missouri Press. Green TR, Ryan CA (1972): Wound induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Scicnce 175~776-777. Gross P. Price PW (1988): Plant influences on parasitism of two Icafminers: A test of enemy-free space. Ecology 69: 1506-15 16. Grove JF, Pople M (1980): The insecticidal activity of beauvericin. a new depsipeptide toxic to Arfemiu sulinu. Tetrahedon Lett 49:42554258. Harborne JB (1983):Toxins of plant-fungal interactions. In Keeler RF, Tu A T (eds): “Handbook of Natural Toxins, Vol. I . Plant and Fungal Toxins.” New York: Marcel Dekker, Inc., pp 743-784. Hawkins BA (1988): Foliar damage, parasitoids, and competition: A test using herbivores of birch. Ecol Entomol I3:301-308. Heinrich B, Collins SL (1983): Caterpillar leaf damage and the game of hide-and-seek with birds. Ecology 64592-602. Hill NS, Stringer WC, Rottinghaus GE, Belesky DP, Parrott WA, Pope DD (1990): Growth, morphological, and chemical component responses of tall fescue to Acremonium coenophiulum. Crop Sci 3 0 156161.

Hill NS, Belesky DP, Stringer WC (1991): Competitiveness of tall fescue as influenced by Acremonium coenophiufum.Crop Sci 3 1: 186190. Hochberg ME, Lawton JL (1990): Competition between kingdoms. Trends Ecol Evol 5:367-371. Holmes RT, Schultz JC, Nothnagle P (1979): Bird predation on forest insects: An enclosure experiment. Science 206:462-463. Horn HS (1976): Succession. In May RM (ed): “Theoretical Ecology: Principles and Applications.” Philadelphia: Saunders, pp 187-204. Hunter MD, Ohgushi T, Price PW, (eds) (1992): “Effects of Resource Distribution on Animal-Plant Interactions,” San Diego: Academic Press. Janzen DH (1966): Coevolution of mutualism between ants and acacias in Central America. Evolution 20:249-275.

Janzen DH (1988): On the broadening of insect-plant research. Ecology 69:905. Jarvis BB, Mokhtari-Rejali N. Schenkel EP, Barros CS, Matzenbacher NI (1991): Trichothecene mycotoxins from Brazilian Bucchoris species. Phytochemistry 30:789-797. Jenny T (1988): Can predation lead to narrow food spccialization in phytophagous insects? Ecology 69:902-904. Johnson MC, Pirone TP, Siege1 MR, Varney DR (1982): Detection of Epichloe fyphinu in tall fescue by means of enzyme-linked immunosorbent assay. Phytopathology 72547-650. Jones CG (1991): Interactions among insects, plants. and microorganisms: A net effects perspective on insect performance. In Barbosa P. Krischik VA, Jones CG (eds): “Microbial Mediation of Plant-Herbivore Interactions.” New York: John Wiley and Sons, Inc., pp 7-35. Karban R. Ricklefs RE (1984): Leaf traits and species richness of lepidopteran larvae on deciduous trees in southern Ontario. Oikos 43: 165- 170. Karban R, Myers J (1989): Induced plant response to herbivory. Ann Rev Ecol Syst 20:331-348. Karban R. Adamchak R, Schnathorst WC (1987): Induced resistance and interspecific competition between spider mites and a vascular wilt fungus. Science 235678-680. Kelrick MI, Kasper NA, Bultman TL, Taylor S (1990): Direct inleractions between infected and uninfected individuals of Fesfucu urunclinucm: Differential allocation to shoot and root biomass. In Quisenberry SS, Joost RE (eds): “Proceedings of the International Symposium on AcremoniumlGrass Interactions.’’ Baton Rouge, LA, Louisiana Agricultural Experiment Station. pp 2 1-29. Kimmons CA, Gwinn KD, Bernard EC (1990): Nematode reproduction on endophyte-infected and endophyte-free tall fescue. Plant Dis 74:757-761. Kiraly Z, El Hammady M. Pozsar BI (1967): Increased cytokinin activity in rust-infected bean and broad bean leaves. Phytopathology 57:93-94. Krischik VA (1991): Specific or generalized plant defense: reciprocal interactions between herbivores and pathogens. In Barbosa P. Krischik VA, Jones CG (eds): “Microbial Mediation of Plant-Herbivore Interactions.” New York: John Wiley and Sons, Inc., pp 309-340. Krischik VA, Barbosa P. Reichelderfer C F (1988): Three trophic level interactions: Allelochemicals, Munducu sextu and Eucillus thuringiensis var. kurstaki Berliner. Environ Entornol 17:476-482. Larsson SA (1989): Stressful times for the plant stress-insect performance hypothesis. Oikos 56:277-283. Larsson SA, Wiren L, Lundgren. Ericsson T (1986): Etfects of light and nutrient stress on leaf phenolic chemistry in Sulix dusycludos and susceptibility to Gullerucellu lineolu (Coleoptera). Oikos 47:205-2 10. Latch GCM, Christensen MJ, Gaynor DL (1985): Aphid detection of endophyte infection in tall fescue. NZ J Agric Res 28: 129- 132. Latch GCM, Potter LR, Tyler BF (1987): Incidence of endophytes in seeds from collections of Lolium and Festucu species. Ann Appl Biol 1 1 1~59-64. Lawton JH (1986): Food shortage in the midst of plenty? The case for birch-feeding insects. Proc, 3rd European Cong Entomol; pp 219228. Letourneau DK (1988): Microorganisms as mediators of intertrophic and intratrophic interactions. In Barbosa P, Letourneau DK (eds): “Novel Aspects of Insect-Plant Interactions.” New York: John Wiley and Sons, Inc., pp 91-95. Lewis GC, Clements RD (1986): A survey of ryegrass endophyte (Acremonium loliue) in the United Kingdom and its apparent ineffectuality as a seedling pest. J Agric Sci 107:633-638. Lieberman D, Lieberman M (1984): The causes and consequences of synchronous flushing in a dry tropical forest. Biotropica 16:193-201. Marks S, Clay K (1990): Effects of carbon dioxide enrichment, nutrient addition, and fungal endophyte infection on the growth of two grasses. Oecologia. 84:207-214.

NNGl AND HERBIVORE COMMUNITIES

Marks S, Clay K, Cheplick GP (1991): Effects of fungal endophytes on interspecific and intraspecific competition in the grasses Fesruca arundinacea and Lolium perenne. J. Appl. Ecol. 28:194-204. Marquis RJ, Alexander HM (1992): Evolution of resistance and virulence in plant-herbivore and plant-pathogen interactions. Trends EcoI. EvoI. 7:126-129. Massad E (1987): Transmission rates and the evolution of pathogenicity. Evolution 41:1127-1130. Mattson WJ, Haack RA (1987): The role of drought stress in provoking outbreaks of phytophagous insects. In Barbosa P, Schultz JC, eds. insect Outbreaks. San Diego, Academic Press, pp 365407. McCaErey AM, Kelrick MI, Ballmann A (1991): Seed selectivity of a native rodent granivore for endophytically infected and uninfected seeds of tall fescue. Abstract. Annual Meeting of the American Society of Mammalogists, Manhattan Kansas. McIntyre JL, Dodds JA, Hare J D (1981): Effects of localized infections of Nicoriuna tubacum by tobacco mosaic virus on systemic resistance against diverse pathogens and an insect. Phytopathology 7 l:297301. McKey DB, Wateran PG, Mbi CN. Gartlan JS, Strusaker (1978): Phenolic content of vegetation in two African rain forests: ecological implications. Science 202:61-64. Miller JD, Strongman D, Whitney NJ (1985): Observations on fungi associated with spruce budworm infested balsam fir needles. Can J For Res 152396-901. Mitter C, Farrell 8, Futuyma DJ (1991): Phylogeneticstudies of insectplant interactions: insights into thc genesis of diversity. Trends Ecol Evol 6290-293. Mole S , Waterman PG (1988): Light induced variation in phenolic lcvcls in foliage of rain forest plants. 11. Potcntial significance to herbivores. J Chem Ecol 14:23-34. O’Day MH. Bailey WC, Niblack TC (1990): Phytonematodecommunities in tall fescue varieties with varying levels of cndophyte (Acremonium coenopliialum) infection. In Quisenberry S S , Joost RE (eds): “Proceedings of the International Symposium on AcremoniumiGrass Interactions.“ Baton Rouge, LA, Louisiana Agricultural Experiment Station, pp 170-172. Ohgushi T (1992): Resource limitation on insect herbivore populations. In Hunter MD, Ohgushi T, Price PW (eds): “Effects of Resource Distribution on Animal-Plant Interactions.” San Diego: Academic Press, pp 200-241. Paige K, Whitham TG (1987): Overcompensation in response to mammalian herbivory: The advantage of being eaten. Am Nat, 129:407416. Pederson JF, Rodriguez-Kabana 9, Shelby RA (1988): Ryegrass cultivars and endophyte in tall fescue affect nematodes in grass and succeeding soybean. Agron J 80911-814. Pegg G F (1981): The involvement of growth regulators in the diseased plant. In Ayres PG (ed): “Effects of Disease on the Physiology of the Growing Plant.” London: Cambridge University Press. Pinkerton BW, Rice JS, Undersander DJ (1990): Germination in Festuca arundinacea as affected by the endophyte Acremonium roenophialum. In Quisenberry SS, Joost RE (eds): “Proceedings of the International Symposium on AcremoniumlGrass Interactions.” Baton Rouge, LA, Louisiana Agricultural Experiment Station, pp 176-1 80. Price PW (1983): Hypotheses on the organization and evolution of herbivore communities. In Denno RF, McClure MS (eds): “Variable Plants and Herbivores in Natural and Managed Systems.” New York: Academic Press. pp 559-596. Price PW (1992): Plant resources as the mechanistic basis for insect herbivore population dynamics. In Hunter MD, Ohgushi T, Price PW (eds): “Effects of Resource Distribution on Animal-Plant Interactions.” San Diego: Academic Press, pp 139- 174. Price PW, Westoby M, Rice 9, Atsatt PR, Fritz RS, Thompson JN,

207

Mobley K (1986): Parasite mediations in ecological interactions. Ann Rev Ecol Syst 17:487-505. Puttick GM (1986): Utilization of evergreen and deciduous oaks by the California oak moth, f‘hrygunidia cali/ornicu. Oecologia 68:589-594. Raupp MJ, Denno RF (1983): Leaf age as predictor of herbivore distribution and abundance. In Denno RF, McClure MS (eds): “Variable Plants and Herbivores in Natural and Managed Systems.’’ New York: Academic Press, pp 91 -124. Rausher MD (1988): Is coevolution dead? Ecology 69398-901. Read JC, Camp BJ (1986): The effect of fungal endophyte Acremonium coenophialum in tall fescue on animal performance, toxicity and stand maintenance. Agron J 78:848-50. Rhoades DF (1979): Evolution of plant chemical defense against herbivores. In Rosenthal GA and Janzen DH (eds): “Herbivores: Their Interaction with Secondary Plant Metabolites.” London: Academic Press, pp 3-54. Rhoades DF, Cates RG (1976): Toward a general theory of plant antiherbivore chemistry. Recent Adv Phytochem 10:168-213. Richardson MD, Bacon CW, Hoveland CS (1990): The effect of endophyte removal on gas exchange in tall fescue. In Quisenberry SS. Joost RE (eds): Proceedings of the International Symposium on AcremuniumlGrass Interactions.” Baton Rouge, LA, Louisiana Agricultural Experiment Station, pp 189- 193. Rissing SW (1986): Indirect effects of granivory by harvester ants: Plant species composition and reproductive increase near ant nests. Oecologia 68:231-234. Rockwood LL (1974): Seasonal changes in the susceptibility of Crescuntia alufa leaves to the flea beetle, 0edion.vchus sp. Ecology 55: 142148. Russell GB, Sutherland ORW, Hutchins RFN, Christmas PE (1978): Vcstitol: a phytoalexin with insect fceding deterrcnt activity. J Chem ECOI4571 -579. Savopoulou-Soultana M. Tzanakakis ME (1988): Development of Lohesia horranu (Lepidoptcra: Tortricidae) on grapes and apples infected with the fungus Botryfis cincru. Environ Entomol 17: 1-6. Schultz JC (1983): Habitat selection and foraging tactics ofcaterpillars in heterogeneous trees. In Denno RF, McClurc MS (eds): “Variable Plants and Herbivores in Natural and Managed Systems.” New York: Academic Press. pp 61-90. Schultz JC (1988): Many factors influence the evolution of insects diets, but plant chemistry is central. Ecology 69:896-897. Scriber JM, Lederhouse RC (1992): The thermal environment as a resource dictating geographic patterns of feeding specialization of insect herbivores. In Hunter MD, Ohgushi T, Price PW (eds): “Effects of Resource Distribution on Animal-Plant Interactions.” San Diego: Academic Press, pp. 430-466. Scriber JM, Slansky F Jr (1981): The nutritional ecology of immature insects. Ann Rev Entomol 26: 183-21 1 . Seaman FC (1 984): The effects of tannic acid and other phenolics on the growth of the fungus cultivated by the leafcutting ant, Myrmicocrypta buenzlii. Biochem Syst Ecol 12155-158. Shenvood-Pike M, Stone JK, Carroll GC ( 1 986): Rhobdoclineparkeri, a ubiquitous foliar endophyte of Douglas-fir. Can J Bot 64:1849-

1855. Shure DJ, Wilson LA (1992): Patch size effects on plant phenolics in successional openings of the Southern Appalachians. Ecology (in press). Simberloff D, Stiling P (1988): Larval dispersion and survivorship in a leaf-mining moth. Ecology 69:1647-1657. Southwood TRE (1973): The insect/plant relationship-an evolutionary perspective. Symp R Entomol SOCLondon 6:3-30. Stamp NE (1992): Theory of plant-insect herbivore interactions on the inevitable brink of re-synthesis. Bull Ecol SOCAm 73:28-34. Strong DR J r (1988): Endophytic mutualism and plant protection from herbivores. Ecology 69:I . Strongman DB, Strunz GM, Giguere P, Yu C-M, Calhoun L (1988):

208

HAMMON AND FAETH

Enniatins from Fusurium uvenuccum isobated from balsam fir foliage and their toxicity to spruce budworm larvae, Choristoneuru fum$erunu (Clem.) (Lepidoptera: Tortricidae). J Chem Ecol 14753764. Strongman DB. Strunz GM, Giguere P, Yu C-M (1990): Trichothecene mycotoxins produced by Fusarium sporotrichoides DAOM 197255 and their effects on spruce budworm, Chorisroneuru fumiferunu. J Chem Ecol 16:1 305- 1609. Sun S,Clarke BB, Funk JR (1990): Effect of fertilizer and fungicide applications on choke expression and endophyte transmission in Chewings Fescue. In Quisenberry SS, Joost RE (eds): "Proceedings of the International Symposium on AcremoniumlGrass Interactions." Baton Rouge, LA, Louisiana Agricultural Experiment Station, pp 62-66. Sutherland BL, Hoglund JH (1990): Effect of ryegrass containing the endophyte Acremonium lolii on associated white clover. In Quisenberry SS. Joost RE (eds): "Proceedings of the International Symposium on AcremoniumlGrass Interactions." Baton Rouge, LA, Louisiana Agricultural Experiment Station, pp 67-71. Sutherland ORW, Russell GB, Biggs DR, Lane GA (1980): Insect feeding deterrent activity of phytoalexin isoflavonoids. Biochem Syst ECOI8~73-75. Szentesi A, Jermy T (1990): The role of experience in host plant choice by phytophagous insects. In Bernays EA (ed): Insect-plant Interactions." Boca Raton, Fh.: CRC Press, vol 111, pp 39-74. Taper ML, Case TJ (1987): Interactions between oak tannins and parasite community structure: Unexpected benefits of tannins to cynipid gall-wasps. Oecologia 7 1:254-26 I . Taper ML, Zimmerman EM, Case TJ (1986): Sources of mortality for a cynipid gall-wasp (Dryocosmus dubiosis (Hymenoptera: Cynipidae)): The importance of the tannin/fungus interaction. Oecologia 68:437-445. Thompson JN (1982): "Interaction and Coevolution." New York: John Wiley and Sons. Thompson J N (1988): Coevolution and alternative hypotheses on insect/plant interactions. Ecology 69393-895.

Toler R (1981): Use of aerial color infrared photography to evaluate crop disease. Plant Dis 65:24-31. Turlings TCJ. Tumlinson IH, Lewis WJ (1990): Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250: 125 1- 1253. Walker LR, Chapin FS 111 (1987): Interactions among processes controlling successional change. Oikos 50: 13 I - 135. Waring RH, Pitman GB (1985): Modifying lodgepole pine stands to change susceptibility to mountain pine beetle attack. Ecology 66: 889-897. West C (1985): Factors underlying the late seasonal appearance of the lepidopterous leaf-mining guild on oak. Ecol Entomol 10:111- 120. West CP, Izekor E, Oosterhuis DM, Robbins RT (1988): The effect of Acremonium comophiulum on the growth and nematode infestation of tall fescue. Plant and Soil I12:3-6. White TCR (1974): A hypothesis to explain outbreaks of looper caterpillars, with special reference to populations of Selidosema suuvis in a plantation of Pinus radiutu in New Zealand. Oecologia 22:119134. White TCR (1984):The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia 63:90- 105. Whitman DW (1988): AIlelochemical interactions among plants, herbivores, and their predators. In Barbosa P. Letourneau DK (eds): "Novel Aspects of Insect-Plant Interactions." New York: John Wiley and Sons, pp I 1-64. Wicklow DT, Carroll GC, eds (1981): "The Fungal Community, Its Organization and Role in the Ecosystem. Mycology Series V. 2." New York: Marcel Dekker, Inc. Williams GC, Nesse RM (1991): The dawn of Darwinian medicine. Quart Rev Biol 66:l-22. Wolock MC. Clay K (1991): Avian seed preference and weight loss experiments: the eKcct of fungal endophyte infected tall fescue seeds. Oecologia 88:296-302. Zuckcr WV (1983): Tannins: Does structure determine function? An ecological perspective. Am Nat 121:335-365.