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The Chemistry of Defense: Theory and Practice MAY R Proc. Natl. Acad. Sci. USA Vol. 92, pp. 2-8, January 1995 Colloquium Paper This paper was presented at a coUoquium entitled "Chemical Ecology: The Chemistry ofBiotic Interaction, " organized by a committee chaired by Jerrold Meinwald and Thomas Eisner, held March 25 and 26, 1994, at the National Academy of Sciences, Washington, DC. The chemistry of defense: Theory and practice MAY R. BERENBAUM Department of Entomology, 320 Morrill Hall, University of Illinois, 505 South Goodwin, Urbana, IL 61801-3795 ABSTRACT Defensive chemicals used by organisms for Unlike primary metabolites, which are practically universal protection against potential consumers are generally products constituents of cells, tissues, and organs, secondary com- ofsecondary metabolism. Such chemicals are characteristic of pounds are generally idiosyncratic in distribution, both taxo- free-living organisms with a limited range of movement or nomically and ontogenetically. Chlorophyll, for example, the limited control over their movements. Despite the fact that principal photosynthetic pigment, is found in virtually all chemical defense is widespread among animals as well as species of angiosperms, in virtually all life stages ofvirtually all plants, the vast majority of theories advanced to account for individuals. In contrast, the furanocoumarins are secondary patterns of allocation of energy and materials to defensive compounds known from only a handful of angiosperm families chemistry derive exclusively from studies of plant-herbivore (5). Within a species (e.g., Pastinaca sativa), there is variability interactions. Many such theories place an undue emphasis on in furanocoumarin content and composition among popula- primary physiological processes that are unique to plants tions (6, 7); within an individual, there is variation among body (e.g., photosynthesis), rendering such theories limited in their parts during any particular life stage (8) and temporal variation utility or predictive power. The general failure of any single in the appearance of these compounds over the course of all-encompassing theory to gain acceptance to date may development (9); there are even differences in the content of indicate that such a theory might not be a biologically realistic individual seeds, depending upon their location in an umbel expectation. In lieu of refining theory, focusing attention on (10), fertilization history (11), and their position within the the genetic and biochemical mechanisms that underlie chem- schizocarp (12). ical defense allocation is likely to provide greater insights into Secondary chemicals are by definition taxonomically re- understanding patterns across taxa. In particular, generali- stricted in distribution, yet despite this fact there are patterns zations derived from understanding such mechanisms in in production and allocation that transcend taxa (13). Their natural systems have immediate applications in altering pat- presence in an organism is generally characterized by special- terns ofhuman use ofnatural and synthetic chemicals for pest ized synthesis, transport, or storage. Levels of abundance are control. subject to environmental or developmental regulation and, unlike primary constituents, which may be present in virtually Irrespective of taxon, the chemicals that play a prominent role all cells of an organism, chemical defenses are typically com- in interspecific interactions are rarely the same substances partmentalized, even in those cases in which the chemicals are used by an organism to meet the daily challenges of living, such acquired exogenously, as when sequestered from a food as respiration, digestion, excretion, or, in the case of plants, source. There often exists a system for external discharge, photosynthesis. They are, in both plants and animals, of "a delivery, or activation, not only as a means of ensuring contact more secondary character" [to borrow a phrase from Czapek with a potential consumer but also as a means of avoiding (1)]. These secondary compounds are generally derived from autotoxicity until a confrontation arises; and of course these metabolites that do participate in primary physiological pro- compounds are almost invariably, by virtue of structure, cesses. In plants, for example, secondary compounds such as chemically reactive (e.g., able to be taken up by a living system, alkaloids, coumarins, cyanogenic glycosides, and glucosino- to interact with a receptor or molecular target, and to effect a lates derive from amino acid; tricarboxylic acid cycle constit- change in the structure of the molecular target). The remark- uents are involved in the formation of polyacetylenes and able convergence of structural types in plant and insect polyphenols; glucose, aliphatic acids and other "primordial secondary metabolites is at least suggestive that the processes molecules" (2) play a role not only in primary metabolism but leading to biological activity in both groups share certain in secondary metabolism as well. In insects, many defensive fundamental similarities (14). secretions are derived from the same amino acids used to Secondary chemicals can be said to be defensive in function construct proteins [among them, quinones in many beetles and only if they protect their producers from the life-threatening cockroaches derive from tyrosine, formic acid in ants from activities of another organism. Distinguishing between offen- serine, isobutyric acid in swallowtail caterpillars from isoleu- sive and defensive use of chemicals is difficult, and present cine and valine, and alkyl sulfides in ants from methionine (3, terminology does little to assist in making that distinction. The 4)]. Presumably, secondary compounds are physiologically term "allomone" is frequently used synonymouslywith "chem- active in nonconspecific organisms precisely because of their ical defense," yet allomones are not necessarily defensive in secondary nature; it is to be expected that most organisms function. An allomone has been defined as a chemical sub- possess effective means for metabolizing, shunting around, or stance beneficial to its producer and detrimental to its recip- otherwise processing primary metabolites and it is the unusual ient (15), so chemicals used by a predator to lure prey (16) are chemical that circumvents these mechanisms to cause toxicity. rightly regarded as allomonal but are not obviously defensive. By the same token, chemicals that reduce competition for The publication costs of this article were defrayed in part by page charge limited resources, clearly beneficial to the producer, may be payment. This article must therefore be hereby marked "advertisement" in defensive of those resources but are not necessarily defensive accordance with 18 U.S.C. §1734 solely to indicate this fact. in the life of the organism producing them. Allelopathic 2 Downloaded by guest on September 26, 2021 Colloquium Paper: Berenbaum Proc. NatL Acad Sci USA 92 (1995) 3 compounds produced by a plant species may increase fitness being consumed. Large vertebrates, by virtue of size, speed, of a plant by preempting a resource, such as water or soil and strength, often occupy that position in both terrestrial and nitrogen, that might otherwise be exploited by other plants aquatic ecosystems (carnivores and odontocetes, for example). (17), but in the sense that such compounds can kill potential Chemically defended mammals include skunks and the duck- competitors (such as nonconspecific seedlings) they are used billed platypus, both opportunistic scavengers (32). Among in an offensive fashion, as for range expansion at the expense birds, chemical defense has been demonstrated to date only in of another organism. the pitohui (25), which feeds on leaf litter invertebrates (J. A defensive chemical, then, is a substance produced in order Daly; ref. 79), but likely exists in the conspicuously colored to reduce the risk of bodily harm. As such, most are poisons- female hoopoe, which "has a strongly repulsive musty smell defined as "any agent which, introduced (especially in small that emanates from her preen gland, and is believed to have a amount) into an organism, may chemically produce an inju- protective function like attar of skunk" (33). Hoopoes are also rious or deadly effect" (18). This rather restrictive definition opportunistic feeders that consume debris along with insects may not be universally embraced by chemical ecologists. On and other invertebrates. It is somewhat surprising that chem- one hand, the definition implies an interaction with another ical defenses are not more frequently encountered among organism and, particularly with respect to plants, secondary small birds, but the absence of reports may be due to the compounds may fulfill many functions in the life of the tendency of investigators to assume conspicuous plumage producer organism other than producing injurious or deadly results from sexual selection, rather than aposematism and effects on other organisms (19, 20). Many plant secondary distastefulness (25). compounds, for example, are inducible by UV light and In contrast with fast, strong predators, organisms with a presumably serve to protect (or "defend") plants from dam- limited range of movement, or limited control over their aging effects of UV exposure (21); by no stretch of the movements-those that cannot run away from potential pred- imagination can such compounds be considered poisons, since ators-are well represented among the chemically defended they exert no injurious effects on the damaging
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