PerspectiveEcology

The Enemy of My Enemy Is My Ally

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Science  16 Mar 2001:
Vol. 291, Issue 5511, pp. 2104-2105
DOI: 10.1126/science.1059939

When attacked by insects or other herbivores [HN1], plants release airborne chemical information in the form of volatile organic compounds. Assuming that there are no more than three trophic levels in the food chain—plants, herbivores, and predators—emission of these infochemicals may benefit plants in four separate ways. First, these volatiles signal to other herbivores that the plant's defense system [HN2] has been switched on. Second, volatiles let other herbivores know that the plant is already under attack and so, to avoid competition, they may prefer to feed elsewhere. Third, they signal to the predators of herbivores that their prey is in the vicinity. Fourth, as a by-product of attracting predators, the plant alerts hungry herbivores that it is a well-guarded fortress. Taken to their extremes, some of these possibilities exclude one another—for example, a plant that is toxic to herbivores may have few prey to offer predators. Under more realistic conditions, however, all four possibilities may act in concert. Although laboratory (1) and field (2, 3) experiments have amply demonstrated pronounced responses of herbivorous and predaceous insects to herbivore-induced plant volatiles [HN3], all of these experiments have been conducted in agricultural settings (4, 5). On page 2141 of this issue, Kessler and Baldwin [HN4] (6) present evidence that herbivore-induced plant volatiles are both a direct and an indirect plant defense in nature as well. They show that plants under attack by herbivorous insects release volatiles that both repel new herbivores and attract insect predators.

In a series of elegant experiments conducted in the Great Basin desert of south-western Utah [HN5] in the United States, Kessler and Baldwin first established that wild tobacco plants [HN6] release volatiles when fed upon by three species of herbivorous insects (see the figure). Next, they studied the degree of predation of herbivore eggs by native heteropteran leaf bugs. The eggs were glued onto tobacco leaves that had been treated either with a single synthetic volatile identical to those emitted by attacked plants, or with methyl jasmonate (MeJA) [HN7], a chemical that induces plants to release a blend of volatiles similar to that induced by herbivory (7). Finally, they assessed how many eggs were laid by one of the herbivorous insect species on tobacco plants treated with a single volatile or with MeJA. When tobacco plants were treated with different single synthetic volatiles, herbivores avoided laying their eggs in response to some volatiles and predators ate more of the test prey (glued-on herbivore eggs) in response to others. Application of either MeJA or linalool (a synthetic volatile) induced both effects simultaneously. So, the double-edged defense system of plants can be elicited by either a single volatile or a blend of volatiles.

Plant perfumes, hungry herbivores, and biting bugs.

Pictured is a natural ecosystem in the Great Basin desert of southwestern Utah (6). (1) Wild tobacco plants are attacked by caterpillars of the moth Manduca quinquemaculata. (2) This attack induces the tobacco plants to emit volatile organic compounds that attract natural enemies of the caterpillars such as big-eyed bugs (Geocoris pallens). (3) The airborne volatiles also stop adult M. quinquemaculata moths from laying their eggs on tobacco plant leaves [HN12].

CREDIT: A. KESSLER

The Kessler and Baldwin results strongly support the notion that herbivore-induced plant volatiles not only deter herbivores but also attract predators that act as bodyguards. It is not yet clear whether individual volatiles enable predators to identify the species and abundance of herbivores on a particular plant [but see (8)]. It is also not known why volatiles repel herbivores and whether they convey information about the plant's well-defended state. It is possible that these versatile volatiles alert herbivores to one or more of the following: the plant harbors competitors, has activated its direct defenses, has acquired indirect protection from predators. Finally, it remains unclear whether volatiles promote the reproductive success of the plant that emits them. Kessler and Baldwin estimate that luring predators and repelling herbivores results in about a 90% reduction in the number of herbivorous insect eggs laid on volatile-treated tobacco leaves. Of course, it is not the eggs themselves but rather the insect larvae that induce plants to release volatiles, and so plants will attract predators only after the eggs have hatched. Because one hornworm larva [HN8] is enough to completely defoliate several wild tobacco plants (6), one might ask whether the principal job of volatiles is to reduce herbivory such that the plant is not completely defoliated and is still able to reproduce.

To find out why natural selection favors plants that emit an airborne signal upon attack, a cost-benefit analysis should be undertaken. Such an analysis would monitor not only interactions among plants, herbivores, and their predators, but also those between members of the entire food web [HN9] (5, 9, 10). The reason for this is that herbivore-induced plant volatiles may not only lure predators and repel herbivores, but also may attract competitively superior herbivores or predators that also eat plants (omnivores) or hyperpredators, or hyperparasitoids [HN10] (9). Potentially, volatile emission could cause the plant to incur more damage or to lose its bodyguard protection. Moreover, competing nearby plants may profit from the predators lured by a volatile-releasing plant, saving their own energy for other purposes (10). Because Kessler and Baldwin's experiments were conducted in low-density, pioneer vegetation in the desert, such tests need to be repeated in regions with more diverse, dense vegetation. Also, the time scale of future studies should be longer. Kessler and Baldwin's experiments were probably conducted over too short a period to enable them to observe the full behavioral repertoire of all organisms in the food web and the complete range of interspecific interactions. Indeed, anyone undertaking a critical cost-benefit analysis needs to be aware that apparently beneficial interactions are never foolproof and that their outcome may vary between parasitism at one extreme and mutualism at the other, depending on the conditions [HN11] (11). Nevertheless, Kessler and Baldwin have taken an important first step toward unraveling the nature of direct and indirect plant defense.

HyperNotes Related Resources on the World Wide Web

General Hypernotes

The Ecological Society of America provides educational resources and links to ecological resources on the Internet.

The Google Web Directory provides links to ecology resources.

Nearctica provides links to ecology resources on the Internet.

The Ecology WWW Page, maintained by A. Brach, Missouri Botanical Garden and Harvard University Herberia, is a searchable list of ecology resources on the Internet.

BIOSIS Internet Resource Guides offer a collection of links to ecology Web sites.

The Natural Resources Research Information Pages are maintained by Yu-Fai Leung, Department of Parks, Recreation and Tourism Management, North Carolina State University.

The Virtual Library of Botany is a collection of links to Internet resources maintained by S. Russell, Department of Botany and Microbiology, University of Oklahoma, who also makes available Scott's Botanical Links.

The Plant Pathology Internet Guide, maintained by T. Kraska, Institute for Plant Diseases, University of Bonn, Germany, is an annotated resource guide for plant pathology, applied entomology, and related fields. The entomology section includes links to resources in chemical ecology and predation.

The Department of Cell Biology and Molecular Genetics, University of Maryland, makes available lecture notes for a course on plant biology.

E. Iglich, Biology Department, Western Maryland College, Westminster, offers lecture notes for an ecology course.

J. Blair, Division of Biology, Kansas State University, offers lecture notes for an ecology course.

L. Blumer, Department of Biology, Morehouse College, Atlanta, GA, provides lecture notes for a Web course on the fundamentals of ecology offered by the HBCU/MI Environmental Technology Consortium at Clark Atlanta University and Northern Arizona University.

P. Ganter, Biology Department, Tennessee State University, Nashville, provides lecture notes for an ecology course. Presentations on predation, herbivory and plant defenses, and parasitism are included.

P. Schappert, Section of Integrative Biology, School of Biological Sciences, University of Texas, offers lecture notes for an ecology course. Lecture notes on predator-prey interactions and herbivory are provided.

A. Sharov, Department of Entomology, Virginia Institute of Technology and State University, provides lecture notes for a course on quantitative population ecology. A section on predation and parasitism is included.

L. Higley, Department of Entomology, University of Nebraska, provides lecture notes for a course on insect ecology.

J. Holmes, Axelrod Institute of Ichthyology, University of Guelph, provides lecture notes for a community ecology course at the University of Toronto at Scarborough.

M. Berenbaum, Department of Entomology, and D. Seigler, Department of Plant Biology, University of Illinois, provide lecture outlines for a course on chemical ecology.

H. Bestman, Biology Department, King's University College, Alberta, Canada, offers lecture notes in slide format for a course on the chemistry of ecological relationships.

The Department of Plant Protection Services, Swedish University of Agricultural Sciences at Alnarp, provides a resource page on chemical ecology.

The International Society of Chemical Ecology provides an introduction to the science of chemical ecology.

Chemical Ecology: The Chemistry of Biotic Interaction, edited by T. Eisner and J. Meinwald, is a 1995 book available on the Web from the National Academy Press. Included is a chapter titled “The chemistry of defense: Theory and practice.”

L. Bjostad, Department of Entomology, Colorado State University, makes available student review articles on chemical ecology topics prepared for a course on chemical ecology.

The October 2000 issue of Plant Physiology had a symposium report by D. Cosgrove et al. titled “Plant Signaling 2000: Cross talk among geneticists, physiologists, and ecologists.”

Numbered Hypernotes

1. J. Blair offers a presentation on herbivory for an ecology course. S. Mulkey, Department of Botany, University of Florida, discusses herbivory in lecture notes on plant-animal interactions for an ecology course. J. Holmes provides lecture notes on herbivory for a community ecology course. J. Gowda makes available a paper titled “Herbivory, a continuum from antagonistic to mutualistic relationships,” which was prepared for an animal ecology course offered by the Swedish University of Agricultural Sciences.

2. W. J. Lewis, Insect Biology and Population Management Research Laboratory, USDA Agricultural Research Service, Tifton, GA, includes a section on plant defenses in a presentation titled “Biological control as a component of sustainable agriculture.” L. Higley offers lecture notes on insect-plant relations and plant responses to insects for a course on insect ecology. L. Blumer discusses plant defenses against herbivores, herbivore responses, and examples of the effects of plant-herbivore interactions in lecture notes for a course on the fundamentals of ecology. E. Iglich offers a presentation titled “Plant defense systems: Herbivory, microbial and competition” for a botany course. PEST CABWeb, a presentation of CAB International, provides in its Spotlight features section an introductory overview of insect-plant interactions and induced plant defense; abstracts of journal articles about the subject are provided.

3. Botany online: The Internet Hypertextbook includes a section titled “The secondary metabolism of plants: Secondary defence compounds.” C. van den Boom, Phytochemical Group, Laboratory of Organic Chemistry, Wageningen University and Research Center, Netherlands, offers a presentation on her research titled “Chemical analyses of insect-induced plant volatiles.” The October 1999 issue of Plant Physiology had an article by P. Paré and J. Tumlinson titled “Plant volatiles as a defense against insect herbivores.” The 9 May 1997 issue of Science had a report by H. Alborn et al. titled “An elicitor of plant volatiles from beet armyworm oral secretion.” The USDA Agricultural Research Service issued a news release about this research titled “Scientists identify chemical that triggers plant ‘SOS’ call.” The 1 October 1998 issue of Agricultural Research had an article (made available by Britannica.com) by J. Suszkiw titled “Plants send SOS when caterpillars bite.” The Universisty of California, Davis, issued a 10 June 1999 news release titled “Caterpillars foiled when tomato plants summon parasitic wasps” and a 17 November 2000 news release titled “Plant neighbors transmit airborne warnings.” L. Bjostad makes available a student review paper from the 2000 class on chemical ecology by L. Mannix titled “Relationships among plants, insect herbivores, pathogens, and parasitoids expressed by secondary metabolites” and a paper from the 1996 class by J. McIntyre titled “The role of plants in attracting predators and parasitoids to control herbivore feeding.”

4. A. Kessler and I. Baldwin are in the Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany. A Web page for Baldwin is also available at the Department of Biological Sciences, State University at Buffalo. Kessler's Web site provides some background information about this research.

5. The Desert USA Web site offers a presentation on the Great Basin desert. The Exploring the Great Basin Web site has a section on Utah. The American Southwest Web site provides a map of Utah with links to information about parks and other natural attractions in the state. The Nature Conservancy provides information about the Lytle Preserve in southwestern Utah (which was the field station for the reported research). Maptech provides a topographic map of the southwestern corner of Utah. The Color Landform Atlas of the United States Web site offers a collection of maps of Utah.

6. The USDA Plants Database provides a profile of Nicotiana attenuata. The CalFlora Database provides information about Nicotiana attenuata, as well as links to images from the Digital Library Project. The Digital Atlas of the Vascular Plants of Utah, made available by the College of Natural Resources, Utah State University, shows locations for Nicotiana attenuata in Utah. I. Baldwin offers a slide presentation titled “Nicotiana attenuata: A model system for understanding the molecular basis of ecological interactions.”

7. H. Bestman includes a slide about jasmonic acid and methyl jasmonate in the lecture notes on plant defenses for a course on the chemistry of ecological relationships. P. Kenton, Institute of Biological Sciences, University of Wales, Aberystwyth, UK, offers a presentation titled “Jasmonates and plant defence responses”; a section on jasmonate and the wound response is included. The 7 July 1998 issue of the Proceedings of the National Academy of Sciences had an article by I. Baldwin titled “Jasmonate-induced responses are costly but benefit plants under attack in native populations.” A news release about this research was issued by the Max Planck Society for the Advancement of Science.

8. Featured Creatures, a presentation of the Department of Entomology and Nematology, University of Florida, offers an information page on tobacco and tomato hornworms. The Center for Integrated Pest Management, North Carolina State University, makes available information on hornworms from a publication on insect and related pests of vegetables. The Center for Biology Education, University of Wisconsin, presents Exploring Science as Inquiry Using Manduca sexta, a teachers' manual for using the tobacco hornworm in elementary and secondary schools; information about the Manduca life cycle is provided.

9. The Encyclopædia Britannica article on community ecology has a section on food chains and food webs. Kimball's Biology Pages offers a presentation on food chains and webs. Fundamentals of Physical Geography, a Web text by M. Pidwirny, Department of Geography, Okanagan University College, BC, Canada, provides an introduction to trophic pyramids and food webs in the chapter on biogeography and ecology. J. Blair offers a presentation on food webs for an ecology course. R. Myers, Department of Biology, Dalhousie University, Halifax, NS, Canada, offers lecture notes on food webs for an ecology course.

10. The USDA Whitefly Knowledgebase provides definitions of predator, parasitoid, and hyperparasitoid. Biological Control: A Guide to Natural Enemies in North America, a resource provided by the New York State Agricultural Experiment Station at Cornell University, provides introductions to predators and parasitoids.

11. The Encyclopædia Britannica article on community ecology includes a section on interspecific interactions and the organization of communities with information provided about forms of mutualism and antagonism. J. Pascarella, Biology Department, Valdosta State University, GA, offers lecture notes on types of relations among species for an ecology course.

12. Moths of North America, provided by the Northern Prairie Wildlife Research Center, includes an entry for Manduca quinquemaculata (five-spotted hawkmoth) in the moths of Utah section. The Moths of Southeastern Arizona, presented by B. Walsh, Department of Ecology and Evolutionary Biology, University of Arizona, includes a section on hawkmoths; an image comparing M. quinquemaculata and M. sexta is provided. Cornell's Biological Control Web site provides a section by J. Hagler about Geocoris spp. (Heteroptera: Lygaeidae): Bigeyed Bug. The Integrated Plant Protection Center at Oregon State University offers an introduction to the western big-eyed bug (Geocoris pallens) in a Web presentation titled “Identification and management of major pest and beneficial insects in potato.”

13. M. W. Sabelis, A. Janssen, and M. R. Kant are at the Institute of Biodiversity and Ecosystem Dynamics, University of Amsterdam, Netherlands.

References

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