Citation Records Show Plant Herbivory Taking Root As Hot Research Topic

Research Topic Editor's Note: In its continuing analysis of the citation record of ecology and environmental sciences, the newsletter Science Watch recently took a retrospective look at the rankings of papers in the field. Using a customized database--covering the years 1981 to 1993--of the most cited papers in the discipline, Peter D. Moore, a reader in ecology and chairman of human and environmental sciences in the Division of Life Sciences, King's College, London, looked for hot areas of ecological research. His analysis revealed that the study of plant herbivory was one of the field's most important topics over the last 15 years. In fact, some papers in a list of the 10 most cited herbivory articles during the 14-year period covered by the database are still garnering a substantial number of citations. Following is Moore's April 1995 Science Watch report. The article--with an update on the numbers of citations each of the 10 papers has received through April 1995--is presented here with permission of Science Watch and the Philadelphia-based Institute for Scientific Information (ISI). Some papers leave indelible marks on the literature and on the development of their subject, but they can be identified only in retrospect. If we examine the citation ranking of ecological and environmental papers over the past 14 years, one of the most prominent topics to emerge, perhaps surprisingly, is the response of plants to herbivory--how they deal with what's eating them, so to speak. The explosive development of this field can be traced back to the 1959 paper by G.S. Fraenkel (Science, 129:1466) in which the possibility of chemical defenses in plants was examined. The subject, however, began to take off only during the 1970s and 1980s. As a general rule of thumb, about 10 percent of terrestrial plant production is consumed by herbivores, so selective pressures are strong in directing plant evolution toward resisting them. Morphological modifications associated with grazing resistance, such as spines, are the most evident response, but the more subtle and less visually evident development of chemical compounds that render plant tissue unpalatable or toxic to herbivores are now known to be widely distributed in the plant kingdom. One fairly simple observation concerning the growth of vegetation is that when the going is tough, plants grow more slowly. Perhaps less obvious, however, is that resource-limited plants also expend more of their energy in deterring herbivores. The most highly cited and therefore, arguably, the most influential paper related to herbivory over the last 14 years is by P.D. Coley, J.P. Bryant, and F.S. Chapin (1985, paper No. 1). This report sets out the principle that environmental stress in the form of low light intensity, infertile soil, or drought is associated with those plants that are relatively rich in the compounds that deter grazers. But this generally positive association between stress and chemical defense applies to plant species exposed to such stresses over evolutionary periods. A species that is not specifically stress-adapted in this sense, but that is still subjected to drought or physical damage over nonevolutionary periods, may actually prove more attractive to herbivores (T.C.R. White, 1984, paper No. 5). Tannins are one group of plant compounds that have received much attention (W.V. Zucker, 1983, paper No. 4). These compounds delay decomposition when plant tissue falls to the ground, but they are also involved in the deterrence of herbivores. Examining the chemical structure of tannins, Zucker found that condensed tannins are able to complex with such compounds as starch and nucleic acids. He proposed that they are tucked away safely in complexes with the cellulose and pectins of the plant cell wall where they offer defense against microbial attack. Their unpalatability to microbes also slows plant decomposition in the soil, thus ensuring a better regulated supply of regenerated nutrients to the growing plant. The function of tannins is not, therefore, primarily one of herbivore deterrence. Hydrolyzable tannins, on the other hand, have high specificity in attaching themselves to proteins, and are thus potentially ideal in operating against herbivore digestion. The structure of this class of tannins, Zucker claims, is related to its function. Tannins have no evident physiological role apart from these protective ones, so it should be possible to test their defensive potential by observing whether a plant under attack by herbivores stocks up on its chemical defenses. It is also important that any work on tannins as a plant protector should use assay techniques that permit the separation of different types of tannins (J.S. Martin and M.M. Martin, 1982, paper No. 9). In a study of defoliation of red oak by gypsy moth larvae in the United States, J.C. Schultz and I.T. Baldwin (1982, paper No. 7) showed that oaks had a significant buildup of both condensed and hydrolyzable tannins when compared with protected, undamaged branches over the same period. So the idea that tannins are defense compounds is upheld, although the fact that both types of tannin increased might be interpreted as a contradiction of Zucker's structure-function hypothesis. But damaged cells would be subject to microbial attack, so production of condensed tannins in response to herbivory would still have a selective advantage. There is, of course, a far simpler remedy for a plant when attacked by an herbivore--just grow faster. This option was formally set out by S.J. McNaughton (1983, paper No. 8), who proposed that some plants not only may be able to compensate for biomass lost during grazing, but also may actually be stimulated into faster growth by being nibbled. This does, of course, depend upon the extent of initial defoliation and also on the occurrence of a subsequent recovery period free from further grazing. The precise mechanism of the stimulation is unclear. It could be explained by a range of factors, such as better light penetration to remaining leaves or the production of such hormones as cytokinins, which promote renewed growth. The fact that some plants recover from grazing much more effectively than others could be explained in terms of their respective physiological responses. This has been tested in two species of bunchgrass by M.M. Caldwell and colleagues (1981, paper No. 6). They found that the grazing-tolerant species of bunchgrass Agropyron desertiorum switched its resource allocation from roots to shoots following defoliation, thus recovering more quickly than the closely related species A. spicatum, which failed to adjust to the new conditions and just went on producing roots. Although the plants concerned may not enjoy the experience, grazing can prove beneficial to the entire ecological community, in terms of higher energy turnover and elevated biological diversity. In an experiment by G.A. Lamberti and V.H. Resh (1983, paper No. 10), for example, herbivorous caddisfly larvae were excluded from their diatom-dominated algal food source. As a consequence, the biomass of algae rose, but the turnover rate decreased. Grazing actually created conditions of higher primary productivity in which a larger biomass of animal consumers can be supported. From this array of keystone papers, it can be appreciated that the study of herbivory has implications for many areas of ecology, both theoretical and practical, ranging from coevolution to community structure; from resource allocation in competitive interactions to the botanical equivalent of chemical warfare. Undoubtedly, it is the wide potential impact of these findings within this field that has led to its emergence from relative obscurity to occupy a position of high influence in modern ecological thinking. THE 10 MOST CITED PAPERS IN PLANT HERBIVORY, 1981 TO 1993 Rank Paper Citations Citations through 1993 through April 1995 1 P.D. Coley, J.P. Bryant, F.S. Chapin, 321 391 "Resource availability and plant antiherbivore defense," Science, 230: 895-9, 1985. [University of Utah] 2 J.P. Bryant, F.S. Chapin, D.R. Klein, 224 282 "Carbon nutrient balance of boreal plants in relation to vertebrate herbivory," Oikos, 40:357-68, 1983. [University of Alaska, Fairbanks] 3 P.D. Coley, "Herbivory and defensive 220 253 characteristics of tree species in a lowland tropical forest," Ecological Monographs, 53:209-33, 1983.[University of Utah] 4 W.V. Zucker, "Tannins. Does structure 183 195 determine function: an ecological perspective," American Naturalist, 121: 335-65, 1983. [Northern ArizonaUniversity] 5 T.C.R. White, "The abundance of 181 202 invertebrate herbivores in relation to the availability of nitrogen in stressed food plants," Oecologia, 63:90-105, 1984.[Riverina College, Wagga Wagga, Australia] 6 M.M. Caldwell, J.H. Richards, D.A. Johnson, 148 167 R.S. Nowak, R.S. Dzurec,"Coping with herbivory: Photosynthetic capacity and resource allocation intwo semiarid Agropyron bunchgrasses," Oecologia, 50:14-24, 1981. [Utah State University] 7 J.C. Shultz, I.T. Baldwin, "Oak leaf quality 148 158 declines in response to defoliation by gypsy moth larvae," Science, 217:149-50, 1982. [Dartmouth College] 8 S.J. McNaughton, "Compensatory plant growth 142 161 as a response to defoliation by gypsy moth larvae," Oikos, 40:329-36, 1983. [Syracuse University] 9 J.S. Martin, M.M. Martin, "Tannin assays 116 123 in ecological studies: Lack of correlation between phenolics, proanthocyanidins and protein-precipitating constituents in mature foliage of six oak species," Oecologia, 54:205-11, 1982. [University of Michigan] 10 G.A. Lamberti, V.H. Resh, "Stream 112 118 periphyton and insect herbivores: an experimental study of grazing by a caddisfly population," Ecology, 64: 1124-35,1983. [University of California, Berkeley] Source: ISI's High-Impact Papers, 1981-93; Science Citation Index (The Scientist, Vol:9, #13, pg.12, June 26, 1995) (Copyright, The Scientist, Inc.)

Citation Records Show Plant Herbivory Taking Root As Hot Research Topic

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