In search of allelopathy: an eco-historical view of the investigation of chemical inhibition in California coastal sage scrub and chamise chaparral

Journal of the Torrey Botanical Society, Oct-Dec 2004 by Halsey, Richard W

RICHARD W. HALSEY (Southern California Chaparral Field Institute, P.O. Box 545, Escondido, CA 92033). In search of allelopathy: an eco-historical view of the investigation of chemical inhibition in California coastal sage scrub and chamise chaparral. J. Torrey Bot. Soc. 131. 343-367. 2004.-Allelopathy between plants, whereby one species influences another by chemical means, has been speculated upon since the Greeks. During the second half of the twentieth century, southern California was the focal point of allelopathic research by several influential investigators. Frits Went suggested Encelia farinosa, a common desert shrub, inhibited annuals from growing under its canopy by chemical inhibition. Reed Gray and James Bonner conducted further investigations. Cornelius H. Muller questioned the allelopathic explanation for Encelia, but later felt chemical inhibition was the cause for vegetation patterns found in both southern Californian coastal sage scrub, primarily around Salvia leucophylla and Artemisia californica, and Adenostoma fasciculatum (chamise) chaparral. Various investigators challenged Muller's conclusions, but Muller remained convinced allelopathy was an important ecological variable in southern California's shrublands. Muller's passionate belief in his scientific models led him to ignore contrary evidence, yet his dedication to science and the education of his students inspired many. Allelopathy remains a controversial topic today despite hundreds of investigations because of the difficulty in isolating all the possible variables affecting plant growth.

Key words: allelopathy, seed dormancy, coastal sage scrub, chamise chaparral, bare zone, chamise-fire cycle, multiple working hypotheses, bioassay.

Plants and microorganisms produce a variety of chemicals, as byproducts of their metabolic processes, capable of either inhibiting or encouraging the biological actions of other organisms, including their own species. Understanding allelopathy is an attractive research goal, especially when considering its potential application to the commercial production of natural herbicides.

The notion of plants influencing their neighbors has been around since the ancient Greeks. By the mid 1800's, the hypothesis that plants influenced each other by chemical means became widely accepted, especially after the work of French botanist, A.P. DeCandolle in 1832. Hans Molisch, an Austrian plant physiologist, introduced the term "allelopathy" to identify the process in 1937. The word is based on the Greek allelo meaning "one another", and path for "suffering" or "disease." Molisch (1937) applied a broader definition by including both negative as well as positive impacts of chemical interactions occurring between plants, as well as microorganisms. However, by the time Molisch coined the word, the idea had lost considerable scientific support in favor of a different hypothesis explaining the causes of vegetation patterns; the depletion of soil nutrients by competition. Allelopathy became a troublesome variable for the soil depletion model because it created an intolerable degree of uncertainty. It is difficult enough to develop conclusions about plant competition based on soil nutrients without worrying about some unknown chemical interaction influencing experimental results. Consequently, the notion of chemical influence was generally ignored. Yet the subject continued to be of interest to many and was given a new life in the deserts of southern California.

Desert Symbiosis. During field trips into southern California's deserts, Caltech botanist Frits Went noticed there was a strong tendency for annual plants to locate themselves under or near larger, woody species. For desert wildflowers, he felt physical factors, such as shading or soil conditions, did not adequately account for the germination and vegetation patterns he observed. Went decided to quantify his ideas in 1942 with a study of two small shrubs. One, the dusty-gray Ambrosia dumosa (burro-weed) with low growing, brushy stems, harbored an abundant array of annuals under its shady canopy. The other, Encelia farinosa (brittlebush), was an erect, sparsely stemmed shrub with little more than bare ground below. If Encelia shrubs were dead, however, the frequency of annual growth beneath its skeletal frame increased dramatically. In discussing his observations, Went (1942) wrote,

. . . there is a specific effect of shrubs, which must be ascribed to specific materials given off by them. These materials seem to be produced especially by the living shrub and they determine the specific occurrence of definite annuals. No guess as to the nature of these materials will be given; this can safely be postponed until experimental evidence is available.

The Substance. In 1948 Went's investigation attracted the interest of plant physiologist James Bonner, a Caltech colleague of Went. Bonner pursued his interest by accepting a student's research proposal to investigate the chemical cause of Encelia's inhibiting qualities. Working in Bonner's lab, Reed Gray analyzed the plant's roots, leaves and chemical extracts in an effort to identify the toxic principle's source.