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Developing a Theory of Plant-Insect Herbivore Interactions: Are We There Yet? Author(s): Nancy E. Stamp Source: Bulletin of the Ecological Society of America, Vol. 77, No. 1 (Jan., 1996), pp. 51-61 Published by: Ecological Society of America Stable URL: http://www.jstor.org/stable/20168007 . Accessed: 26/12/2013 09:21 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. . Ecological Society of America is collaborating with JSTOR to digitize, preserve and extend access to Bulletin of the Ecological Society of America. http://www.jstor.org This content downloaded from 128.226.37.5 on Thu, 26 Dec 2013 09:21:06 AM All use subject to JSTOR Terms and Conditions lution. Macmillan, New York, USA. Tansley, A. G. 1947. New York, tity. Pages Frederic Ed Jour 1874-1945. ward Clements, nal of Ecology 34:194-196. Tobey, R. 1981. Saving the prairies: the life cycle of the founding plant ecol school of American of ogy, 1895-1955. University California Press, Berkeley, Cali fornia,USA. Shantz, H. 1945. Van Leer, D. 1991. Society Frederic Edward I was to talk Recently, asked about how the field of ecology has benefitted from study of plant-insect To get a herbivore interactions. sense of what ecologists think this I looked has contributed, discipline at seven ecology texts published from 1990 through 1994. Ecology texts are revised about every 5 years for an intensely competitive market, so we might expect that they would reflect what ecologists view as the important contributions of plant-her bivore interactions. On average 2.3% of an ecology text deals with plant herbivore interactions, but that is 9 10 pages less than for competition (3.6%) or animal predation (3.8%). Only three of the seven texts devoted a chapter to the topic of plant-herbi vore interactions. Likewise, mutual ism (e.g., pollination, by animals, seed dispersal ants protecting plants, re microbial-plant associations) ceives much less attention than com petition and predation. A dominant focus on competition and predation limits our understanding of the di of factors versity that shape and maintain communities. and iden in E. Elliott, history of the editor. Columbia American novel. Columbia versity Press, New York, Uni New York, USA. sociology, Ward, L. 1968. Dynamic or applied social science. Two re The 1883 edition volumes. Wilson, of natural cal Review communities. 28:1-240. reflect: vegetation Journal of Vegeta tionScience 2:289-290. D. 1985. Nature's Worster, economy: a history of ecological ideas. Second edition. Cambridge University Press, Cambridge, UK. G. Barbour Michael Department of Environmental Horticulture University of California CA 95616 Davis, Poor coverage of plant-herbivore may 1991. Does exist? Botani Why less coverage? interactions J. B. science Press, printed by Greenwood New York, New York, USA. Whittaker, R. H. 1962. Classification Clements (1874-1945). Ecology 26:317-319. Developing a Theory of Plant-insect Herbi vore Interactions: Are We There Yet? 485-509 (1) age of the subdiscipline, (2) complexity of (3) paucity of math and (4) the large models, ogy of plants, especially production of secondary metabolites, must be taken into account because this often determines food quality for the her the interactions, bivore. ematical animal, For an animal eating another food quality is largely de and ever-increasingvolume of litera fined by energy gained (Stephens ture in this field. and Krebs 1986). For herbivores, food quality is more complicated and First, research on plant-insect herbivore interactions exploded in the late 1960s following publication and Raven's (1964) corre lation of use by related butterfly spe of Ehrlich cies of taxonomically and/or chemi cally related host plants. The subdis cipline of plant-herbivore interac tions, then, is about 35 years old, whereas study of competition and of predation have been active fields of research for about 60 years. Our ideas about the process and conse and preda quences of competition tion have been fairly well developed and articulated in reviews and books for as long as 15-20 years, so it is to authors of ecology texts clearer what to present about competition and predation. Second, plant-herbivore interac tionsmay be poorly covered because of the complexity of factors influ encing these interactions, in particu lar plant chemistry, the interplay of multiple trophic levels, and the inte gration of ecological and evolution ary time. For example, the physiol includes the amounts of nitrogen, water, allelochemicals, and sub stances that determine digestibility. toughness and All of these factors can variable in plant material, be highly while the availability of energy is both relatively high and less vari able. As a consequence of such com plexities, the field of plant-insect herbivore interactionshas given rise to subdisciplines, such as the nutri tional ecology of plant-insect herbi vore systems (Scriber and Slansky 1981, Coley et al. 1985), the phylogenetics of plant-insect herbi vore systems (Farrell et al. 1992), the chemical ecology of plant-insect herbivore-parasitoid systems (Dicke et al. 1990, Vet and Dicke 1992), and tritrophic level interactions (Price et al. Gould 1992). 1980, The Johnson growth of and these subdisciplines has contributed to a greater understandingof themecha nisms underlying patterns of plant insect herbivore interactions, but without a synthesis January This content downloaded from 128.226.37.5 on Thu, 26 Dec 2013 09:21:06 AM All use subject to JSTOR Terms and Conditions 1996 among these it is 51 difficult for authors of textbooks to see how the contributions of these fields link together. Third, developing predictive models of the effects of interactions between trophic levels on population dynamics has long been a goal in ing of the field. Undoubtedly, au thors of ecology texts rely on re views to help them process informa tion and ideas. Broadly focused re concepts. The same was true of the on animal predation. But chapters sections on plant-herbivore interac tions were much less uniform in the principles, ideas, and terms empha sized, and only three books provided views providing syn the necessary thesis cannot keep pace with the rapid expansion of this field. For in models illustrating population dy stance, in the study of the effects of resource availability on plants and, namics in turn, on insects, there has been a proliferation of hypotheses, all of often particularly cals, which However, ecology. in research plant-herbivore interactions has fo cused on the above complexities, the role of allelochemi rather than on modeling plant herbivore population dynamics. Al models though mathematical of the dynamics of interacting populations have been applied to plant-herbivore interactions (May 1973, Noy-Meir 1976, Crawley 1975, Caughley 1983), been may these applications especially be due have satisfactory. to several factors: herbivores kill plants, to predators rarely contrast in not This their (1) host of animal prey, (2) the perceived asym in the interaction (e.g., com to has often been shown petition limit plants, while fewer studies metry have demonstrated strongly limiting of natural on effects herbivory plants do plants, and conversely, have a strong effect on herbivores, 1983), (3) scarcity of data Crawley on plant (e.g., impact of herbivores growth rate, rates of consumption, in the herbivore population density) are currently viable to some degree, e.g., carbon:nutrient balance (Bryant et al. 1983), hypothesis growth-differentiation balance hy pothesis (Loomis 1932, 1953, Lorio 1986, Herms and Mattson 1992), plant stress hypothesis (White 1974, 1984), plant vigor hypothesis (Price et al. 1990, Price fense hypothesis Feeny 1976, 1991), optimal de (McKey 1974, Rhoades and Cates 1976, Rhoades 1979), and resource of competition predation also make such assump systems are even tions, and animal more likely to violate ing and animal assumptions the simplify than plants (Caughley 1976), these versions of have been "predator-prey" models around longer and generally are ac cepted as useful constructs in ecol ogy texts. Fourth, the literature of plant herbivore interactions is increasing exponentially, which makes it diffi cult to assess our currentunderstand 52 illustrate clearly the teractions. The examples came as "gee whiz" types or isolated case studies. For instance, the monarch butterfly story was of ten presented. But usually the biol across more ogy of the particular took system precedence over making clear the generality of the example. The same was true generally for mutualism ex amples in these texts. Furthermore, only one of these texts gave a historical perspective of hypothesis development in the field rule some out, consolidate some or all these hypotheses, or construct some kind of hierarchy, is unclear. As difficult as itmay be to develop such of the field of plant-herbi syntheses, vore interactions needs broadly fo to develop cused syntheses into a presentation ofplant-herbivore interactions models did not key concepts of plant-herbivore in of plant-insect herbivore interac tions. This is unfortunate because de hypothesis (Coley et al. 1987). Yet a synthesis of how these hypotheses to relate one another, where we stand with each of these, and whether we can met Although in 1985, Coley more mature field. Doing so would ensure that the general principles de rived from the study of plant-herbi vore interactions will be incorpo rated into materials we present in our ecology courses. 1976). and herbivores availability form amenable for testing the mod els (Begon and Mortimer 1981), and that allow for the (4) lack of models of herbivores interactions complex with their food supply (e.g., induc Further tion of chemical defense). have restrictive more, most models to be that are unlikely assumptions (Caughley of plants teracting. Examples, as presented, Some additional These reasons observations about for the poor cover interactions age of plant-herbivore are suggested by the ways that com petition, predation, and plant-herbi are presented in vore interactions different texts. For all of the text books, chapters on competitionwere fairly uniform, emphasizing the same principles and ideas and using the same terms. Each text provided models of the effects of competition on population dynamics, and ex amples clearly illustrated the key velopment and testing of hypotheses in this field is a particularly nice ex ample of the scientific process, which is all too elusive to the aver age student. The study of plant-insect herbi vore interactions has given much more to our current understanding of basic ecological issues than is appar ent in these texts. If nothing else, it explains much about the ecology of 50% of the macroscopic species on earth. The fault for an inadequate pre sentation of our current understand herbivore interac ing of plant-insect in tions lies with those of us working this field. We message have not given the basic about a clear ideas emerging in our discipline. We often in detail. In drown other ecologists to pi doing so, we tempt authors geonhole our field as a host-parasite or predator-prey and interaction, to ecol thus important contributions ogy, particularly community ecol ogy, are lost. Themessages of plant-insect herbivore interactions Here I listwhat I perceive as 12 basic generalizations of plant-insect SocietyofAmerica Bulletinof theEcological This content downloaded from 128.226.37.5 on Thu, 26 Dec 2013 09:21:06 AM All use subject to JSTOR Terms and Conditions interactions important to I the field of ecology and evolution. have organized these into six catego ries, which show the scope of the generalizations, emphasizing both the role of chemical and ecology or tritrophic processes, community herbivore level interactions (Table 1). With I provide an ex each generalization, ample or some other justification. This is not an exhaustive equate places or even ad review of the field. Rather it these generalities in broader ecological Table The plant's support various parts of this statement. are characterized ticular are found the Plant (e.g., in the plant Apocyanaceae, Asclepi and Scrophulariaceae) adaceae, and Janzen 1979, Har (Rosenthal borne 1982). Plant genotypes vary in their resistance to insect herbivores. netically interac array of defenses. can have a cost. The herbivore's ability to exploit a plant 3. Herbivores deal with poorer 4. Herbivores have a dynamic food quality than predators. array of countermeasures. plays a large role in feeding 5. Plant diversity specialization. effects: herbivore vs. herbivore, among herbivores vs. plant plant depends on type of feeding and life history traits. 7. Indirect (resource-mediatedand enemy-mediated) interactionsare common between herbivores. families For example, herbivore 8. Herbivory lessens a plant's distribution and abundance Bottom-up: effects of plants ability to compete alters and, consequently, of plants. by par allelochemicals cardenolides of plant-insect itself 1. Plants have a dynamic 6. Competition environmentalconditions. families to defend ability 2. Defenses Lateral 1. Plant species have a dynamic array of defenses, reflecting phylog eny, genotype, phenology and studies of the 12 messages contexts. and pedagogical Numerous 1. Short version tions. on the herbivore's 9. Plant traits can affect performance 10. Parasitoids Top-down: are more often specialized effects of the herbivore's enemies can limit herbivores 11. Enemies enemies of the enemies of herbivores. than predators. on plants and improve plant productivity. cowpeas have three ge to resist a ways different on eating pods specializing on seeds: inhibition and ovipositing of adult feeding, inhibition of ovipo sition, and extension of larval devel beetle (Cuthbert et al. 1974). The genotypes vary in their ex pression of each of these resistance traits. Environmental conditions al ter the genotypic expression of host resistance to herbivores plant (Kennedy and Barbour 1992). For in stance, high levels of fertilizer elimi nated resistance of tomato to three insect herbivore species (Barbour et al. 1991). Jones (1983) gives an ex Community structure 12.Much biodiversity due to plant-herbivore interactions. opment cowpea time. For instance, damage by herbi vores can induce greater chemical defense by plants (Tallamy and Raupp 1991). Such defenses can de ter feeding by insect herbivores, kill them, or slow their growth (Kennedy problem and Barbour 1992, Bernays and Chapman 1994), which makes them to other sources of mor vulnerable bred for palatability. Furthermore, ef illustrating phenological fects on potential defenses. The con centrations of various phytochemi tality. For ecology students,understand cals in bracken fern that can affect insect performance fluctuated over derstanding the growing season. Some increased, others decreased. Thus, a dynamic array of phytochemicals linked to host-plant resistancewas exhibited. All plant defenses are dynamic in evolutionary time; chemical de fenses are also dynamic in ecological ducers, ample ing this first point community is critical to un the role of plants structure. Plants, the energy provide community in (e.g., not for etc.). People probably view plants as for the most part palatable because the grocery store carries only plant that have been products selected or most people do not make the connec tion that nicotine, caffeine, and co caine are natural plant products that help a plant defend vores itself from herbi and pathogens, the concentrations let alone that vary in some for example, with may the pro systematic for the phylogeny, genotype, phenology, and environmental conditions. Al to operate, fend that energy for animals themselves, cattle, gypsy moths, but they de and their other re way, though five of the ecology texts con sources. This now seems obvious to ecologists, but to most people this is veyed news because sented this fundamentalpoint. from their perspective eating plants does not seem to pose a some part of this message, none of the seven texts clearly pre January This content downloaded from 128.226.37.5 on Thu, 26 Dec 2013 09:21:06 AM All use subject to JSTOR Terms and Conditions 1996 53 2. Plant defenses can have a cost that affects growth and other correlates offitness. An experimentby Baldwin, Sims, and Kean (1990) on the effect of leaf damage on wild such costs. tobacco Seed production in plants duced illustrates was that increased re alka loid production in response to dam in damaged age, but not which in plants alkaloid production was blocked with there was auxin. Thus, a trade-off between alkaloid produc tion and seed production. Cost, the trade-off between de fense and correlates of fitness such as growth and seed set, is most com monly demonstrated at vulnerable or when stages For resources a variety of are poor. reasons, it has proven extremely difficult to esti mate these costs (Gulmon and Mooney in 1986). For example, in a defensive trait (such as an 3.Although food quantity is espe cially criticalfor secondary consum ers (carnivores/predators),it is food quality (toughness,digestibility, spines, toxins,and nutrientsof plants) that is of major importance for most insectherbivores. Nitrogen, a limiting nutrient, is content (Scriber course, and in plant 1981). Of eating plant material is fur ther complicated chemicals material Slansky present, by the allelo which can con straingrowth (Slansky 1992). Numerous studies and reviews provide evidence for the message nogenetic genotypes of fall canker in a (Mole eral, resistance plant because tively rapid Earth is now of a are the founda plants With climate the rela that change experiencing, plants and be increasingly stressed, to her thus the cost of resistance may bivory may increase sumes (Ayres the general Increasingly, that we 1993). public can (or soon will able to) genetically engineer as be our way out of trouble with insect pests. But plants to resist engineered insect pests may be less fit than the original plant stock because ally mean an added added genes usu cost of synthe sizing plant chemicals (Tiedje et al. 1989). Thus, an understandingof the potential cost of plant resistance to herbivory is critical to determining how tomaintain (or increase) pro ductivity in natural and managed ecosystems. 54 physiological mechanisms. Defensive countermeasures em ployed by insect herbivores include clipping trichomes (hairlike growths on plants that may chemicals), cutting contain defensive leaf veins to pre vent transport of defensive chemi cals, aversion learning, inducing detoxification systems, altering gut Ph, maintaining gut redox conditions and gut surfactants (detergents that herbivores for the economy tion of communities. have a dynamic The to herbivory Ecology studentsneed to develop an appreciation 4. Insect herbivores transfer, a 1992). it is that, in gen ness costs to a plant (Simms of energy ferences in timing of leaf flush of in dividual host plants (maple and oak). 1994). However, to conclude cal inefficiency has fit they do not sum to 100% of the or reasonable on insect solubilize phenolic-protein com plexes), altering rate of excretion, having reduced sensitivity to allelochemicals, and sequestering plant toxins (Slansky 1992, Dussourd 1993). Determining that decrease in reproduction if together ganism of food quality array of countermeasures that facilitate exploitation of plants, which include behavioral and 1% of biomass) not result constraint herbivores helps explain the ecologi and Scriber 1985), so herbivores deal with poorer food quality than preda tors. Much of the variation in rela tive growth rate of insect herbivores can be explained by nitrogen and water to un on in sect herbivorenumbers,which in turn limits secondary consumers, or predators. This message about the central principle of ecology. allelochemical comprising less than may sects to extract is fundamental derstanding a major limitation in plant ma much less concentrated terial than in animal tissue (Slansky that food quality is more of a prob lem for most insect herbivores than food quantity. For instance, parthe crease make that nitrogen difficult for in worm differ in both adult emergence time and egg hatching time (Mitter et al. 1979). These times parallel dif cankerworms grow best on young leaves, which have higher ni trogen and water content. Individual trees tend to be relatively constant in timing of leaf flush, e.g., early year after year, and cankerworm clones tend to use the same trees year after year. Consequently, via genotype and low dispersal, the herbivores are able to track the narrow window of availability of new leaves, the high est quality food. It is the work on in sect herbivores, a very diverse group of herbivores in terms of plant tissue that makes used and feeding method, it clear that obtaining high-quality food is a basic problem for herbivore species in general. Yet only half of the ecology texts addressed this point, and even then the message was diffusely presented. It is a point that seems obvious to us, but one that students can easily miss. Understanding that animalsmust extract nitrogen in order to grow and thatplants contain little nitrogen and can counter plant de fenses increases our understanding of the mechanisms structuring food webs and provides insight into the success of insect pests. 5. Plants are a major force driving the evolution offeeding specializa tion by insect herbivores that frequently leads to narrow host plant ranges. This point is nicely illustrated in and Mitter's (1994) study of Farrell milkweeds (Asclepias) of beetles and a group on them. Phy specializing logenies of the host plants and herbi vores are closely matched. While the process that generates patterns of feeding specialization is unclear, host-plant chemistry would often have had a role, perhaps directly as feeding deterrent or stimulant, re ducing or enhancing insect growth or survivorship, or perhaps simply by favoring "specialization" through simplification of decision-making Bulletin of theEcoiogical Society of America This content downloaded from 128.226.37.5 on Thu, 26 Dec 2013 09:21:06 AM All use subject to JSTOR Terms and Conditions texts gave borers, seed and fruit feeders, but less for exposed leaf chewers (Denno et al. 1995). In contrast to other data an example of feeding specialization and mentioned by insect herbivores the roles of secondary metabolites, this how common none indicated sets (e.g., Connell 1983, Schoener 1983), the data set for insect herbi to compare is large enough vores feeding guilds and life history traits pattern was. and and aggregation), (e.g., mobility thus to test hypotheses. For example, competition was detected more fre and Chapman processes (Bernays 1994). Al 1994, Bernays and Wcislo though half of the ecology people may think that her like grasshop bivores are generally have a very pers, some of which Most wide more host plant range. But in fact, than 90% of insect herbivores to plants in three or are restricted fewer plant families (Bernays and Graham 1988), and 70% of insect are even more special herbivores their feeding to plant restricting ized, species in one family (Bernays and So the study of Chapman 1994). interactions, with an plant-herbivore emphasis on the role of phytochem istry, has contributed to significantly of host plant our understanding by insect herbivores specificity of a striking pattern yielding biodiversity. This is an important since plants and insect her message, bivores together account for about 50% of macroscopic species (Strong et al. 1984). 6. The importance of direct competi tion forfood among insect herb ivores instructuringcommunities depends on typeoffeeding and life history traits. Half tioned of the ecology texts men Smith Hairston, and that Slobodkin's (1960) observation is green," from which "the world these authors deduced that predators, rather than food, limited population size of herbivores. for a Although different reason (number of species present on a host plant being limited by pool Strong, of gregated feeders species, (Denno and forb and grass et al. 1995). Since insect herbivores account for 26% of the macroscopic species (Strong et al. 1984), these patterns of competi insect herbivores give tion between us insight into the conditions under can be more or which competition less important than other factors in structuringcommunities. 7. Indirect,or resource-mediated and enemy-mediated,interactions among insect herbivores as well as negative ent, yet both are important in orga nizing community structure. Large vertebrate herbivores are often eco systemmodifiers (e.g., beaver, prai rie dogs, moose, Thomson's gazelle, and elephants alter nutrient cycling of and abundance and distribution and thus have a large impact plants) on other herbivores (McDowell and et al. 1986, McNaughton Pastor et al. 1988, Whicker and Detling 1988). In comparison, on a herbivores operate insect Naiman 1988, yet can have just as pro on their associates. found an effect herbivores associa ability can reduce nitrogen avail in and induce plant defenses tions. Resource-mediated interactions foliage, resulting in reduced growth rate, survival, fecundity and density refers to feeding by of herbivores one causing herbivore species changes in the plant that in turn in fluence the plant's quality as food of other herbivore species (Denno et the scale of ef al. 1995). Likewise, fects of enemy-mediated interactions differs for invertebratevs. vertebrate herbivores, yet both contribute sig nificantly to community structure. for other species 1993). (Damman For example, damage on cotton by a herbivorous mite induced resistance These indirect interactions to armyworms than ecological subtleties; and another mite spe and Carey 1984, (Karban Karban 1988). In enemy-mediated interactions, herbivores interact indi the foraging be rectly by affecting havior and population dynamics of cies natural enemies. For instance, leaf miners near colonies of ant-tended treehoppers suffered lower levels of predation by nabid bugs than those colonists), farther from the ant-treehopper groups, because the ants chased bugs away leaf miners insect herbivores as it is for other kinds of organisms. However, a re cent review of 193 species interac tions suggests that exploitative and interference competition are impor tant for insect herbivores, particu larly for sap feeders,wood and stem the interactions of predators and of predators and leaf miners. Enemy mediated interactionsbetween insect herbivores are as common as direct competitive interactions, and re source-mediated interactions be tween insect herbivores are more ence of (Fritz 1983). Thus, the benefitted by the pres treehoppers, which are more they are importantin explaining the distribu of insect herbi tion and abundance vores. 8. Herbivory lessens a plant's ability to compete with its neighbors and thus affects plant density. of Here are a few examples increasing levels of de many. With foliation, defoliated plants were the reached a similar conclusion: is not as important a competition force in structuring communities of (1984) of resource scale of effects For example, throughfeeding, insect common,frequently resulting in positive The mediated interactionsbetween inver tebrateherbivores vs. those between vertebrate herbivores is quite differ microscale, are and Southwood potential Lawton, quently between sessile species, ag common than direct competitive in teractions (Damman 1993). Also, in contrast to competitive interactions, not all indirect interactionsbetween herbivoreshave a negative outcome. altered in terms of height smaller and produced damaged fewer plants and mass, than un and Bazzaz seeds (Lee 1980). In another study, insectherbi vores feeding on flowers and fruits dramatically reduced seedling re cruitment to the plant population (Louda 1982). Thus, herbivory less ens a plant's ability to competewith its neighbors and influences popula tion size of plants. January This content downloaded from 128.226.37.5 on Thu, 26 Dec 2013 09:21:06 AM All use subject to JSTOR Terms and Conditions 1996 55 Although this message seems ob vious to us, the implications for a plant are not so obvious to students, most of whom have had little or no experience ture. The gardens or agricul fundamental ecological constraints on plants are that plants have limited resources, some of which with they must neighbors use to battle with and herbivores. plant-insect What the herbivore literature shows is that even small herbivores, such as insects, can reduce the abil ity of a plant to compete with its neighbors for light, water, and nutri ents and consequently influence dis tribution and abundance of plant spe cies (Louda et al. 1990). 9. Plant chemistryandmorphology can influence the abilities of parasitoids and insectpredators to locate insectherbivores. Examples of how plant chemistry and morphology hinder the herbi enemies vores' are the numerous studies on the effects of trichomes on herbivores and their invertebrate en emies. Some trichomes have glands at the tips that break open to release chemicals, and the exudate from the trichomes can hinder insect preda tors. For instance, four cultivars of tomato differing in their susceptibil ity to an insect herbivore that was a specialist on Solanaceae were tested (Barbour et al. 1993). Egg predators were placed on leaves, with tri chomes unmanipulated or exudate removed from the trichomes. When the exudate was present, egg con sumption declined in the more resis tant cultivars. Predator mortality was higher when was the exudate is an example of present. This chemical resistance interfering with of the host plant the effectiveness of can also Trichomes emies (Vet and mans are visually relatively poor students do not Dicke 1992). Hu oriented and have a sense of smell, so easily relate to the fact that detecting odor plays a huge role in a parasitoid or insect predator's ability to locate hosts or prey. Most vertebrate predators de pend greatly on visual prey (Heinrich Collins 1993), on plant pend cues to locate 1993, Seigel and and they do not de chemistry for cues. Plant-insect herbivore-insect enemy interactions pattern show a very different from that of plant-vertebrate herbivore-enemy interactions: a plants (i.e., use of plant morphology and chemistry as cues, and tolerance or detoxification of plant allelo vore-enemy biodiversity. chemicals interactions on plants. None of the ecology texts con the veyed point that plants can en hance or hinder the activity and thus effectiveness of the herbivores' en 11. Parasitoids and insect predators can reduce herbivore populations enough to improveplant productivity emies. This is an important message for understanding tritrophic level in teractions in natural systems and the limits of biological control in agri and otherfitness correlates. For example, the mango shoot was accidentally caterpillar intro duced to Guam, where one of the major crops is mango. In 1986, a culture and managed parasitoid forests. How can enemies be selected upon by their prey or hosts? De fenses, concealment, and phenology, numbers of insect herbivores limit was introduced to control the caterpillar pest. With the in crease in parasitism, caterpillar num bers declined (Nafus 1991). What were the consequences for the plants? After 1986, the number of flowers and fruits increased. Extra-floral nectaries on plants promote this kind of relationship be tween plants and insects attacking the evolutionary herbivores 10. Insect herbivores act as selective agents on their enemies, with the result that parasitoids tend to be more host specific than predators. vores' options of the herbi enemies (Price 1994). Allelochemicals herbivores ingested by insect can interfere with devel than predators and their generation timemust be synchronized to thatof their host. Such characteristicsallow parasitoids to use microhabitats that would not support a predator and to evolve as fast as theirhost (Weseloh 1993). the Ecological sitoids and insect herbivores than predators (ratio of 0.9:1:0.1), i.e., there are seven times as many parasi toid as predator species (Price 1980). The rich biodiversity of the inver tebrate portion of the third trophic level reflects an intimate link with of the third trophic level (= carnivores) are intimately linked with portion On the other hand, parasitoids and insect predatorsuse plant chem istry as a cue to locate theirhosts or prey (Vinson 1976, Obrycki 1986). For instance, chemical changes in plant tissue induced by herbivores have been shown to attract insect en of which are much less spe in diet (Price 1980). For in in the British insect fauna, there are many more species of para cialized stance, None ingested). of the texts ecology put this together in a way that permits students to see the of plant-insect consequences herbi of parasi opment and survivorship toids and insect predators (Barbosa et al. 1991, Malcolm 1992). But parasitoids are usually much smaller Bulletin predators, greater interdependency with plants that, in turn, has shaped a very differ ent sensory perception of the world. About 25% of the macroscopic spe cies are parasitoids and insect preda tors (Price 1980). Thus, a large pro egg predators. search physically hinder parasitoids ing for their hosts (Hulspas-Jordan and van Lentren 1978). 56 The result of such interactions is that parasitoids are relatively special ized in use of host species and are much more speciose than insect Society 1978, Koptur (Bentley 1977, Tilman and thus are an of this top product 1992), evolutionary down effect of the herbivores' en emies on plants. Although extra-flo ral nectaries are usually discussed in in ecology texts, they are presented the context of a special type of mutu alism rather than as at one end of a continuum of interactions among plants, insect herbivores and insects attacking herbivores. That may be a consequence of thinking that plants and predators do not interact,but as discussed in points 9 and 10 above, of America This content downloaded from 128.226.37.5 on Thu, 26 Dec 2013 09:21:06 AM All use subject to JSTOR Terms and Conditions parasitoids and insect predators clearly respond to plant traits and plants can provide signals to insects, This is an though nonspecifically. example of how we can help students see the broader patterns, as opposed to just seeing the details of a particu lar case study. That parasitoids and invertebrate predators can reduce herbivore popu lations enough to improve plant pro in ductivity has been demonstrated thus natural and managed systems, ter the introduction of the parasi toids, species diversity increased dra matically, and thus the parasitoid spe acted as a keystone species (sensu Paine 1966) by suppressing the dominant herbivore. Although not a natural system, this example illus cies trates natural (and repre common phe sents an increasingly as species are moved nomenon around the world by humans). Al though many biodiversity processes know there is a few have a con people crisis, for what main control a viable biological alternative to pesticides commercial in at least some situations (Jutsum ceptual 1988, Waage and Greathead 1988). Even though most of the ecology texts provided an example of bio logical control, only half of these on system (1966,1974) rocky intertidal system help students see the link between in texts logical scale and biodiversity pression on an ecological making plants clearly made the point that benefit by the presence and predators. of parasitoids 12. The problems framework tains a community of diverse of organisms teractions on an eco (an ex scale of But to see processes). picture, such examples evolutionary the broader need to be integrated that must be organ such as the mango Guam and Paine' s isms. Examples into a hierarchy overcome before insects can feed on plants have led to host plant special ization and proliferation of species. which we can now of generalities, provide, for instance, via an overview of the messages of plant-insect herbi Plant effects on herbivores carry vore-insect over to the third trophic level, (Table 1). Lastly, although there is much to admire in these ecology texts, I felt that none of these 12 messages were conveyed clearly in these texts, that especially toparasitoids, resulting in another very speciose group. The number of macroscopic spe cies is estimated as between 5 and 30 million 1988). Although insect species are distributed among only 8 of 29 insect orders, they account for 26% of the and macroscopic species (Weis Berenbaum the her 1989). Thus, most (Wilson herbivorous bivorous insect orders are very spe cies rich. Insects, their host plants and their parasitoids and invertebrate predators together account for an es timated 75% of species. Thus, study of plant-insect herbivore interac tions, as evident by these messages (Table 1), has taken us a long way toward understanding a large portion of this planet's The mango biodiversity. system on Guam is, not interactions enemy in any way that a student could and recognize and assimilate, there were not even hints of many of them. This handicaps students in un as the issues such of crisis, management of rapid global pests, consequences warming, etc. As a starting place for a more detailed overview of plant I suggest herbivore interactions, Abrahamson's (1989) edited volume on plant-animal interactions. derstanding biodiversity Some general comments about thesepoints microcosm reflecting the sum effects of these 12 points for community ecology. Prior to the introductionof parasitoids to control the dominant insect herbivore on mango, diversity of insect herbivores on mango was low (SchreinerandNafus 1992). Af herbivore interactions, herbivores mon available, but it is also worth noting some importantdiffer ences between invertebrateand ver tebrate terrestrialherbivores. In gen eral, 10 of these points apply to plant-vertebrate as well as plant-in vertebrate herbivore systems. The exceptions are points 9 and 12. Re are not a com feature of plant-vertebrate her bivore systems. Exception to point 12 requires more explanation. Relatively less di versity of vertebrate herbivores com pared to invertebrate herbivores may largely reflect the constraints of size and of endothermy for Due to these birds and mammals. constraints and thus a need for large amounts of food, vertebrate herbi body vores are usually generalist feeders to though they limit their feeding particular types of plants or plant and Georgiadis parts (McNaughton 1986, Lindroth 1989). Furthermore, parasites and preda tors of vertebrate herbivores are not as speciose as those of invertebrate herbivores, reflecting the differences in the direct and indirect on vertebrate vs. parasites and predators. plants effects of invertebrate the relationship of Consequently, these points, especially the effects of plant chemistry, competition and predation, for vertebrate herbivore vs. invertebrate herbivore systems systems, differs. The high degree of exhibited by feeding specialization most insect herbivores is largely at tributed to two selective pressures, host plant chemistry and the herbi vores' enemies (Bernays and Gra ham 1988), although competition may play an important role for many et al. insect herbivores (Denno 1995). Thus, plant chemistry, preda tors being deterred by prey contain ing plant toxins, and parasites' spe cialization shaped by plant chemistry seem much more than important in structuring inverte competition brate herbivore communities they do in vertebrate The focus here is on plant-insect is a garding point 9, the effects of plants on the herbivores' predators, other than through changes in numbers of herbivore In contrast, munities. ter-specific competition than com intra- and in may have a larger role in shapingvertebrateher bivore communities (Lindroth1989). Even though 10 of themessages apply to both invertebrateand verte brate terrestrialherbivores, some of these points need furtherexplanation relative to vertebrates. Regarding January This content downloaded from 128.226.37.5 on Thu, 26 Dec 2013 09:21:06 AM All use subject to JSTOR Terms and Conditions 1996 57 point 3, due to body size and to en dothermy of birds and mammals, ob taining sufficient food quantity, e.g., during unfavorable seasons, may of ten constrain vertebrate herbivores more dom than food quality. That is sel the case for insect herbivores, but only active in part because they are in unfavorable seasons. 1 and 2, adapta points during Regarding tions to herbivory cotyledonous by most plants, mono such as struc meristems, high root-to-shoot ratio, seem to re and grazing tolerance, flect an association with orthopteran and large mammals in ecology texts and to facilitate the presentation of the mes sages of plant-herbivore interactions to ecology students (via communi cating to those teaching ecology and writing ecology texts). However, for some other groups, I would suggest on a subset focusing sages. For example, seven introductory of these mes I also examined texts biology in 1990-1995 for their published tural reinforcement through accumu lation of silica, intercalary sheathed insects represented coverage of plant-herbivore interac tions. On average, two pages, or 0.2% of the text, dealt with plant herbivore interactions. Conse quently, given the page restriction, these texts could not begin to cover et al. 1985). In con (McNaughton trast, adaptations to herbivory by the 12 messages that I have listed. Four of the texts addressed some part of point 1, three addressed some part other terrestrial plants (e.g., elabo rate secondary chemistry) largely re flect an association with other in of points sects. Thus, for the former group of the cost of evading and suf in terms is mainly fering herbivory interactions entirely. My rec ommendation for an introductory bi text is solid presentation ology of points 1, 4, 5, 1 1, and 12. We might also want to emphasize these five to the public. messages plants, of tolerance mechanisms, whereas for the latter group, cost is more likely to include physical and chemi 4, 5 and 11, but none ad dressed points 6-10 or point 12. One text ignored plant-her introductory bivore degree to which these 12 messages would apply to marine sys tems is unclear. Marine plant-herbi vore systems differ fundamentally from terrestrial systems (Hay 1991). For example, in general the intensity of grazing is greater in marine sys tems, the dispersal stages (planktonic larvae) have very limited ability to choose microhabitats, and specialist herbivores are rare. Probably the messages apply in general, but with a qualifier for point 11 in particular. Marine mesograzers (such as amphi pods and polychaetes), probably the to terrestrial equivalents insects, are subject to intense preda as well as car tion by herbivorous fish (Hay and Fenical nivorous ecological Conclusions our colleagues, and the Acknowledgments I thank Robert Fritz, Patrice Mor row, John Titus, Rich Wilkens, and ErnestWilliams for their insightful comments on the manuscript, and May Berenbaum for the suggestion to look at introductory biology texts. Literature cited Abrahamson, W. G. 1989. Plant-ani mal interactions. McGraw-Hill, New York, New York, USA. M. P. 1993. Plant defense, Ayres, herbivory, and climate change. Pages 75-94 in P. M. Kareiva, J. G. Kingsolver, and R. B. Huey, editors. Biotic interactions and global change. Sinauer Associ ates, Sunderland,Massachusetts, USA. I. T., C. L. Sims, Baldwin, and S. E. Kean. 1990. The reproductive consequences associated with in ducible in alkaloidal responses wild tobacco. Ecology 71:252 The study Barbosa, of the chemical de fense in plants and insect herbivores has shaped much of our current thinking about the interactions of In turn, that plants and herbivores. research has contributed fundamen tally to study of terrestrial tritrophic and thus substantially interactions, increased our understanding of com structure. Those are signifi munity to the field of cant contributions it in that has taken us a long ecology, toward understanding the ecol ogy of 75% of the macroscopic spe cies. way 1988). Thus, enemies of mesograzers effect on may not have a positive a title was, My "Developing in herbivore theory of plant-insect are we there yet?" The teractions: answer is "We are there, but our col leagues writing ecology texts do not plant productivity. Twelve points, as opposed to some other number, worked for meeting my primary objectives in writing this paper, which were to alert researchers in plant-herbivore interactions as to how our field is have a clear sense of that."We are at a place now where we have some systematically organized generaliza tions, and thushave a basic theoryof plant-insect herbivore interactions. However, we need to do a better job at conveying the big messages of the 58 to students, public. 262. cal defenses. The study of plant-herbivore interactions Bulletin of the Ecological Society P. P., Kemper. Gross, and J. 1991. Influence of plant on the tobacco allelochemicals hornworm and its parasitoid, Cotesia congregata. 72:1567-1575. Ecology Barbour, J. D., R. R. Farrar, and G. G. Kennedy. 1991. Interaction of fertilizer regime with host-plant in tomato. Entomolo resistance gia Experimentalis et Applicata 60:289-300. Barbour, J. D., R. R. Farrar, and G. G. Kennedy. 1993. Interaction of Manduca mato sexta with resistance insect in to predators. Entomologia Experimentalis et Applicata 68:143-155. Begon, M., Population study and M. Mortimer. 1981. a unified ecology, of Blackwell UK. animals and plants. Scientific, Oxford, Bentley, B. L. 1977. Extrafloral nec taries and protection by pugna Re cious bodyguards. Annual view of Ecology 8:407-427. of America This content downloaded from 128.226.37.5 on Thu, 26 Dec 2013 09:21:06 AM All use subject to JSTOR Terms and Conditions and Systematics Bernays, E., and M. Graham. 1988. On the evolution of host specific arthropods. ity in phytophagous Ecology 69:886-892. Bemays, E. A., and R. F. Chapman. 1994. Host-plant selection by phy tophagous insects. Chapman and New York, Hall, New York, USA. and W. E. A., Bernays, T. Wcislo. 1994. Sensory capabilities, infor mation and resource Review processing, specialization. Quarterly of Biology 69:187-204. to vertebrate herbivory. Oikos 40:357-368. 1976. Plant-herbivore in R. M. Pages 94-113 G. Caughley, systems. May, editor. Theoretical ecology: W. principles and applications. Penn B. Saunders, Philadelphia, sylvania, USA. P. D. 1987. Coley, in plant variation properties: Interspecific anti-herbivore the role 'of habitat quality and rate of disturbance. 106 (Supple New Phytologist ment):25 1-263. Coley, P. D., Chapin, 1985. and plant availability vore defense. Science and F. S. Resource J. H. 1983. On the preva Connell, lence and relative importance of interspecific competition: evi dence from field experiments. Naturalist 122:661 American 696. J. 1983. Herbivory, the inter dynamics of animal-plant actions. University of California Press, Berkeley, California, USA. Cuthbert, F. P., Jr., R. L. Fery, and 0. L. Chambliss. 1974. Breeding for resistance to cowpea curculio in southern peas. HortScience 9:69-70. Damman, H. 1993. Patterns of inter action among herbivore species. Pages 132-169 in N. B. Stamp and T. M. Casey, editors. Cater pillars: ecological and evolution ary constraints on foraging. Chapman and Hall, New York, J. Taka Sabelis, humus. 1990. Plant strategies of in pest for application Journal of Chemical Ecology 16:3091-3118. D. E. 1993. Foraging with Dussourd, finesse: caterpillar adaptations for circumventingplant defenses. Pages 92-131 T. M. Casey, in N. E. Stamp and editors. USA. 18:586-608. Stamp and T. M. Casey, editors. and evo Caterpillars: ecological lutionary constraints on foraging. Chapman and Hall, New York, New York, USA. D. A., Herms, grow B. D., C. Mitter, and D. 1992. Diversification J. at interface. Bio the insect-plant Science 42:34-42. Feeny, P. 1976. Plant apparency and Recent Ad defense. chemical vances in Phytochemistry 10: 1-40. Fritz, R. S. 1983. Ant protection of a conse host plant's defoliator: quence of an ant-membracid mu 1978. Gahan de Faculteit schappen relationship (Hymenoptera: Landbouwweten Gent Rijksuniversiteit Johnson, M. T., and F. Gould. 1992. of genetically engi Interaction neered host plant resistance and enemies of Heliothis natural virescens (Lepidoptera: Noctui dae) in tobacco. Environmental Entomology 21:586-597. Jones, C. G. 1983. Phytochemical and insect variation, colonization, of communities: The case num). Denno the of plant form and func tion. Cambridge University Press, economy Cambridge, UK. Hairston, N. G., F. E. Smith, The Aphelinidae). Mededelingen van bracken On to Re leaf structure between host-plant of and parasitization efficiency the parasitic Encarsia wasp S. L., and H. A. Mooney. on plant Cost of defense in T. productivity. Pages 681-698 editor. Quarterly view of Biology 67:283-335. P. M., and J. C. van Hulspas-Jordan, tualism.Ecology 64:789-797. Gulmon, 1986. J. Givnish, J. Mattson. of plants: 43:431-440. American Zoologist 34:57-69. Futuyma. and W. or defend. formosa 1994. and C. Mitter. radiation in insects and time and opportunity. B. D., de of Ecology 19:111-145. and Systematics Heinrich, B. 1993. How avian preda tors constrain caterpillar forag 224-247 in N. E. ing. Pages Lentren. P. R., and P. H. Raven. Butterflies and plants: a Evolution study in coevolution. Ehrlich, 1964. Adaptive of chemical Review 1992. The dilemma Caterpil and evolutionary lars: ecological constraints on foraging. Chapman and Hall, New York, New York, Farrell, Evolution 6:362-365. Hay, M. E., and W. Fenical. 1988. Marine plant-herbivore interac fense. Annual manipulating predator-prey inter actions through allelochemicals: prospects Hay, M. E. 1991. Marine-terrestrial contrasts in the ecology of plant chemical defenses against herbi in Ecology and vores. Trends tions: the ecology and M. A. Post J. Bruin, Farrell, antiherbi 230:895 899. Crawley, M. M., M. W. bayashi, plants: J. P. Bryant, III. mology 40:297-331. Dicke, control. Bryant, J. P., F. S. Chapin, III, and D. R. Klein. 1983. Carbon/nutri ent balance of boreal plants in re lation New York, USA. and J. Denno, R. F., M. S. McClure, R. Ott. 1995. Interspecific interac insects: tions in phytophagous re-examined and res competition urrected. Annual Review of Ento and L. B. Slobodkin. 1960. Community structure,population control, and competition.American Naturalist 94:421-425. Harbomne,J. B. 1982. Introductionto ecological biochemistry. Aca demic Press, London,UK. fern (Pteridium aquili in R. F. Pages 513-558 and M. S. McClure, edi tors. Variable plants and herbi vores in natural and managed sys tems. Academic New Press, York, New York, USA. Jutsum, A. R. 1988. Commercial plication of biological ap control: status and prospects. Philosophi cal Transactionsof theRoyal So ciety of London, Series B 318:357-373. Karban, R. 1988. Resistance to beet armyworms (Spodoptera exigua) induced by exposure to spider January This content downloaded from 128.226.37.5 on Thu, 26 Dec 2013 09:21:06 AM All use subject to JSTOR Terms and Conditions 1996 59 mites (Tetranychus turkestani) in cotton. American Natu Midland ralist 119:72-82. R., Karban, 1984. and J. R. Carey. of cotton seed Induced resistance Science 225:53-54. G. G., and J. D. Barbour. in Resistance variation lings to mites. Kennedy, 1992. natural Pages systems. and managed 13-41 in R. S. Fritz and E. L. Simms, editors. tance to herbivores Plant resis and patho evolution, and ge gens: ecology, netics. University of Chicago S. 1992. Extrafloral Koptur, nectary interactions between in sects and plants. Pages 81-130 in Insect E. A. Bernays, editor. IV. Volume plant interactions. mediated CRC, Boca Raton, Florida, USA. 1980. Lee, T. D., and F. A. Bazzaz. Effects of defoliation and compe tition on growth and reproduction in the annual plant Abutilon Journal of Ecology phrasti. theo 68: 813-821. Lindroth, R.L. 1989. Mammalian interactions. herbivore-plant Pages 163-206 hamson, in W. G. Abra editor. Plant-animal in New teractions. McGraw-Hill, York, New York, USA. Loomis, W. E. 1932. Growth-differ vs. carbohy entiation balance ratio. Proceedings drate-nitrogen of the American Society of Horti cultural Science 29:240-245. correlation. 1953. Growth inW. E. Loomis, Pages 197-252 editor. Growth and differentiation Iowa State College in plants. Press, Ames, Iowa, USA. Lorio, P. L., ferentiation Jr. 1986. Growth-dif balance: a basis Diego, California, S. B. Malcolm, for southern pine understanding Forest interactions. beetle-tree 14: and Management Ecology 259-273. USA. 1992. Natural enemies: biology of predators, the population parasites, Blackwell Scien and diseases. tific, Oxford, UK. May, R. M. 1973. Stability and com in model ecosystems. plexity Press, University Princeton, New D. M., McDowell, Jersey, USA. and R. J. Naiman. 1986. Structure and function of a benthic invertebrate munity as influenced (Castor canadensis). stream com by beaver Oecologia D. 1974. Adaptive patterns McKey, in alkaloid physiology. American Naturalist 108:305-320. J. S. J., and N. 1986. Ecology of Af Georgiadis. rican grazing and browsing mam mals. Annual Review of Ecology McNaughton, 17:39-65. and Systematics S. J., R. W. Ruess, and McNaughton, S. W. Seagle. 1988. Large mam mals and process dynamics in Af rican ecosystems. BioScience Ecology 66:528-535. J. C. C., D. J. Futuyma, Mitter, Schneider, and J. D. Hare. 1979. Genetic variation and host plant in a parthenogenetic relations 33:777-790. and con S. 1994. Trade-offs Mole, in plant-herbivore straints de fense theory: a life-history per of Louda, S. M. 1982. Limitations the recruitment of the shrub Hap spective. Oikos 71:3-12. control of Nafus, D. 1991. Biological lopappus squarrosus (Asteraceae) by flower- and seed-feeding in sects. Journal of Ecology 70:43 53. Louda, S. M., K. H. Keeler, and R. D. Holt. 1990. Herbivore influ ences on plant performance and Pen icillaria jocosatrix (Lepi doptera:Noctuidae) on mango on Guam with notes on the biology of its parasitoids. Environmental Entomology 20:1725-1731. Noy-Meir, I. 1975. Stability of graz ing systems: an application of 60 Bulletin of the Ecological J. J. 1986. The influence of foliar pubescence on entomopha Boethel in D. J. and R. D. Eikenbary, tors. Interactions of plant edi resis tance and parasitoids and preda New tors of insects. Halsted, York, New York, USA. Paine, R. T. 1966. Food web com plexity and species diversity. American Naturalist 100:65-75. . 1974. Intertidal community structure:experimental studies on the relationship nant competitor a domi and its principal between predator.Oecologia 15:93-120. Pastor, J., R. J. Naiman, and P. McInnes. microbes, B. Dewey, 1988. Moose, and the boreal forest. Price, P. P. 1980. Evolutionary ogy of parasites. Princeton biol Uni New Jer Press, Princeton, versity sey, USA. Price, P. W. 1994. Evolution of para Pages 472 sitoid communities. 491 in B. A. Hawkins and W. Sheehan, editors. Parasitoid com munity ecology. Oxford Univer sity Press, Oxford, UK. . 1991. The plant vigor hy and herbivore attack. pothesis Oikos 62:244-251. 38:794-800. S. J., J. L. Tarrants, McNaughton, M. M. McNaughton, and R. H. Davis. 1985. Silica as a defense and a growth against herbivory in African grasses. promotor Evolution Obrycki, BioScience 38:770-777. 68:481-489. moth. predator-prey graphs. Journal of Ecology 63:459-481. gous species. Pages 61-83 Prey defense and predator foraging. Pages 458 475 in M. J. Crawley, editor. Princeton Illinois, USA. Press, Chicago, interactions. Pages competitive in J. Grace and D. Til 413-444 man, editors. Perspectives on plant competition. Academic Press, San Price, P. W., C. E. Bouton, P. Gross, B. A. McPheron, J. N. Thomp 1980. Inter son, and A. E. Weis. among three trophic lev els: influence of plants on inter actions between insect herbivores and natural enemies. Annual Re actions view of Ecology and Systematics 11:41-65. N. Cobb, T. P. Craig, J. K. Itami, S. Fernandes, and R. W. Preszler. Mopper, 1990. Insect herbivore population Price, P. W., G. W. on trees and shrubs: dynamics new approaches relevant to latent and eruptive species and life table development. Pages 1-38 in E. A. Bernays, editor. Insect-plant in teractions.Volume II.CRC, Boca Raton, Florida,USA. Rhoades, D. F. 1979. Evolution of plant chemical defense against herbivores. Pages 3-54 in G. A. Society of America This content downloaded from 128.226.37.5 on Thu, 26 Dec 2013 09:21:06 AM All use subject to JSTOR Terms and Conditions Rosenthal and D. H. Janzen, edi with secondary plant metabolites. Academic Press, New York, New York, USA. D. F., and R. G. Cates. Rhoades, 1976. Toward a general theory of plant antiherbivore chemistry. Re in phytochemistry cent advances G. A., and D. H. Janzen, their editors. 1979. Herbivores: interaction with secondary plant metabolites. Academic Press, New York, New York, USA. Schoener, T. W. 1983. Field experi ments on interspecific competi tion. American Naturalist 122: 240-285. I. H., Schreiner, 1992. Changes and D. M. Nafus. in a moth commu nity mediated con by biological trol of the dominant species. En vironmentalEntomology 21:664 668. Scriber, J. M., USA. and F. Slansky. Comprehensive iology, Insect Phys and Phar Biochemistry Strong, D. R., New York, USA. Simms, E. L. 1992. Costs of plant re sistance to herbivory. Pages 392 425 in R. S. Fritz and E. L. Simms, editors. Plant resistance to herbivores and pathogens: and genetics. evolution, University of Chicago Press, Chi cago, Illinois, USA. Slansky, F., Jr. 1992. Allelochemi cal-nutrient interactions in herbi vore nutritional ecology. Pages 135-174 in G. A. Rosenthal and M. R. Berenbaum, editors. Herbi patterns and mechanisms. Harvard University Press, Cambridge,Massachusetts, USA. D. W., Tallamy, and M. J. Raupp, 1991. Phytochemical in John duction by herbivores. Wiley and Sons, New York, New York, USA. Tiedje, J. M., R. K. Colwell, Y. L. editors. R. E. Hodson, R. E. Grossman, Lenski, R. N. Mack, and P. J. Re gal. 1989. The planned introduc tion of genetically engineered or Entomology 26:183-211. R. A., and J. T. Collins. Seigel, 1993. Snakes: ecology and be New York, havior. McGraw-Hill, J. H. Lawton, and R. on 1984. Insects Southwood. plants: community 1981. Society Weis, A. E., and M. R. Berenbaum. W. plants. G. Plant-animal Ecology and M. Dicke. 1992. use by of infochemical enemies in a tritrophic natural context. Annual Review 37:141-172. mology S. B. 1976. Host Vinson, of Ento lenges sophical and opportunities. Transactions Philo of the New York, New R. M. 1993. Potential ef Weseloh, fects of parasitoids on the evolu tion of caterpillar foraging behav ior. Pages 203-223 in N. E. and T. M. Casey, editors. and evo Caterpillars: ecological Stamp lutionaryconstraints on foraging. Chapman and Hall, New York, New York, USA. A. D., and J. K. Detling. Whicker, 1988. Ecological prairie dog consequences disturbances. of Bio Science 38:778-785. White, T. C. R. 1974. A hypothesis to explain outbreaks of looper caterpillars with special reference to populations of Selidosema in a plantation of Pinus ra in New Zealand. Oecologia suavis . 1984. The abundance of in in relation vertebrate herbivores to the availability in of nitrogen stressed food plants. Oecologia 63:90-105. E. 0. Wilson, state 1988. The current of biological diversity. Pages 3-18 in E. 0. Wilson, edi tor. Biodiversity. National Acad emy selection by insect parasitoids. Annual Re 21:109-133. view of Entomology J. K., and D. J. Greathead. Waage, 1988. Biological control: chal in editor. York, USA. 16:279-301. L. E. M., 123-162 interactions. McGraw-Hill, ants and tent caterpillars: timing of nectar production in relation to suscepti bility of caterpillars to ant preda tion. Ecology 59:686-692. Pages Abrahamson, Ecology 70:298-315. 1978. Cherries, Series 1989. Herbivorous insects and diata D. of London, B 318:111-128. consider ganisms: ecological ations and recommendations. Tilman, Vet, Royal green Slansky, F., and J. M. Scriber. 1985. Food consumption and utilization. The nutritional ecology of imma ture insects. Annual Review of ecology, sec ondary plant metabolites. Volume edition. Academic II. Second Press, New York, New York, macology 4:87-163. 10:168-213. Rosenthal, their interaction with vores: tors.Herbivores: their interaction Press, Washington, D.C., USA. Department Nancy E. Stamp of Biological Sciences Binghamton University State University of New York Binghamton, NY 13902-6000 January 1996 This content downloaded from 128.226.37.5 on Thu, 26 Dec 2013 09:21:06 AM All use subject to JSTOR Terms and Conditions 61